Abstract
Salinization is one of the main global environmental issues of the Anthropocene with various consequences for aquatic ecosystems. To understand diatom ecology and evolution from this perspective without knowing the impact of salinity on their physiological and molecular mechanisms is unimaginable. For this reason, we collected the existing knowledge about the intracellular and morphological changes of diatoms induced by salinity. The available studies revealed that salt stress can significantly affect, among others, their photosynthetic activities, pigment contents, growth rate, metabolism, and toxin synthesis. Acclimation capability of diatoms is apparent: they can adjust turgor pressure and ion homeostasis and produce compatible solutes for osmoprotection applying a number of biochemical pathways and complementary mechanisms. Morphological changes like shape resistance, post-auxospore formation, and several micro- and nano-sized sometimes species-specific variations can also be explained by the increasing salinity. Furthermore, abnormal forms indicate the extreme and complex effect of salinity and collateral stress factors. Their salinity tolerance threshold is species specific, which can be exploited by biotechnology. According to studies collected for this review, it is obvious that diatoms have various phenotypic responses to salinity; however, knowledge about their molecular background and long-term adaptation of the species are completely missing.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Though even the ancient civilizations experienced the phenomenon of salinization of aquatic ecosystems (Jacobsen & Adams, 1958), it had been considered as a local environmental problem up to the end of the twentieth century (e.g., Kirst, 1989). However, and quite recently, it has grown into a global problem. Natural processes can form saline inland surface waters (known as primary salinization, e.g., Rengasamy, 2006; Herbert et al., 2015), besides, anthropogenic activities such as mining, fertilizers, agricultural, and industrial wastewaters and climate change (Bąk et al., 2020; Liu et al., 2020) contribute considerably to enhancing the salinity of freshwaters (secondary salinization). Since many organisms are glycophytes (e.g., Sudhir & Murthy, 2004; Gupta & Huang, 2014), salinity became a strong evolutionary pressure (Latta et al., 2012) and, being one of the most important environmental constraints, it threatens aquatic biota and indirectly ecosystem services provided by them (Cunillera-Montcusí et al., 2022). Despite the recently increasing scientific interest in salinization (Fig. 1), a number of knowledge gaps exist (Cunillera-Montcusí et al., 2022), which would be keys for understanding and predicting its consequences for aquatic ecosystems, society, and economy.
Number of publications focusing on salinization of aquatic ecosystems on the basis of Web of Science database (searching for “salinization in aquatic ecosystems” at June 13, 2022) and its trend (black line)
Depending on qualitative and quantitative changes in salts, aquatic organisms can suffer from osmotic shock in different ways. Therefore, these substances can have different toxicities on the biota. Despite, in salinity regulation and legislation conductivity, thresholds are determined only for irrigation and drinking water, while thresholds which can be lethal for aquatic organisms are generally missing from these standards (Kunz et al., 2013; Cañedo-Argüelles et al., 2016; Schuler et al., 2019) or they are inadequate for their protection (Hintz et al., 2022).
In unfavorable circumstances organisms try to survive, regulate, and maintain their physiological integrity. Salt stress, both osmotic and ionic, influences several physiological processes (Sudhir & Murthy, 2004; Parida & Das, 2005; Gupta & Huang, 2014). Phenotypic alterations, which represent considerable costs for species (Coldsnow et al., 2017), are the basis of and stand behind the changes observed at community and higher levels. Biota are able to live within a certain degree of salinity changes, but different types of organisms can cope with salt stress in different ways (Erdmann & Hagemann, 2001; Ma et al., 2010). Physiological acclimation of aquatic organisms to salts has attracted considerable attention from the second half of the twentieth century, and some reviews were published in this topic over this time, including higher plants (Karsten, 2012; Kumar et al., 2014), animals (Kinne, 1966; Larsen et al., 2014; Pourmozaffar et al., 2020), bacteria (da Costa et al., 1998; Ma et al., 2010), algae (Kirst, 1989), and cyanobacteria (Erdmann & Hagemann, 2001). But none dealt specifically with diatoms, they were only mentioned marginally or in combination with other algae without specific details (in Kirst, 1989; Bisson & Kirst, 1995; Hagemann, 2016). However, this taxonomically separated algal group is among the most successful organisms from ecological and evolutionary point of view. Their silica cell wall and their cell functions are clearly different from other eukaryotic algae (Wilhelm et al., 2006), which assume their distinct phenotypic responses (intracellular and morphological changes) to salinization.
Studies of osmotic stress on diatoms date back to the 1970’s (Schobert, 1974; Liu & Hellebust, 1976). These researches were sporadic and were focused only on few species. Detailed and comprehensive study about the physiological processes and acclimation strategies of diatoms as a main algal group of aquatic ecosystems have been lacking, despite their huge importance, for instance, in global primary production (Malviya et al., 2016) and nutrient and biogeochemical cycles (Struyf et al., 2009; Tréguer et al., 2018; Seckbach & Gordon, 2019). Furthermore, their salt acclimation properties can be also interesting for other reasons, since using their salt resistance strategy diatoms can open possibilities for their useful and efficient biotechnological applications (Seckbach & Gordon, 2019).
Therefore, this review is conducted to collect and summarize present ecophysiological knowledge on diatoms, the possible effects of salinity on diatoms at cellular and intracellular level, their potential strategies against osmotic pressure, their tolerance to different ion concentrations, and their applicability in the field of biotechnology. (Diatom species mentioned in this review are collected in Supplement 1 with their authors and currently accepted names.)
Intracellular response
Changes in salinity can directly and indirectly affect photosynthetic organisms (Kirst, 1989; Hasegawa et al., 2000; Sudhir & Murthy, 2004; Parida & Das, 2005; Gupta & Huang, 2014; Hasanuzzaman & Tanveer, 2020), including diatoms by causing osmotic and salt stress. These effects can be expressed on physiological (e.g., photosynthesis, growth rate), biochemical (e.g., ion regulation, induction of enzymes), and molecular levels (e.g., gene expression) (Kirst, 1989; Munns, 2002; Parida & Das, 2005).
Depending on the salt concentration, the photosynthetic electron transport activities, respiration rate, and photosynthetic pigment content can change similarly to growth and reproduction rates (see examples in Brand, 1984). Salinity affects diatom protein synthesis, lipid, and fatty acid metabolism leading changes in membrane instability and permeability and furthermore can affect biosilification (detailed in the chapter of “Morphological response of diatoms”) and nutrient dynamics reviewed by Saros & Fritz (2000a). Moreover, salinity can induce production of toxins (e.g., domoic acid; Lelong et al., 2012) and reactive oxygen species (ROS), of which the latter can lead to changes in various cellular components, such as proteins, lipids, and fatty acids (e.g., Mallick & Mohn, 2000). Moreover, it can alter the movement and the cell size of diatoms (Mitra et al., 2012). Table 1 summarizes the observed effects of salinity on diatoms.
Organisms can respond to increasing salinity by acclimation or adaptation (MacIntyre et al., 2002) to resist or survive salt stress (Hasegawa et al., 2000; Parida & Das, 2005; Gupta & Huang, 2014; Khan et al., 2020). During the adaptation irreversible change of genotype occurs among the generations leading evolutionary consequences (Orr, 2005), while acclimation means intra-generational quick changes, where cellular compartments and process change (Horowitz, 2001; MacIntyre et al., 2002). Osmoacclimation is a reversible biochemical, biophysical and physiological modification in cellular structure and function to osmotic stress (Reed, 1984). It is generally divided into three different main (restoration of the turgor and cell volume, restoration of ion homeostasis and osmotic adjustment) and several complementary processes (Kirst, 1989; Erdmann & Hegemann, 2001) (Fig. 2). Response to salinity changes is species- (McLachlan, 1961; Šolić et al., 1994; Clavero et al., 2000; Thessen et al., 2005; Petrou & Ralph, 2011) or even strain specific (Balzano et al., 2011; Glaser & Karsten, 2020). These differences contribute to their optimal fitness, influence competitive interactions, determine the potential magnitude and rate of selection, therefore, influence the ecological success and evolutionary longevity (Godhe & Rynearson, 2016).
Schematic figure of intracellular processes in diatoms induced by salinity
Restoration of the turgor and cell volume
Diatoms can sustain or adjust turgor pressure in only 5–10 s due to their perforated valves and the elastic girdle band. In contrast to the so-called soft algae, which can change their cell volume as a result of the entry or loss of water (Bisson & Kirst, 1995). Diatoms are capable to change the membrane permeability and fluidity (Erdmann & Hegemann, 2001; de Castro Araújo & Garcia, 2005; Parida & Das, 2005; Chen et al., 2008; Cheng et al., 2014; Indrayani et al., 2020; Jaramillo-Madrid et al., 2020) and regulate the water flux via alteration of lipid, protein, sterol, or fatty acid content of membranes (like Nitzschia laevis, Chen et al., 2008; Thalassiosira pseudonana, Phaeodactylum tricornutum, Chaetoceros muelleri, Jaramillo-Madrid et al., 2020; Amphora sp. Indrayani et al., 2020) (Table 1; Fig. 2). Water channels could facilitate water movement across the membranes, but this kind of equipment has not been observed in diatoms unlike in some other algae (Chara sp., Henzler & Steudle, 1995; Synechococcus sp. Allakhverdiev et al., 2000) and in higher plants (Weig et al., 1997).
Restoration of ion homeostasis
In general, the unbalanced cellular ion homeostasis can be controlled by uptake/export of ions and changes in the permeability of the cell membrane (Erdmann & Hegemann, 2001). Diatoms are able to maintain their ion homeostasis by active transport of Cl−, Na+, and K+ ions out from the cell or into the vacuole through antiporter and transporter systems or by passive transport through membrane protein channels (Boyer, 1976; Fujii et al., 1995; Krell et al., 2008; Cheng et al., 2014; Nakov et al., 2020). Moreover, salt-induced alteration in membrane permeability and fluidity can regulate the restoration process of ion homeostasis, since a rigid membranes can lead to a moderately active Na+/H+ antiporter system (Allakhverdiev et al., 1999). However, accumulation of these ions in high amounts (~ 100 mM) is disadvantageous for diatoms, since they may inhibit activities of many enzymatic processes (Kirst, 1989) (Fig. 2).
Osmotic adjustment
Osmotic adjustment is a slow process which lasts for 40–120 min in microalgae during which osmoprotection is induced by accumulation of compatible, osmotically active substances as low molecular weight organic molecules, and stress proteins occur until a new steady state is achieved (Kirst, 1989; Erdmann & Hegemann, 2001). Diatoms can produce compatible osmolytes; up-to-date 19 osmolytes are detected in them (Table 1). However, there might be other possible ones (e.g., dulcitol, trehalose), which have been already known in other algae and cyanobacteria (Erdmann & Hegemann, 2001). These compatible solutes can be arranged on the basis of the energetic budget necessary for the biosynthesis and by the degree of their solubility (Oren, 1999; Erdmann & Hegemann, 2001). Accordingly, the highest salt tolerance can be achieved by accumulation of glycerol. Its energetic cost is only 30 ATP equivalent per molecule and it is the most hydrophilic compound. The lowest tolerance level is represented by accumulating of disaccharides, for example, trehalose and sucrose, for which the energetic cost is 109 ATP equivalent per molecule. The most widely compatible solute used by diatoms is proline needing 62 ATP equivalent per molecule, which could be important in short-term acclimation, but might not be maintained in the long term (Nakov et al., 2020).
In order to expand their salinity tolerance, diatoms can produce compatible solutes having distinct protective properties (Kirst, 1996; Van Bergeijk et al., 2003; Scholz & Liebezeit, 2012) and can utilize different mechanisms with the same osmoregulators (Kauss, 1978; Krell et al., 2008; Cheng et al., 2014). For instance, the biochemical pathway seems to be more important than the accumulation of osmolytes themselves, which, in turn, could also explain the accumulation of different osmoprotectants (Garza‐Sánchez et al., 2009; Scholz & Liebezeit, 2012). In proline accumulation, these differences can be achieved by the less energy-consuming ornithine pathway compared to glutamate route (like Achnanthes delicatula, Fragilariopsis cylindrus, Nitzschia constricta) or involving a new alternative pathway such as the urea cycle as it was shown in case of Thalassiosira pseudonana and Phaeodactylum tricornutum (Armbrust et al., 2004; Krell et al., 2007, 2008; Allen et al., 2011; Scholz & Liebezeit, 2012). Furthermore, osmolytes are often insufficient alone for osmotic acclimation (Kauss, 1978; Hellebust, 1985) as they are coordinated and changed depending on the different ion species (Kirst, 1989).
Additionally, the synthesis of a single osmoprotectant such as dimethylsulfoniopropionate (DMSP) is too slow for short-term acclimation, but their uptake from the surrounding environment (e.g., after release from algal cells due to loss of membrane integrity; Lyon et al., 2016) is a relatively fast process to adjust osmotic pressure. This extracellular uptake is possible by use of their transport proteins, which is, otherwise, more typical for heterotrophic bacteria than phototrophic organisms (Erdmann & Hegemann, 2001). Moreover, they have a wide variety of transport systems, through which osmolytes may be facilitated by the adjustment process (Tuchman, 1996; Welsh, 2000) of DMSP (Van Bergeijk et al., 2003), proline (Schobert, 1980), glycine betaine (Keller et al., 1999), and amino acids (Admiraal et al., 1984; Nilsson & Sundbäck, 1996) (Fig. 2.).
Complementary mechanisms
Beside the main processes, diatoms have several secondary mechanisms that supplement their success in acclimation (Erdmann & Hegemann, 2001) (Fig. 2). Diatoms can produce extracellular polymeric substances and regulate their content and composition in order to reduce the negative impacts of osmotic and salt stress (Underwood & Aslam, 2015). Through this, they can, e.g., retain water, restrict the diffusion of anions, and modify their motility (Allan et al., 1972; Hoagland et al., 1993; Underwood & Paterson, 2003; Underwood et al., 2004; Abdullahi et al., 2006; Aslam et al., 2012; Steele et al., 2014). They can regulate their antioxidants via enhancing the production of carotenoids, xanthophylls, cyclophilins, and DMSP (Sunda et al., 2002; Theseira et al., 2020), in order to avoid ROS formation and prevent cell damage (Krell, 2006; Janknegt et al., 2008; Krell et al., 2008; Markina & Aizdaicher, 2016; Ayache et al., 2020). In addition, they can increase enzymatic activity of, e.g., superoxide dismutase, peroxiredoxin, and thioredoxin to detoxify ROS (Rijstenbil, 2003; Krell et al., 2008; Roncarati et al., 2008). Since all of the mentioned acclimation strategies need extra energy, diatoms can vary the adenosine levels of the cells which support the cellular energy charge (Prestegard et al., 2014) or accumulate lipids in order to store energy and carbon (Cheng et al., 2014; Ishika et al., 2018; Navarro et al., 2021).
The process of salt response is related to the expression of various genes (e.g., Munns, 2002; Parida & Das, 2005), since genes are responsible for encoding salt stress proteins or for upregulation/downregulation of RNA (Parida & Das, 2005). Nevertheless, regarding diatoms, small amount of molecular-based approaches (mRNA sequencing, gene knockdown, and whole-genome shotgun) have been applied to explain their salt tolerance mechanisms (Ambrust et al., 2004; Krell, 2006; Krell et al., 2008, Allen et al., 2011; Bussard et al., 2017; Pinseel et al., 2022). These processes seem to be allied to generally multigenic traits and they are likely to act additively and synergistically as in higher plants (Parida & Das, 2005). Based on a genetic study, besides osmolyte production and ion homeostasis, other processes can also play important roles in the salt tolerance mechanisms of diatoms, such as ROS scavenging and protein degradation (Krell et al., 2008). Thus, the simultaneous metabolic processes seem to be also crucial in salt acclimation of diatoms like in higher plants (Parida & Das, 2005). During the acclimation, diatoms may reduce their transcription costs when they decrease the expressions of some genes and/or they change metabolic pathways to ensure the energy demand of their intracellular ion homeostasis (Haimovich‐Dayan et al., 2013; Bussard et al., 2017). Furthermore, under high salt content clear intraspecific sequence differences (in Cylindrotheca closterium) can be observed and this differentiation can speed up the speciation processes (Balzano et al., 2011; Glaser & Karsten, 2020).
In summary, beyond the salinity limits, algal growth may be sacrificed to maintain osmotic adjustments for guaranteeing survival (Kirst, 1989). It is obvious that diatoms can apply many salt tolerance mechanisms. However, there are other possible strategies like role of stress hormones (Stirk et al., 2018), Ca2+ regulation (Bisson & Kirst, 1995), water channels (Allakhverdiev et al., 2000), and supplying extra energy by alternative pathways in photosynthesis (Satoh et al., 1983, Erdmann & Hegemann, 2001), which are known for other algae but still not for diatoms. Furthermore, since other physical and chemical parameters, such as nutrient enrichment (Saros & Fritz, 2000a), temperature (Lengyel et al., 2020), or different ionic compositions (Ziemann, 1967), may expand the tolerance range and their combined investigation has been an urgent need.
Morphological response of diatoms
Diatom species can adapt well to constraints, like salinity (Leterme et al., 2010), which induces several phenotypic changes of diatoms. This variation of morphological features explained by salinity was demonstrated already at the beginning of the twentieth century by Richter (1909) for Nitzschia putrida. The phenotypic changes of diatoms can be conspicuous in light microscopy or can be discovered only on nanoscales. In some cases, diatoms maintain their normal outline and in other cases they change it completely. This morphological plasticity is determined by the gene pool diversity (Cox, 2006) and can explain their ecological success in different, sometimes extreme environments (Leterme et al., 2013). Vice versa, these altered morphological features can indicate the changes of environmental drivers (Trobajo et al., 2004).
Shape resistance
Specific gravity of silica cell walls (2.4 g cm−3) is more than twice as high as that of the protoplasm. Therefore, diatoms are too heavy to remain in suspension in waterbody without easily adjustable mechanisms. For minimizing sedimentary loss of species the following evolutionary mechanisms are available: to decrease size, to decrease specific gravity, and to increase form resistance (Naselli-Flores et al., 2021).
From the point of view of shape resistance, presence of Chaetoceros, a primarily marine genus, with only few species adapted to inhabit continental saline waters, is especially interesting. Its species exploit almost all evolutionary mechanisms to remain entrained in the euphotic layers. Cells are small, weakly silicified, and contain lipids as storage materials (Miller et al., 2014) (Fig. 3.) making the cells relatively light compared to other diatoms. Additionally, cells often form chains and/or long spines on the valve, which increases form resistance (Padisák et al., 2003) (Fig. 3.). These features are largely shared with species of Thalassiosira and Acanthoceras. Because of their extended area and relatively stable environment, oceans represent diversity hot spots for diatoms (Potapova, 2011). Therefore, the above-mentioned diatoms are, presumably, did not adapted to increased salinization of freshwaters, but “backward.” They evolved under “average” marine conditions and progressively inhabited hyposaline regions, finally entering into inland waters. This required not only adaptation to relatively low salinity but also to the different ionic compositions of these habitats. Why do not we have more marine species in continental saline lakes? The answer is that waters with intermediate salt content are intermittent and isolated in space and time; therefore, they constitute migration barriers through both directions (Potapova, 2011). The separated evolution of freshwater and marine diatoms probably lay in their physiological thresholds (Potapova, 2011), which is a task to explore using laboratory experiments and ecophysiological tools.
Shape resistance of diatoms to changing salinity in the phytoplankton: a common forms of planktic diatoms in freshwaters. Diatom cells b with spines, chains, and c lipid materials in saline waters
Dimorphism
Salinity-dependent dimorphism is characteristic for some diatoms (Cyclotella cryptica, C. meneghiniana, Anomoeoneis sphaerophora, Surirella peisonis, Navicula cuspidata). The typical valve structure can be found at low salinities (Fig. 4a) and post-auxospores at high salinities (Schultz, 1971; Schmid, 1977, 1979). One common feature of dimorphism is the appearance of “craticula” and “heribaudii” (the normal vegetative cells produce four inner valves: two craticulae and inside them two heribaudii; Round et al., 2000), which can develop during the resting spore formation as a protection from the elevated salt concentration or desiccation (Schmid, 1979, 2009; web1) as observed only in few members of the genus Craticula (Levkov et al., 2016) (Fig. 4b).
Morphological response of diatoms to increasing salinity: a the initial, normal forms of diatom species at lower salt concentration. The appearance of b craticula” forms, c cell size reductions and altered chain morphologies, and d teratological forms with increasing salinity
To cover the cell with organic casing (Thalassiosira weissflogii, Achnanthidium minutissimum, Navicula minima; Vrieling et al., 2007), serve a similar function, and save the cell against osmotic pressure (Gélabert et al., 2004).
Polymorphism
Salinity-caused osmotic pressure can also influence the chain morphology of diatoms. The distance between two adjacent cells of Skeletonema subsalsum and S. potamos Hasle (Fig. 4c) and the average cell number in a chain can increase with increasing salinity (S. subsalsum). At high salinity (35 psu) diatom species can enlarge their cell size resulting in shorter chains (Fig. 4c); moreover, the number of the chloroplasts in these cells can also increase (Hasle & Evensen, 1975; Paasche et al., 1975; Sarno et al., 2007; Torgan et al., 2009; Balzano et al., 2011; Falasco et al., 2021).
Salinity may have a direct effect on cell morphogenesis (Roubeix & Lancelot, 2008) by affecting the thickness of the silica wall. Namely, the external ionic strength affect the uptake of silicic acid and other ions and their ratio determine the silica polymerization. Under high salinities the aggregation of small silica particles inside the silica deposition vesicle is less expressed, resulting in thicker but more hydrated biosilica (Vrieling et al., 2007). In case of, e.g., Cyclotella meneghiniana and Thalassiosira pseudonana (Olsen & Paasche, 1986), these thin valves were observed with poorly developed spines and costae and sometimes missing silica granules along the valve mantle (Cyclotella meneghiniana) (Tuchman et al., 1984).
Complete cell size reduction (Thalassiosira pseudonana and T. weissflogii) (Fig. 4c) or only the height of the valve is demoted (Cyclotella meneghiniana) at higher salinity levels (Hildebrand et al. 2006; García et al., 2012). Height reduction is driven by turgor pressure during the interphase before the division. At high salinity, freshwater diatoms may not be able to produce so high intracellular osmolarity to reach the similar turgor pressure as at low salinity levels (Roubeix & Lancelot, 2008), which results in changes of size. Furthermore, smaller than average cell size of Stephanodiscus minutulus, Brachysira vitrea, Asterionella formosa, Achnanthes minutissima, and Tabellaria flocculosa is also characteristic at enhanced heavy metal concentration (Lynn et al., 2000; Cattaneo et al., 2004; Su et al., 2018).
Specific surface area and the pore size of Thalassiosira punctigera, Thalassiosira weissflogii, Cocconeis placentula, and Skeletonema subsalsum increase with the increasing salinity (Paasche et al., 1975; Vrieling et al., 2007; Leterme et al., 2010, 2013). Through pores, as nanoscale features of the cell membrane, the nutrients and other chemicals are exchanged with size selective filtering of molecules and nanoparticles (Fritz et al., 2010; Su et al., 2018). With the pore size compensation the species can maintain a steady diffusive flux toward the cell (Leterme et al., 2010). But contradictory results exist. In case of Cocconeis pinnata, the elevated salinity induced bigger pore size, but smaller surface area (Leterme et al., 2013) than average. There are further examples when salinity differently affects the valve morphology (changes in length, width, fibula, and stria density) both in pennate and centric diatoms (Nitzschia pusilla, N. frustulum, N. palea, N. filiformis var. conferta, Craticula subminuscula, Eolimna subminuscula, Gomphonema augur, Nitzschia palea var. debilis (Geissler, 1968, 1970a, 1970b; Schultz 1971; Schmid, 1977; Jahn, 1986; Wendker & Geissler, 1988; Wendker, 1990; Trobajo et al., 2011), and Stephanodiscus hantzschii (Geissler 1982, 1986). These contradictory results demonstrate that the morphological changes induced by salinity could be taxon or even clone specific (Trobajo et al., 2004).
Diatom teratological forms
Salinity can result in more pronounced, significant alterations in the valve structure leading to abnormal forms (Noune et al., 2023) (Fig. 4d). This significant modification and deformed outlines are referred to as teratological forms if they can potentially alter the physiological mechanisms and cell movement of diatoms (Falasco et al., 2009a). Significant changes in valve structure caused by salinity can be the number and place of the fultoportule (Thalassiosira weissflogii, Bussard et al., 2017; Cyclotella meneghiniana, Håkansson & Chepurnov, 1999) as well as the irregular or absent areolae (Synedra acus, Basharina et al., 2012; Thalassiosira eccentrica, Schmid, 1984). The osmotic stress may also result in displaced central nodules, fragmented raphae, altered stria pattern (Anomoeoneis costata, Anomoeoneis sphaerophora f. costata, Cyclotella meneghiniana, Håkansson & Chepurnov, 1999; Cyclotella cryptica, Noune et al., 2023), and abnormal valve outlines (Navicula cryptocephala, Aleem, 1950; Navicula gregaria, Cox, 1995; Cyclotella cryptica, Noune et al., 2023), which make the identification considerably difficult or impossible (Castillo et al., 1995) in highly saline environments.
In mining effluents, besides the high salinity, radioactive nuclides and high concentration of heavy metals further burden the aquatic ecosystems (Tipping et al., 2009), and besides the already mentioned teratological forms, further abnormal features can be detected as altered linear and central area in Fragilaria capucina var. capitellata (Falasco et al., 2009b), raphe modulations in Cymbella excisa, Encyonema minutum (Falasco et al., 2009b), Eunotia subarcuatoides (Furey et al., 2009), Cocconeis sawensis (Al-Handal et al., 2014), and Humidophila perpusilla (Millan et al., 2020), raphe canal adjustments in Nitzschia genus (Adshead-Simonsen et al., 1981), unusual colony forms in Tabellaria flocculosa with cells attached as straight chain colonies instead of the common zigzag form (Adshead-Simonsen et al., 1981), and mixed, substantially uncommon outline of the valves in Fragilaria vaucheriae, Synedra vaucheriae, Encyonema sp., Planothidium frequentissimum, and Navicula tripunctata (Falasco et al., 2009b).
In a recently published review about the teratology of diatoms, salinity caused deformities are mainly mentioned as a part of “multiple” impact (Falasco et al., 2021) under extreme environmental conditions (Padisák & Naselli-Flores, 2021), like high concentration of sulfate and carbonate salts (Cocconeis sawensis, Al-Handal et al., 2014), natural radioactivity (Crenotia angustior, Humidophila perpusilla, Planothidium frequentissimum, Millan et al., 2020), low discharge and high temperature (Achnanthes coarctata, Fragilaria crotonensis, Navicula tripunctata, Neidiomorpha binodis, Nitzschia sp., Ulnaria ulna, Sellaphora seminulum, Lai et al., 2019), high UV radiation, geothermal flux, nutrient supply (Cocconeis placentula, Nitzschia liebethruthii, Surirella chilensis, Cabrol et al., 2007), and industrial contamination in the genus Tabularia is mentioned as an example as a collateral stress factor (Falasco et al., 2021) resulting in teratological forms of diatoms (Fig. 4d).
Although these external morphological changes presumably caused by intracellular changes in response to salinity, studies about the links between intracellular processes and cell wall morphogenesis are rare (as you can see above) just as there are minimal explanations of the gene-level regulation of the valve morphology (Bussard et al., 2016.). However, change in the morphology might be explained with the trouble in uptaking silica (Cattaneo et al., 2004; Vrieling et al., 2007), which is regulated by sulfhydryl (-SH) groups on the cell surface (Lewin, 1954) as they have a high affinity to heavy metals and other toxic compounds. The increasing -SH binders reduce the silica uptake and inhibit ATPs as active sites of the -SH groups (De La Rocha et al., 2000). An another explanation might be that at high salinity level cytoskeletal genes are down-regulated, which cause changes in the gene expressions resulting in modification of the position of the silica deposition vesicle with the consequent modification of valve morphology (Bussard et al., 2016.) To understand these morphological changes in more detail, the extension of knowledge about molecular, physiological processes, and cell cycle regulation is necessary (Leterme et al., 2013). This knowledge would allow us to understand the plastic and genetic component of the salinity tolerance and the potential response on evolutionary time scale along increasing salinity (Castillo et al., 2018).
Salt tolerance of diatoms
Elevated salinity can cause sublethal or even lethal effects for a variety of organisms (e.g., Hart et al., 1991; Hintz & Relyea, 2019) depending on their tolerance ranges. The number of experimental studies analyzing the toxic effect of salinity or its different components on freshwater diatoms is limited. Most of the available studies are focusing on brackish and marine species; however, some of them are common in freshwaters with elevated ion content. The salt tolerance of Nitzschia species is often examined using different endpoints and units of salinity (Clavero et al., 2000; Trobajo et al., 2011; Lengyel et al., 2015, 2020; Bagmet et al., 2017).
Photosynthetic activity of N. aurariae, N. reskoi, and N. supralitorea along Cl− and SO42− gradients were measured, where the survival limit concentrations were 9, 8.5, and 11 g l−1 Cl− and 12, 6.5, and 13.5 g l−1 SO42− (Lengyel et al., 2020). However, 50% photosynthetic activity declines of N. frustulum (isolated from soda pans) were noticed at 5.25 g l−1 Cl− and 4.8 g l−1 SO42− concentrations (Lengyel et al., 2015, 2020). N. frustulum and N. pusilla isolated from brackish water showed a very broad salinity range (still well growing at 32 g l−1; Trobajo et al., 2011). In the study of Clavero et al. (2000), N. frustulum, Navicula phyllepta, and Amphora angusta still grew at about 75 g l−1 salinity. The freshwater clones of Nitzschia palea and N. filiformis var. conferta showed reduced growth above 16 g l−1 (Trobajo et al., 2011). A study highlighted that the reproductive rate of the isolated N. palea was not influenced by the original habitat where the species was isolated; this species survives at salinity of up to 22 g l−1 and dies at 37 g l−1 (Bagmet et al., 2017).
The hypothetical salinity threshold limits of diatoms are assumed from 0.2 to 18 g l−1 (Potapova, 2011); however, the above-mentioned studies revealed that this barrier is highly exceeded under natural conditions and is species specific. Further experiments and long-term mesocosm experiments would be needed to identify precisely these thresholds (Cañedo-Argüelles et al., 2016) and the examination of the impacts of complex chemical mixtures (“chemical cocktails”) is also urgent (Kaushal et al., 2021) to develop the recent water quality guidelines to protect aquatic ecosystems from secondary salinization (Hintz et al., 2022).
Biotechnology
Diatoms are a widely distributed group of microalgae with capabilities that make them ideal for multiple biotechnological applications. Although most of their biotechnological use is not specifically linked to their salt tolerance (B-Béres et al., 2022), there are some examples for those linked to salinity (Marella et al., 2020a, 2020b). One of them is to find a way using diatoms to obtain drinking water from unconventional water supplies as brackish groundwater or reclaimed water (Ikehata et al., 2018), although this ability of diatoms has only recently been used in water reuse and desalination (Ikehata et al., 2017, 2018; Alsar et al., 2020). It is well known that silica is essential for building the cell wall of diatoms, thus these algae efficiently extract dissolved silica from water. An up-to-date study pointed out that a diatom consortium dominated by Nitzschia, Pseudostaurosira and Halamphora species successfully removed more than 95% of reactive silica from brackish agricultural drainage water within 28 h (Ikehata et al., 2017). In addition, Nitzschia and Pseudostaurosira species were effectively applied in reverse osmosis methods, in which 95% of concentrate aqueous silica (78 mgl−1) was removed under suboptimal conditions within 72 h (Ikehata et al., 2018). Not only diatom cells but also deionized diatomite (Diatomaceous Earth) can be used in desalinization processes as the pretreated diatomite was able to remove even more than 50% of NaCl content of waters (Alsar et al., 2020).
It is also known that saline lakes host diatoms, like Nitzschia palea, which can produce considerable amount of lipids for alternative fuel production (Abdel-Hamid et al., 2013). This production of diatoms are also characteristic during the removal of nutrients from natural and wastewater (Adey et al., 2011, 2013), when significant amount of biomass are produced with high percentage of various unsaturated or saturated fatty acids and lipids (20–30% of dry cell weight). These compounds are known to be widely used as raw material of cosmetics, medicines, biofuel precursors, and aquaculture food implementers (Mishra et al., 2017; Marella et al., 2020a, 2020b).
In the last decades, we witness the significant development of biotechnology. Diatoms seem to be a promising source (Seckbach & Gordon, 2019) as their special morphological features and intracellular processes may provide several unexplored potential for further industrial application especially in connection with salinization (Ishika et al, 2018; Navarro et al., 2021). However, there are many unanswered questions in this area. Research and a deeper understanding of the processes at both genotypic and phenotypic levels in diatoms would further accentuate its applicability in biotechnology (Mishra et al., 2017).
Conclusion
Diatoms have developed a number of salt tolerance mechanisms in order to ensure their success in continental salty environments. However, our knowledge has been limited concerning the intracellular changes and its consequences, similar to understanding the detailed process of biomineralization and the meaning of the morphological variations of these beautiful microscopic creatures. Although salinity tolerances are driven by genes and infraspecific genetic diversity, genomic, transcriptomic, proteomic, and metabolic studies and their combinations are almost completely missing; however, they would be crucial to discover the relevant processes and their energy costs. Salt-responsive genes, salt-sensible mutants, and the gene regulation of the morphological changes induced by salinity have been also sparsely explored. Besides short-term acclimation studies, further, long-term studies would be necessary to reveal the adaptation of diatoms to salinization. This knowledge would be an effective key for understanding the salinity induced processes also at higher (population, community, ecosystem, and above up to biogeochemistry) levels and to manage the ecological and economic consequences of salinization. Furthermore, these results could open the way for more and more biotechnological applications as ecosystem services provided by diatoms.
Data availability
Ethical and professional principles were completely followed.
References
Abdel-Hamid, M. I., D. A. El-Refaay, M. Abdel-Mogib & Y. A. Azab, 2013. Studies on biomass and lipid production of seven diatom species with special emphasis on lipid composition of Nitzschia palea (Bacillariophyceae) as reliable biodiesel feedstock. Algological Studies 143: 65–87.
Abdullahi, A. S., G. J. C. Underwood & M. R. Gretz, 2006. Extracellular matrix assembly in diatoms (Bacillariophyceae). V. Environmental effects on polysaccharide synthesis in the model diatom, Phaeodactylum tricornutum. Journal of Phycology 42: 363–378.
Adey, W. H., P. C. Kangas & W. Mulbry, 2011. Algal turf scrubbing: cleaning surface waters with solar energy while producing a biofuel. BioScience 61: 434–441.
Adey, W. H., H. D. Laughinghouse, J. B. Miller, L.-A.C. Hayek, J. G. Thompson, S. Bertman, K. Hampel & S. Puvanendran, 2013. Algal turf scrubber (ATS) floways on the Great Wicomico River, Chesapeake Bay: productivity, algal community structure, substrate and chemistry. Journal of Phycology 49: 489–501.
Admiraal, W., R. W. P. M. Laane & H. Peletier, 1984. Participation of diatoms in the amino acid cycle of coastal waters; uptake and excretion in cultures. Marine Ecology Progress Series 15: 303–306.
Adshead-Simonsen, P. C., G. E. Murray & D. J. Kushner, 1981. Morphological changes in the diatom, Tabellaria flocculosa, induced by very low concentrations of cadmium. Bulletin of Environmental Contamination and Toxicology 26: 6.
Aleem, A. A., 1950. Distribution and ecology of British marine littoral diatoms. Journal of Ecology 38: 75–106.
Al-Handal, A., C. Riaux-Gobin, D. Abdulla & M. Ali, 2014. Cocconeis sawensis sp. nov. (Bacillariophyceae) from a saline lake (Sawa Lake), South Iraq: comparison with allied taxa. Phytotaxa 181: 216–228.
Allakhverdiev, S. I., Y. Nishiyama, I. Suzuki, Y. Tasaka & N. Murata, 1999. Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt stress. Proceedings of the National Academy of Sciences 96: 5862–5867.
Allakhverdiev, S. I., A. Sakamoto, Y. Nishiyama & N. Murata, 2000. Inactivation of photosystems I and II in response to osmotic stress in Synechococcus Contribution of Water Channels. Plant Physiology 122: 1201–1208.
Allan, G. G., J. Lewin & P. G. Johnson, 1972. Marine polymers IV Diatom Polysaccharides. Botanica Marina 15: 102–108.
Allen, A. E., C. L. Dupont, M. Oborník, A. Horák, A. Nunes-Nesi, J. P. McCrow, H. Zheng, D. A. Johnson, H. Hu, A. R. Fernie & C. Bowler, 2011. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473: 203–207.
Alsar, Zh., B. Duskinova & Z. Insepov, 2020. New sorption properties of diatomaceous Earth for water desalination and reducing salt stress of plants. Eurasian Chemico-Technological Journal 22: 89.
Apoya-Horton, M. D., L. Yin, G. J. C. Underwood & M. R. Gretz, 2006. Movement modalities and responses to environmental changes of the mudflat diatom Cylindrotheca closterium (Bacillariophyceae). Journal of Phycology 42: 379–390.
Armbrust, E. V., J. A. Berges, C. Bowler, B. R. Green, D. Martinez, N. H. Putnam, S. Zhou, A. E. Allen, K. E. Apt, M. Bechner, M. A. Brzezinski, B. K. Chaal, A. Chiovitti, A. K. Davis, M. S. Demarest, J. C. Detter, T. Glavina, D. Goodstein, M. Z. Hadi, U. Hellsten, M. Hildebrand, B. D. Jenkins, J. Jurka, V. V. Kapitonov, N. Kröger, W. W. Y. Lau, T. W. Lane, F. W. Larimer, J. C. Lippmeier, S. Lucas, M. Medina, A. Montsant, M. Obornik, M. S. Parker, B. Palenik, G. J. Pazour, P. M. Richardson, T. A. Rynearson, M. A. Saito, D. C. Schwartz, K. Thamatrakoln, K. Valentin, A. Vardi, F. P. Wilkerson & D. S. Rokhsar, 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306: 79–86.
Aslam, S. N., T. Cresswell-Maynard, D. N. Thomas & G. J. C. Underwood, 2012. Production and characterization of the intra- and extracellular carbohydrates and polymeric substances (EPS) of three Sea-Ice diatom species, and evidence for a cryoprotective role for EPS. Journal of Phycology 48: 1494–1509.
Ayache, N., F. Hervé, N. Lundholm, Z. Amzil & A. M. N. Caruana, 2020. Acclimation of the marine diatom Pseudo-nitzschia australis to different salinity conditions: effects on growth, photosynthetic activity, and domoic acid content. Journal of Phycology 56: 97–109.
Ayache, N., F. Hervé, V. Martin-Jézéquel, Z. Amzil & A. M. N. Caruana, 2019. Influence of sudden salinity variation on the physiology and domoic acid production by two strains of Pseudo-nitzschia australis. Journal of Phycology 55: 186–195.
Baek, S. H., S. W. Jung & K. Shin, 2011. Effects of temperature and salinity on growth of Thalassiosira pseudonana (Bacillariophyceae) isolated from ballast water. Journal of Freshwater Ecology 26: 547–552.
Bagmet, V. B., S. R. Abdullin, B. R. Kuluev, O. I. Davidovich & N. A. Davidovich, 2017. The effect of salinity on the reproduction rate of Nitzschia palea (Kützing) W. Smith (Bacillariophyta) clones. Russian Journal of Ecology 48: 287–289.
Bąk, M., D. Halabowski, A. Kryk, I. Lewin & A. Sowa, 2020. Mining salinisation of rivers: its impact on diatom (Bacillariophyta) assemblages. Fottea 20: 1–16.
Balzano, S., D. Sarno & W. H. C. F. Kooistra, 2011. Effects of salinity on the growth rate and morphology of ten Skeletonema strains. Journal of Plankton Research 33: 937–945.
Basharina, T. N., E. N. Danilovtseva, S. N. Zelinskiy, I. V. Klimenkov, Y. V. Likhoshway & V. V. Annenkov, 2012. The Effect of titanium, zirconium and tin on the growth of diatom Synedra acus and morphology of its silica valves. Silicon 4: 239–249.
B-Béres, V., C. Stenger-Kovács, K. Buczkó, J. Padisák, G. B. Selmeczy, E. Lengyel & K. Tapolczai, 2022. Ecosystem services provided by freshwater and marine diatoms. Hydrobiologia. https://doi.org/10.1007/s10750-022-04984-9.
Bisson, M. A. & G. O. Kirst, 1995. Osmotic acclimation and turgor pressure regulation in algae. The Science of Nature 10: 461–471.
Boyer, J. S., 1976. Water deficits and photosynthesis. In Kozlowski, T. T. (ed), Soil Water Measurement, Plant Responses, and Breeding for Drought Resistance Academic Press, London: 153–190.
Brand, L. E., 1984. The salinity tolerance of forty-six marine phytoplankton isolates. Estuarine, Coastal and Shelf Science 18: 543–556.
Bromke, M. A., P. Giavalisco, L. Willmitzer & H. Hesse, 2013. Metabolic analysis of adaptation to short-term changes in culture conditions of the marine diatom Thalassiosira pseudonana. PLoS ONE 8: e67340.
Bussard, A., E. Corre, C. Hubas, E. Duvernois-Berthet, G. Le Corguillé, L. Jourdren, F. Coulpier, P. Claquin & P. J. Lopez, 2017. Physiological adjustments and transcriptome reprogramming are involved in the acclimation to salinity gradients in diatoms. Environmental Microbiology 19: 909–925.
Cabrol, N. A., C. P. McKay, E. A. Grin, K. T. Kiss, É. Ács, B. Tóth, I. Grigorszky, K. Szabó-Taylor, D. A. Fike, A. N. Hock, C. Demergasso, L. Escudero, P. Galleguillos, B. H. Grigsby, J. Z. Román & C. Tambley, 2007. Signatures of habitats and life in Earth’s high-altitude lakes: clues to Noachian aqueous environments on Mars. In Chapman, M. G. (ed), The Geology of Mars Cambridge University Press, Cambridge: 349–370.
Cañedo-Argüelles, M., C. P. Hawkins, B. J. Kefford, R. B. Schäfer, B. J. Dyack, S. Brucet, D. Buchwalter, J. Dunlop, O. Frör, J. Lazorchak, E. Coring, H. R. Fernandez, W. Goodfellow, A. L. G. Achem, S. Hatfield-Dodds, B. K. Karimov, P. Mensah, J. R. Olson, C. Piscart, N. Prat, S. Ponsá, C.-J. Schulz & A. J. Timpano, 2016. Saving freshwater from salts. Science 351: 914–916.
Castillo, A. M., D. M. T. Sharpe, C. K. Ghalambor & L. F. De León, 2018. Exploring the effects of salinization on trophic diversity in freshwater ecosystems: a quantitative review. Hydrobiologia 807: 1–17.
Castillo, J. A., M. E. Meave del Castillo & D. U. Hernández-Becerril, 1995. Morphology and distribution of species of the diatom genus Skeletonema in a tropical coastal lagoon. European Journal of Phycology 30: 107–115.
Cattaneo, A., Y. Couillard, S. Wunsam & M. Courcelles, 2004. Diatom taxonomic and morphological changes as indicators of metal pollution and recovery in Lac Dufault (Québec, Canada). Journal of Paleolimnology 32: 163–175.
Chen, G.-Q., Y. Jiang & F. Chen, 2008. Salt-induced alterations in lipid composition of diatom Nitzschia laevis (Bacillariophyceae) under heterotrophic culture condition. Journal of Phycology 44: 1309–1314.
Cheng, R., J. Feng, B.-X. Zhang, Y. Huang, J. Cheng & C.-X. Zhang, 2014. Transcriptome and gene expression analysis of an oleaginous diatom under different salinity conditions. BioEnergy Research 7: 192–205.
Clavero, E., M. Hernández-Mariné, J. O. Grimalt & F. Garcia-Pichel, 2000. Salinity tolerance of diatoms from thalassic hypersaline environments. Journal of Phycology 36: 1021–1034.
Coldsnow, K. D., B. M. Mattes, W. D. Hintz & R. A. Relyea, 2017. Rapid evolution of tolerance to road salt in zooplankton. Environmental Pollution 222: 367–373.
Cox, E. J., 1995. Morphological variation in widely distributed diatom taxa : taxonomic and ecological implications. Proceedings of the 13th International Diatom Symposium, Italy Biopress: 335–345.
Cox, E. J., 2006. Raphe loss and spine formation in Diadesmis gallica (Bachillariophyta)-an intriguing example of phenotypic polymorphism in a diatom. Nova Hedwigia 130: 163–176.
Cunillera-Montcusí, D., M. Beklioğlu, M. Cañedo-Argüelles, E. Jeppesen, R. Ptacnik, C. A. Amorim, S. E. Arnott, S. A. Berger, S. Brucet, H. A. Dugan, M. Gerhard, Z. Horváth, S. Langenheder, J. C. Nejstgaard, M. Reinikainen, M. Striebel, P. Urrutia-Cordero, C. F. Vad, E. Zadereev & M. Matias, 2022. Freshwater salinisation: a research agenda for a saltier world. Trends in Ecology & Evolution 37: 440–453.
da Costa, M. S., H. Santos & E. A. Galinski, 1998. An overview of the role and diversity of compatible solutes in Bacteria and Archaea. In Antranikian, G. (ed), Biotechnology of Extremophiles Springer, Berlin: 117–153.
de Castro Araújó, S. & V. M. T. Garcia, 2005. Growth and biochemical composition of the diatom Chaetoceros cf. wighamii brightwell under different temperature, salinity and carbon dioxide levels. I. Protein, carbohydrates and lipids. Aquaculture 246: 405–412.
De La Rocha, C. L. D., D. A. Hutchins, M. A. Brzezinski & Y. Zhang, 2000. Effects of iron and zinc deficiency on elemental composition and silica production by diatoms. Marine Ecology Progress Series 195: 71–79.
De Miranda, M., M. Gaviano & E. Serra, 2005. Changes in the cell size of the diatom Cylindrotheca closterium in a hyperhaline pond. Chemistry and Ecology 21: 77–81.
Dickson, D. M. J. & G. O. Kirst, 1987. Osmotic adjustment in marine eukaryotic algae: the role of inorganic ions, quaternary ammonium, tertiary sulphonium and carbohydrate solutes. New Phytologist 106: 645–655.
Doucette, G. J., K. L. King, A. E. Thessen & Q. Dortch, 2008. The effect of salinity on domoic acid production by the diatom Pseudo-nitzschia multiseries. Nova Hedwigia 133: 31–46.
Erdmann, N. & M. Hagemann, 2001. Salt acclimation of algae and cyanobacteria: a comparison. In Rai, L. C. & J. P. Gaur (eds), Algal Adaptation to Environmental Stresses: Physiological, Biochemical and Molecular Mechanisms Springer, Berlin: 323–361.
Falasco, E., F. Bona, G. Badino, L. Hoffmann & L. Ector, 2009a. Diatom teratological forms and environmental alterations: a review. Hydrobiologia 623: 1–35.
Falasco, E., F. Bona, M. Ginepro, D. Hlúbiková, L. Hoffmann & L. Ector, 2009b. Morphological abnormalities of diatom silica walls in relation to heavy metal contamination and artificial growth conditions. Water SA 35: 5.
Falasco, E., F. Bona, A. M. Risso & E. Piano, 2021. Hydrological intermittency drives diversity decline and functional homogenization in benthic diatom communities. Science of the Total Environment 762: 143090.
Fritz, S. C., B. F. Cumming, F. Gasse & K. R. Laird, 2010. Diatoms as indicators of hydrologic and climatic change in saline lakes. In Smol, J. P. & E. F. Stoermer (eds), The Diatoms: Applications for the Environmental and Earth Sciences Cambridge University Press, Cambridge: 186–208.
Fujii, S., N. Nishimoto, A. Notoya & J. A. Hellebust, 1995. Growth and osmoregulation of Chaetoceros muelleri in relation to salinity. Plant and Cell Physiology 36: 759–764.
Furey, P. C., R. L. Lowe & J. R. Johansen, 2009. Teratology in Eunotia taxa in the Great Smoky Mountains National Park and description of Eunotia macroglossa sp. nov. Diatom Research 24: 273–290.
García, N., J. A. López-Elías, A. Miranda, M. Martínez-Porchas, N. Huerta & A. García, 2012. Effect of salinity on growth and chemical composition of the diatom Thalassiosira weissflogii at three culture phases. Latin American Journal of Aquatic Research 40: 435–440.
Garza-Sánchez, F., D. J. Chapman & J. B. Cooper, 2009. Nitzschia ovalis (Bacillariophyceae) Mono lake strain accumulates 1,4/2,5 cyclohexanetetrol in response to increased salinity. Journal of Phycology 45: 395–403.
Geissler, U., 1968. Zur Variabilität der Schalenmerkmale bei einigen Diatomeen. Berichte Der Deutschen Botanischen Gesellschaft 80: 756.
Geissler, U., 1970a. Die Variabilität der Schalenmerkmale bei den Diatomeen. Nova Hedwigia 19: 623–773.
Geissler, U., 1970b. Die Schalenmerkmale der Diatomeen - Ursachen ihrer Variabilität und Bedeutung für die Taxonomie. Nova Hedwigia Beihefte 31: 511–535.
Geissler, U., 1982. Experimentelle Untersuchungen zur Variabilität der Schalenmerkmale bei einigen zentrischen Süsswasser-Diatomeen. 1. Der Einfluss unterschiedlicher Salzkonzentrationen auf den Valva-Durchmesser von Stephanodiscus hantzschii Grunow. Nova Hedwigia Beih 73: 211–246.
Geissler, U., 1986. Experimental investigations on the variability of frustule characteristics of several freshwater diatoms. 2. The influence of different salt concentrations on some valve structures of Stephanodiscus hantzschii Grunow. In Ricard, M. (ed), Proceedings of the 8th International Diatom Symposium. Koeltz, Königstein, Germany: 59–66.
Gélabert, A., O. S. Pokrovsky, J. Schott, A. Boudou, A. Feurtet-Mazel, J. Mielczarski, E. Mielczarski, N. Mesmer-Dudons & O. Spalla, 2004. Study of diatoms/aqueous solution interface. I. Acid-base equilibria and spectroscopic observation of freshwater and marine species. Geochimica Et Cosmochimica Acta 68: 4039–4058.
Glaser, K. & U. Karsten, 2020. Salinity tolerance in biogeographically different strains of the marine benthic diatom Cylindrotheca closterium (Bacillariophyceae). Journal of Applied Phycology 32: 3809–3816.
Godhe, A. & T. Rynearson, 2016. The role of intraspecific variation in the ecological and evolutionary success of diatoms in changing environments. Philosophical Transactions of the Royal Society b: Biological Sciences 372: 20160399.
Gupta, B. & B. Huang, 2014. Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. International Journal of Genomics 2014: 701596.
Hagemann, M., 2016. Coping with high and variable salinity: molecular aspects of compatible solute accumulation. In Borowitzka, M. A., J. Beardall & J. A. Raven (eds), The Physiology of Microalgae Springer, Dordrecht: 359–372.
Haimovich-Dayan, M., N. Garfinkel, D. Ewe, Y. Marcus, A. Gruber, H. Wagner, P. G. Kroth & A. Kaplan, 2013. The role of C4 metabolism in the marine diatom Phaeodactylum tricornutum. New Phytologist 197: 177–185.
Håkansson, H. & V. Chepurnov, 1999. A study of variation in valve morphology of the diatom Cyclotella meneghiniana in monoclonal cultures: effect of auxospore formation and different salinity conditions. Diatom Research 14: 251–272.
Hart, B. T., P. Bailey, R. Edwards, K. Hortle, K. James, A. McMahon, C. Meredith & K. Swadling, 1991. A review of the salt sensitivity of the Australian freshwater biota. Hydrobiologia 210: 105–144.
Hasanuzzaman, M. & M. Tanveer, 2020. Salt and Drought Stress Tolerance in Plants: Signaling Networks and Adaptive Mechanisms, Springer, Dordrecht:
Hasegawa, P. M., R. A. Bressan, J.-K. Zhu & H. J. Bohnert, 2000. Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51: 463–499.
Hasle, G. R. & D. L. Evensen, 1975. Brackish-water and fresh-water species of the diatom genus Skeletonema Grev. I. Skeletonema subsalsum (A. Cleve) Bethge. Phycologia 14: 283–297.
Hellebust, J. A., 1985. Mechanisms of response to salinity in halotolerant microalgae. In Pasternak, D. & A. San Pietro (eds), Biosalinity in Action: Bioproduction with Saline Water Springer, Dordrecht: 69–81.
Henzler, T. & E. Steudle, 1995. Reversible closing of water channels in Chara internodes provides evidence for a composite transport model of the plasma membrane. Journal of Experimental Botany 46: 199–209.
Herbert, E. R., P. Boon, A. J. Burgin, S. C. Neubauer, R. B. Franklin, M. Ardón, K. N. Hopfensperger, L. P. M. Lamers & P. Gell, 2015. A global perspective on wetland salinization: ecological consequences of a growing threat to freshwater wetlands. Ecosphere 6: art206.
Hildebrand, M., E. York, J. I. Kelz, A. K. Davis, L. G. Frigeri, D. P. Allison & M. J. Doktycz, 2006. Nanoscale control of silica morphology and three-dimensional structure during diatom cell wall formation. Journal of Materials Research 21: 2689–2698.
Hintz, W. D. & R. A. Relyea, 2019. A review of the species, community, and ecosystem impacts of road salt salinisation in fresh waters. Freshwater Biology 64: 1081–1097.
Hintz, W. D., S. E. Arnott, C. C. Symons, D. A. Greco, A. McClymont, J. A. Brentrup, M. Cañedo-Argüelles, A. M. Derry, A. L. Downing, D. K. Gray, S. J. Melles, R. A. Relyea, J. A. Rusak, C. L. Searle, L. Astorg, H. K. Baker, B. E. Beisner, K. L. Cottingham, Z. Ersoy, C. Espinosa, J. Franceschini, A. T. Giorgio, N. Göbeler, E. Hassal, M.-P. Hébert, M. Huynh, S. Hylander, K. L. Jonasen, A. E. Kirkwood, S. Langenheder, O. Langvall, H. Laudon, L. Lind, M. Lundgren, L. Proia, M. S. Schuler, J. B. Shurin, C. F. Steiner, M. Striebel, S. Thibodeau, P. Urrutia-Cordero, L. Vendrell-Puigmitja & G. A. Weyhenmeyer, 2022. Current water quality guidelines across North America and Europe do not protect lakes from salinization. Proceedings of the National Academy of Sciences 119: e2115033119.
Hoagland, K. D., J. R. Rosowski, M. R. Gretz & S. C. Roemer, 1993. Diatom extracellular polymeric substances: function, fine structure, chemistry, and physiology. Journal of Phycology 29: 537–566.
Horowitz, M., 2001. Heat acclimation: phenotypic plasticity and cues to the underlying molecular mechanisms. Journal of Thermal Biology 26: 357–363.
Ikehata, K., Y. Zhao, J. Ma, A. T. Komor, N. Maleky & M. A. Anderson, 2018. A novel photobiological process for reverse osmosis concentrate treatment using brackish water diatoms. Water Supply 18: 594–602.
Ikehata, K., Y. Zhao, N. Maleky, A. T. Komor & M. A. Anderson, 2017. Aqueous silica removal from agricultural drainage water and reverse osmosis concentrate by brackish water diatoms in semi-batch photobioreactors. Journal of Applied Phycology 29: 223–233.
Indrayani, I., N. R. Moheimani, K. de Boer, P. A. Bahri & M. A. Borowitzka, 2020. Temperature and salinity effects on growth and fatty acid composition of a halophilic diatom, Amphora sp. MUR258 (Bacillariophyceae). Journal of Applied Phycology 32: 977–987.
Ishika, T., P. A. Bahri, D. W. Laird & N. R. Moheimani, 2018. The effect of gradual increase in salinity on the biomass productivity and biochemical composition of several marine, halotolerant, and halophilic microalgae. Journal of Applied Phycology 30: 1453–1464.
Jackson, A. E., S. W. Ayer & M. V. Laycock, 1992. The effect of salinity on growth and amino acid composition in the marine diatom Nitzschia pungens. Canadian Journal of Botany 70: 2198–2201.
Jacobsen, T. & R. M. Adams, 1958. Salt and silt in Ancient Mesopotamian Agriculture. Progressive changes in soil salinity and sedimentation contributed to the breakup of past civilizations. Science 128: 1251–1258.
Jahn, R., 1986. A study ofGomphonema augur Ehrenberg. The structure of the frustule and its variability in clones and populations. In Ricard, M. (ed), 8th Diatom Symposium. Koeltz, Königstein, Germany: 191–204
Janknegt, P. J., W. H. Van De Poll, R. J. W. Visser, J. W. Rijstenbil & A. G. J. Buma, 2008. Oxidative stress responses in the marine Antarctic diatom Chaetoceros brevis (Bacillariophyceae) during photoacclimation. Journal of Phycology 44: 957–966.
Jaramillo-Madrid, A. C., J. Ashworth & P. J. Ralph, 2020. Levels of diatom minor sterols respond to changes in temperature and salinity. Journal of Marine Science and Engineering 8: 85.
Kageyama, H., Y. Tanaka, A. Shibata, R. Waditee-Sirisattha & T. Takabe, 2018a. Dimethylsulfoniopropionate biosynthesis in a diatom Thalassiosira pseudonana: identification of a gene encoding MTHB-methyltransferase. Archives of Biochemistry and Biophysics 645: 100–106.
Kageyama, H., Y. Tanaka & T. Takabe, 2018b. Biosynthetic pathways of glycinebetaine in Thalassiosira pseudonana; functional characterization of enzyme catalyzing three-step methylation of glycine. Plant Physiology and Biochemistry 127: 248–255.
Karsten, U., 2012. Seaweed acclimation to salinity and desiccation stress. In Wiencke, C. & K. Bischof (eds), Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization Springer, Berlin: 87–107.
Kaushal, S. S., G. E. Likens, M. L. Pace, J. E. Reimer, C. M. Maas, J. G. Galella, R. M. Utz, S. Duan, J. R. Kryger, A. M. Yaculak, W. L. Boger, N. W. Bailey, S. Haq, K. L. Wood, B. M. Wessel, C. E. Park, D. C. Collison, B. Y. Aaqob, I. Aisin, T. M. Gedeon, S. K. Chaudhary, J. Widmer, C. R. Blackwood, C. M. Bolster, M. L. Devilbiss, D. L. Garrison, S. Halevi, G. Q. Kese, E. K. Quach, C. M. P. Rogelio, M. L. Tan, H. J. S. Wald & S. A. Woglo, 2021. Freshwater salinization syndrome: from emerging global problem to managing risks. Biogeochemistry 154: 255–292.
Kauss, H., 1978. Osmotic regulation in algae. In Reinhold, L., J. B. Harbone & T. Swain (eds), Progress in Phytochemistry Elsevier, Amsterdam: 1–27.
Keller, M. D., R. P. Kiene, P. A. Matrai & W. K. Bellows, 1999. Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton II. N-Limited Chemostat Cultures. Marine Biology 135: 249–257.
Kettles, N. L., S. Kopriva & G. Malin, 2014. Insights into the regulation of DMSP synthesis in the diatom Thalassiosira pseudonana through APR activity, proteomics and gene expression analyses on cells acclimating to changes in salinity, light and nitrogen. PLoS ONE 9: e94795.
Khan, W.-D., M. Tanveer, R. Shaukat, M. Ali & F. Pirdad, 2020. An overview of salinity tolerance mechanism in plants. In Hasanuzzaman, M. & M. Tanveer (eds), Salt and Drought Stress Tolerance in Plants: Signaling Networks and Adaptive Mechanisms Springer, Berlin: 1–16.
Kinne, O., 1966. Physiological aspects of animal life in estuaries with special reference to salinity. Netherlands Journal of Sea Research 3: 222–244.
Kirst, G. O., 1989. Salinity tolerance of eukaryotic marine algae. Annual Review of Plant Physiology and Plant Molecular Biology 40: 21–53.
Kirst, G. O., 1996. Osmotic adjustment in phytoplankton and macroalgae. In Kiene, R. P., P. T. Visscher, M. D. Keller & G. O. Kirst (eds), Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds Springer, Boston: 121–129.
Krawiec, R. W., 1982. Autecology and clonal variability of the marine centric diatom Thalassiosira rotula (Bacillariophyceae) in response to light, temperature and salinity. Marine Biology 69: 79–89.
Krell, A., 2006. Salt stress tolerance in the psychrophilic diatom Fragilariopsis cylindrus. Dissertation, Universität Bremen.
Krell, A., B. Beszteri, G. Dieckmann, G. Glöckner, K. Valentin & T. Mock, 2008. A new class of ice-binding proteins discovered in a salt-stress-induced cDNA library of the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae). European Journal of Phycology 43: 423–433.
Krell, A., D. Funck, I. Plettner, U. John & G. Dieckmann, 2007. Regulation of proline metabolism under salt stress in the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae). Journal of Phycology 43: 753–762.
Kumar, M., P. Kumari, C. R. K. Reddy & B. Jha, 2014. Salinity and desiccation induced oxidative stress acclimation in seaweeds. Advances in Botanical Research 71: 91–123.
Kunz, J. L., J. M. Conley, D. B. Buchwalter, T. J. Norberg-King, N. E. Kemble, N. Wang & C. G. Ingersoll, 2013. Use of reconstituted waters to evaluate effects of elevated major ions associated with mountaintop coal mining on freshwater invertebrates. Environmental Toxicology and Chemistry 32: 2826–2835.
Lai, G. G., B. M. Padedda, C. E. Wetzel, M. Cantonati, N. Sechi, A. Lugliè & L. Ector, 2019. Diatom assemblages from different substrates of the Casteldoria thermo-mineral spring (Northern Sardinia, Italy). Botany Letters 166: 14–31.
Larsen, E. H., L. E. Deaton, H. Onken, M. O’Donnell, M. Grosell, W. H. Dantzler & D. Weihrauch, 2014. Osmoregulation and excretion. Comprehensive. Physiology 4: 405–573.
Latta, L. C., L. J. Weider, J. K. Colbourne & M. E. Pfrender, 2012. The evolution of salinity tolerance in Daphnia: a functional genomics approach. Ecology Letters 15: 794–802.
Lelong, A., H. Hégaret, P. Soudant & S. S. Bates, 2012. Pseudo-nitzschia (Bacillariophyceae) species, domoic acid and amnesic shellfish poisoning: revisiting previous paradigms. Phycologia 51: 168–216.
Lengyel, E., A. W. Kovács, J. Padisák & C. Stenger-Kovács, 2015. Photosynthetic characteristics of the benthic diatom species Nitzschia frustulum (Kützing) Grunow isolated from a soda pan along temperature-, sulfate- and chloride gradients. Aquatic Ecology 49: 401–416.
Lengyel, E., D. Lázár, A. J. Trájer & C. Stenger-Kovács, 2020. Climate change projections for Carpathian soda pans on the basis of photosynthesis evidence from typical diatom species. Science of the Total Environment 710: 136241.
Leterme, S. C., A. V. Ellis, J. G. Mitchell, M.-J. Buscot, T. Pollet, M. Schapira & L. Seuront, 2010. Morphological flexibility of Cocconeis placentula (Bacillariophyceae) nanostructure to changing salinity levels. Journal of Phycology 46: 715–719.
Leterme, S. C., E. Prime, J. Mitchell, M. H. Brown & A. V. Ellis, 2013. Diatom adaptability to environmental change: a case study of two Cocconeis species from high-salinity areas. Diatom Research 28: 29–35.
Levkov, Z., S. Tofilovska & D. Mitić-Kopanja, 2016. Species of the diatom genus Craticula Grunow (Bacillariophycea) from Macedonia. Contributions, Section of Natural, Mathematical and Biotechnical Sciences, MASA 37: 129–165.
Lewin, J. C., 1954. Silicon metabolism in diatoms. I. Evidence for the role of reduced sulfur compounds in silicon utilization. The Journal of General Physiology 37: 589–599.
Liu, M. S. & J. A. Hellebust, 1976. Effects of salinity and osmolarity of the medium on amino acid metabolism in Cyclotella cryptica. Canadian Journal of Botany 54: 938–948.
Liu, X., G. Zhang, J. Zhang, Y. J. Xu, Y. Wu, Y. Wu, G. Sun, Y. Chen & H. Ma, 2020. Effects of irrigation discharge on salinity of a large freshwater lake: a case study in Chagan Lake, Northeast China. Water 12: 2112.
Lundholm, N., J. Skov, R. Pocklington & Ø. Moestrup, 1997. Studies on the marine planktonic diatom Pseudo-nitzschia. 2. Autecology of P. pseudodelicatissima based on isolates from Danish coastal waters. Phycologia 36: 381–388.
Lynn, S. G., S. S. Kilham, D. A. Kreeger & S. J. Interlandi, 2000. Effect of nutrient availability on the biochemical and elemental stoichiometry in the freshwater diatom Stephanodiscus minutulus (Bacillariophyceae). Journal of Phycology 36: 510–522.
Lyon, B. R., J. M. Bennett-Mintz, P. A. Lee, M. G. Janech, G. R. DiTullio, B. R. Lyon, J. M. Bennett-Mintz, P. A. Lee, M. G. Janech & G. R. DiTullio, 2016. Role of dimethylsulfoniopropionate as an osmoprotectant following gradual salinity shifts in the sea-ice diatom Fragilariopsis cylindrus. Environmental Chemistry 13: 181–194.
Lyon, B. R., P. A. Lee, J. M. Bennett, G. R. DiTullio & M. G. Janech, 2011. Proteomic analysis of a Sea-Ice diatom: salinity acclimation provides new insight into the dimethylsulfoniopropionate production pathway. Plant Physiology 157: 1926–1941.
Ma, Y., E. A. Galinski, W. D. Grant, A. Oren & A. Ventosa, 2010. Halophiles 2010: life in saline environments. Applied and Environmental Microbiology 76: 6971–6981.
MacIntyre, H. L., T. M. Kana, T. Anning & R. J. Geider, 2002. Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. Journal of Phycology 38: 17–38.
Mallick, N. & F. H. Mohn, 2000. Reactive oxygen species: response of algal cells. Journal of Plant Physiology 157: 183–193.
Malviya, S., E. Scalco, S. Audic, F. Vincent, A. Veluchamy, J. Poulain, P. Wincker, D. Iudicone, C. de Vargas, L. Bittner, A. Zingone & C. Bowler, 2016. Insights into global diatom distribution and diversity in the world’s ocean. Proceedings of the National Academy of Sciences 113: 1516–1525.
Marella, T. K., I. Y. López-Pacheco, R. Parra-Saldívar, S. Dixit & A. Tiwari, 2020a. Wealth from waste: diatoms as tools for phycoremediation of wastewater and for obtaining value from the biomass. Science of the Total Environment 724: 137960.
Marella, T. K., A. Saxena & A. Tiwari, 2020b. Diatom mediated heavy metal remediation: a review. Bioresource Technology 305: 123068.
Markina, Zh. V. & N. A. Aizdaicher, 2016. The effect of lowered salinity of sea water on the growth and photosynthetic pigment content in three strains of the microalgae Pseudo-nitzschia pungens (Grunow ex. P.T. Cleve) Hasle, 1993 (Bacillariophyta). Russian Journal of Marine Biology 42: 414–418.
McLachlan, J., 1961. The effect of salinity on growth and chlorophyll content in representative classes of unicellular marine algae. Canadian Journal of Microbiology 7: 399–406.
McParland, E. L., A. Wright, K. Art, M. He & N. M. Levine, 2020. Evidence for contrasting roles of dimethylsulfoniopropionate production in Emiliania huxleyi and Thalassiosira oceanica. New Phytologist 226: 396–409.
Millan, F., C. Izere, V. Breton, O. Voldoire, D. G. Biron, C. E. Wetzel, D. Miallier, E. Allain, L. Ector & A. Beauger, 2020. The effect of natural radioactivity on diatom communities in mineral springs. Botany Letters 167: 95–113.
Miller, M. R., S. Y. Quek, K. Staehler, T. Nalder & M. A. Packer, 2014. Changes in oil content, lipid class and fatty acid composition of the microalga Chaetoceros calcitrans over different phases of batch culture. Aquaculture Research 45: 1634–1647.
Miller, R. L. & D. L. Kamykowski, 1986. Effects of temperature, salinity, irradiance and diurnal periodicity on growth and photosynthesis in the diatom Nitzschia americana; light-saturated growth. Journal of Phycology 22: 339–348.
Mishra, M., A. P. Arukha, T. Bashir, D. Yadav & G. B. K. S. Prasad, 2017. All new faces of diatoms: potential source of nanomaterials and beyond. Frontiers in Microbiology 8: 1239.
Mitra, A., S. Zaman, S. K. Ray, S. Sinha & K. Banerjee, 2012. Inter-relationship between phytoplankton cell volume and aquatic salinity in Indian Sundarbans. National Academy Science Letters 35: 485–491.
Munns, R., 2002. Comparative physiology of salt and water stress. Plant, Cell & Environment 25: 239–250.
Murugaraj, N. G. N. & S. Jeyachandran, 2007. Effect of salinity stress on the marine diatom Amphora coffeaeformis (Ag.) Kuetz (Bacillariophyceae) in relation to proline accumulation. Seaweed Research and Utilization 29: 227–231.
Nakov, T., K. J. Judy, K. M. Downey, E. C. Ruck & A. J. Alverson, 2020. Transcriptional response of osmolyte synthetic pathways and membrane transporters in a euryhaline diatom during long-term acclimation to a salinity gradient. Journal of Phycology 56: 1712–1728.
Naselli-Flores, L., T. Zohary & J. Padisák, 2021. Life in suspension and its impact on phytoplankton morphology: an homage to Colin S. Reynolds. Hydrobiologia 848: 7–30.
Navarro, F. E., M. C. Damiani, P. I. Leonardi & C. A. Popovich, 2021. Temperature and salinity effect on tolerance and lipid accumulation in Halamphora coffeaeformis: an approach for outdoor bioenergy cultures. BioEnergy Research. https://doi.org/10.1007/s12155-021-10349-2.
Nilsson, C. & K. Sundbäck, 1996. Amino acid uptake in natural microphytobenthic assemblages studied by microautoradiography. Hydrobiologia 332: 119–129.
Noune, F., N. Chaib, H. Kaddeche, S. Dzizi, S. Metallaoui & S. Blanco, 2023. Effect of salinity on valves morphology in freshwater diatoms. Environmental Monitoring and Assessment 195: 159.
Olsen, S. & E. Paasche, 1986. Variable kinetics of silicon-limited growth in Thalassiosira pseudonana (Bacillariophyceae) in response to changed chemical composition of the growth medium. British Phycological Journal 21: 183–190.
Oren, A., 1999. Bioenergetic aspects of halophilism. Microbiology and Molecular Biology Reviews 63: 334–348.
Orr, H. A., 2005. The genetic theory of adaptation: a brief history. Nature Reviews Genetics 6: 119–127.
Paasche, E., S. Johansson & D. L. Evensen, 1975. An effect of osmotic pressure on the valve morphology of the diatom Skeletonema subsalsum (A. Cleve) Bethge. Phycologia 14: 205–211.
Padisák, J., É. Soróczki-Pintér & Z. Rezner, 2003. Sinking properties of some phytoplankton shapes and relation of form resistance to morphological diversity of plankton: an experimental study. Hydrobiologia 500: 243–257.
Padisák, J. & L. Naselli-Flores, 2021. Phytoplankton in extreme environments: importance and consequences of habitat permanency. Hydrobiologia 848: 157–176.
Parida, A. K. & A. B. Das, 2005. Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety 60: 324–349.
Paul, J. S., 1979. Osmoregulation in the marine diatom Cylindrotheca fusiformis. Journal of Phycology 15: 280–284.
Pednekar, S. M., S. S. Bates, V. Kerkar & S. G. P. Matondkar, 2018. Environmental factors affecting the distribution of Pseudo-nitzschia in two Monsoonal Estuaries of Western India and effects of salinity on growth and domoic acid production by P. pungens. Estuaries and Coasts 41: 1448–1462.
Petrou, K., M. A. Doblin & P. J. Ralph, 2011. Heterogeneity in the photoprotective capacity of three Antarctic diatoms during short-term changes in salinity and temperature. Marine Biology 158: 1029–1041.
Petrou, K. & P. J. Ralph, 2011. Photosynthesis and net primary productivity in three Antarctic diatoms: possible significance for their distribution in the Antarctic marine ecosystem. Marine Ecology Progress Series 437: 27–40.
Pinseel, E., T. Nakov, K. van den Berge, K. M. Downey, K. J. Judy, O. Kourtchenko, A. Kremp, E. C. Ruck, C. Sjöqvist, M. Töpel, A. Godhe & A. J. Alverson, 2022. Strain-specific transcriptional responses overshadow salinity effects in a marine diatom sampled along the Baltic Sea salinity cline. The ISME Journal 16: 1776–1787.
Potapova, M., 2011. Patterns of diatom distribution in relation to salinity. In Seckbach, J. & P. Kociolek (eds), The Diatom World Springer, Dordrecht: 313–332.
Pourmozaffar, S., S. Tamadoni Jahromi, H. Rameshi, A. Sadeghi, T. Bagheri, S. Behzadi, M. Gozari, M. R. Zahedi & S. Abrari Lazarjani, 2020. The role of salinity in physiological responses of bivalves. Reviews in Aquaculture 12: 1548–1566.
Prestegard, S. K., G. Knutsen & L. Herfindal, 2014. Adenosine content and growth in the diatom Phaeodactylum tricornutum (Bacillariophyceae): effect of salinity, light, temperature and nitrate. Diatom Research 29: 361–369.
Radchenko, I. G. & L. V. II’yash, 2006. Growth and photosynthetic activity of diatom Thalassiosira weissflogii at decreasing salinity. Biology Bulletin 33: 242–247.
Reed, R. H., 1984. Use and abuse of osmo-terminology. Plant, Cell & Environment 7: 165–170.
Rengasamy, P., 2006. World salinization with emphasis on Australia. Journal of Experimental Botany 57: 1017–1023.
Richter, O., 1909. Zur Physiologie der Diatomeen. Die Biologie der Nitzschia putrida Benecke. Sitzungsberichte der Akademie der Wissenschaften, mathematisch-naturwissenschaftliche Klasse der Akademie der Wissenschaften, Wien.
Rijstenbil, J. W., 2003. Effects of UVB radiation and salt stress on growth, pigments and antioxidative defence of the marine diatom Cylindrotheca closterium. Marine Ecology Progress Series 254: 37–48.
Rijstenbil, J. W., 2005. UV- and salinity-induced oxidative effects in the marine diatom Cylindrotheca closterium during simulated emersion. Marine Biology 147: 1063–1073.
Rijstenbil, J. W., J. A. Wijnholds & J. J. Sinke, 1989. Implications of salinity fluctuation for growth and nitrogen metabolism of the marine diatom Ditylum brightwellii in comparison with Skeletonema costatum. Marine Biology 101: 131–141.
Roncarati, F., J. W. Rijstenbil & R. Pistocchi, 2008. Photosynthetic performance, oxidative damage and antioxidants in Cylindrotheca closterium in response to high irradiance, UVB radiation and salinity. Marine Biology 153: 965–973.
Roubeix, V. & C. Lancelot, 2008. Effect of salinity on growth, cell size and silicification of an euryhaline freshwater diatom: Cyclotella meneghiniana Kütz. Transitional Waters Bulletin 2: 31–38.
Round, F. E., R. M. Crawford & D. G. Mann, 2000. Diatoms: Biology and Morphology of the Genera, Cambridge University Press, Cambridge:
Sarno, D., W. H. C. F. Kooistra, S. Balzano, P. E. Hargraves & A. Zingone, 2007. Diversity in the genus Skeletonema (Bacillariophyceae): III. Phylogenetic position and morphological variability of Skeletonema costatum and Skeletonema grevillei, with the description of Skeletonema ardens sp. nov. Journal of Phycology 43: 156–170.
Saros, J. E. & S. C. Fritz, 2000a. Nutrients as a link between ionic concentration/composition and diatom distributions in saline lakes. Journal of Paleolimnology 23: 449–453.
Saros, J. E. & S. C. Fritz, 2000b. Changes in the growth rates of saline-lake diatoms in response to variation in salinity, brine type and nitrogen form. Journal of Plankton Research 22: 1071–1083.
Satoh, K., C. M. Smith & D. C. Fork, 1983. Effects of salinity on primary processes of photosynthesis in the red alga Porphyra perforata. Plant Physiology 73: 643–647.
Schmid, A., 1977. Morphologische und physiologische Untersuchungen an Diatomeen des Neusiedler Sees. II. licht und rasterelektronenmikroskopische Schalenanalyse der umweltabhangigen Zyklomorphose von Anomoeoneis sphaerophora (KG.) Pfitzer. Nova Hedwigia 38: 309–351.
Schmid, A.-M. M., 1984. Wall morphogenesis in Thalassiosira eccentrica: comparison of auxospore formation and the effect of MT-inhibitors. In Mann, D. G. (ed), Proceedings of the 7th International Diatom Symposium. Koeltz, Koenigstein: 47–70.
Schmid, A.-M.M., 1979. Influence of environmental factors on the development of the valve in diatoms. Protoplasma 99: 99–115.
Schmid, A.-M.M., 2009. Induction of resting-spores in the pennate diatom Navicula (Craticula) cuspidata by uncoupling of the cell and plastid cycles. Nova Hedwigia 135: 85–101.
Schobert, B., 1974. The influence of water stress on the metabolism of diatoms. I. Osmotic resistance and proline accumulation in Cyclotella meneghiniana. Zeitschrift Für Pflanzenphysiologie 74: 106–120.
Schobert, B., 1977. The influence of water stress on the metabolism of diatoms. II. Proline accumulation under different conditions of stress and light. Zeitschrift Für Pflanzenphysiologie 85: 451–461.
Schobert, B., 1980. Proline catabolism, relaxation of osmotic strain and membrane permeability in the diatom Phaeodactylum tricornutum. Physiologia Plantarum 50: 37–42.
Scholz, B. & G. Liebezeit, 2012. Compatible solutes in three marine intertidal microphytobenthic Wadden Sea diatoms exposed to different salinities. European Journal of Phycology 47: 393–407.
Schuler, M. S., M. Cañedo-Argüelles, W. D. Hintz, B. Dyack, S. Birk & R. A. Relyea, 2019. Regulations are needed to protect freshwater ecosystems from salinization. Philosophical Transactions of the Royal Society B 374: 20180019.
Schultz, M. E., 1971. Salinity-related polymorphism in the brackish-water diatom Cyclotella cryptica. Canadian Journal of Botany 49: 1285–1289.
Seckbach, J. & R. Gordon, 2019. Diatoms: Fundamentals and Applications, Scrivener Publishing LLC, Beverly:
Smayda, T. J., 1969. Experimental observations on the influence of temperature, light, and salinity on cell division of the marine diatom, Detonula confervacea (Cleve) Gran. Journal of Phycology 5: 150–157.
Søgaard, D. H., P. J. Hansen, S. Rysgaard & R. N. Glud, 2011. Growth limitation of three Arctic sea ice algal species: effects of salinity, pH, and inorganic carbon availability. Polar Biology 34: 1157–1165.
Šolić, M., J. Jug-Dujaković & N. Krstulović, 1994. Simultaneous effects of light intensity, temperature and salinity on the growth of some phytoplankton species important in aquaculture. Acta Adriatica 35: 21–26.
Steele, D. J., D. J. Franklin & G. J. C. Underwood, 2014. Protection of cells from salinity stress by extracellular polymeric substances in diatom biofilms. The Journal of Bioadhesion and Biofilm Research 30: 987–998.
Stirk, W. A., P. Bálint, D. Tarkowská, M. Strnad, J. van Staden & V. Ördög, 2018. Endogenous brassinosteroids in microalgae exposed to salt and low temperature stress. European Journal of Phycology 53: 273–279.
Struyf, E., A. Smis, S. Van Damme, P. Meire & D. J. Conley, 2009. The global biogeochemical silicon cycle. Silicon 1: 207–213.
Su, Y., N. Lundholm & M. Ellegaard, 2018. Effects of abiotic factors on the nanostructure of diatom frustules-ranges and variability. Applied Microbiology and Biotechnology 102: 5889–5899.
Sudhir, P. & S. D. S. Murthy, 2004. Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42: 481–486.
Sunda, W., D. J. Kieber, R. P. Kiene & S. Huntsman, 2002. An antioxidant function for DMSP and DMS in marine algae. Nature 418: 317–320.
Theseira, A. M., D. A. Nielsen & K. Petrou, 2020. Uptake of dimethylsulphoniopropionate (DMSP) reduces free reactive oxygen species (ROS) during late exponential growth in the diatom Thalassiosira weissflogii grown under three salinities. Marine Biology 167: 127.
Thessen, A. E., Q. Dortch, M. L. Parsons & W. Morrison, 2005. Effect of salinity on Pseudo-nitzschia species (Bacillariophyceae) growth and distribution. Journal of Phycology 41: 21–29.
Tipping, E., A. P. Jarvis, M. G. Kelly, S. Lofts, F. L. Merrix & S. J. Ormerod, 2009. Ecological Indicators for Abandoned Mines, Phase 1: Review of the Literature, Environment Agency, Bristol:
Torgan, L. C., V. Becker & C. B. Dos Santos, 2009. Skeletonema potamos (Bacillariophyta) in Patos Lagoon, southern Brazil: taxonomy and distribution. Revista Peruana De Biología 16: 93–96.
Tréguer, P., C. Bowler, B. Moriceau, S. Dutkiewicz, M. Gehlen, O. Aumont, L. Bittner, R. Dugdale, Z. Finkel, D. Iudicone, O. Jahn, L. Guidi, M. Lasbleiz, K. Leblanc, M. Levy & P. Pondaven, 2018. Influence of diatom diversity on the ocean biological carbon pump. Nature Geoscience 11: 27–37.
Trobajo, R., E. J. Cox & X. D. Quintana, 2004. The effects of some environmental variables on the morphology of Nitzschia frustulum (Bacillariophyta), in relation its use as a bioindicator. Nova Hedwigia 79: 433–445.
Trobajo, R., L. Rovira, D. G. Mann & E. J. Cox, 2011. Effects of salinity on growth and on valve morphology of five estuarine diatoms. Phycological Research 59: 83–90.
Tuchman, M. L., E. Theriot & E. F. Stoermer, 1984. Effects of low level salinity concentrations on the growth of Cyclotella meneghiniana Kütz. (Bacillariophyta). Archiv Für Protistenkunde 128: 319–326.
Tuchman, N. C., 1996. The role of heterotrophy in algae. In Stevenson, R. J., M. L. Bothwell & R. L. Lowe (eds), Algal Ecology: Freshwater Benthic Ecosystems Academic Press, Amsterdam: 299–319.
Underwood, G. J. C. & S. N. Aslam, 2015. Adaptation of diatom extracellular polymeric substance (EPS) production in response to temperature and salinity stress in Sea Ice environments. European Journal of Phycology 50: 76–76.
Underwood, G. J. C., M. Boulcott, C. A. Raines & K. Waldron, 2004. Environmental effects on exopolymer production by marine benthic diatoms: dynamics, changes in composition, and pathways of production. Journal of Phycology 40: 293–304.
Underwood, G. J. C. & D. M. Paterson, 2003. The importance of extracellular carbohydrate productionby marine epipelic diatoms. Advances in Botanical Research 40: 183–240.
Van Bergeijk, S. A., C. Van der Zee & L. J. Stal, 2003. Uptake and excretion of dimethylsulphoniopropionate is driven by salinity changes in the marine benthic diatom Cylindrotheca closterium. European Journal of Phycology 38: 341–349.
Vrieling, E. G., Q. Sun, M. Tian, P. J. Kooyman, W. W. C. Gieskes, R. A. van Santen & N. A. J. M. Sommerdijk, 2007. Salinity-dependent diatom biosilicification implies an important role of external ionic strength. Proceedings of the National Academy of Sciences 104: 10441–10446.
Weig, A., C. Deswarte & M. J. Chrispeels, 1997. The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiology 114: 1347–1357.
Welsh, D. T., 2000. Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiology Reviews 24: 263–290.
Wendker, S., 1990. Morphologische Untersuchungen an Populationen aus dem Formenkreis um Nitzschia frustulum (Kützing) Grunow. Diatom Research 5: 179–187.
Wendker, S. & U. Geissler, 1988. Investigations on valve morphology of two Nitzschia lanceolatae. In Round, F. E. (ed), Proceedings of the 9th International Diatom Symposium. Biopress, Bristol: 469–480.
Wilhelm, C., C. Büchel, J. Fisahn, R. Goss, T. Jakob, J. Laroche, J. Lavaud, M. Lohr, K. Stehfest, K. Valentin & P. G. Kroth, 2006. The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist 2006(157): 91–124.
Ziemann, H., 1967. Die Wirkung der Kaliabwässer auf die Flora und Fauna der Gewässer unter besonderer Berücksichtigung der Werra und Wipper. Fortschrifte Der Wasserchemie Und Ihrer Grenzgebiete 7: 50–80.
Acknowledgements
The authors of present research were supported by the National Laboratory for Water Science and Water Safety program (RRF-2.3.1-21-2022-00008) from the National Research, Development and Innovation Office (JP, CS-K, GBS, EL); by the National Research, Development and Innovation Office (NKFIH) – K119208 (KB), KKP 144068 (CS-K, JP, EL); by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences – BO-00458-20-8 (VB-B); by the New National Excellence Program of the Ministry for Innovation and Technology from the Source of the National Research, Development and Innovation Fund – ÚNKP-21-5 (VB-B), ÚNKP-22-3-II-PE-11 (TJA-I); and by the Center for Ecological Research – BA4902/21 (Riverine Project) (VB-B, KB).
Funding
Open access funding provided by University of Pannonia. This project was financially supported by the National Research, Development and Innovation Office – NKFIH—K137950 (CS-K) and FK132142 (VB-B).
Author information
Authors and Affiliations
Contributions
The concept, the structure, and drafting the key issues of this paper were developed by CS-K and EL. All other authors contributed equally by writing sections commenting on others, adding details.
Corresponding author
Ethics declarations
Conflict of interest
The co-author Judit Padisák is an Associate Editor of Hydrobiologia and a guest editor of this volume; therefore, she cannot participate in processing of this paper.
Ethical approval
Ethical and professional principles were completely followed.
Additional information
Handling editor: Sidinei M. Thomaz
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Guest editors: Erik Jeppesen, Miguel Cañedo-Argüelles, Sally Entrekin, Judit Padisák & S.S.S. Sarma / Effects of induced changes in salinity on inland and coastal water ecosystems
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Stenger-Kovács, C., Béres, V.B., Buczkó, K. et al. Review of phenotypic response of diatoms to salinization with biotechnological relevance. Hydrobiologia 850, 4665–4688 (2023). https://doi.org/10.1007/s10750-023-05194-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-023-05194-7