Abstract
In coastal zones, salinity is commonly a rather local environmental factor that can be highly variable. Future climate change scenarios indicate for many coastal regions besides warming also changes in current salinity regime due to less precipitation, higher evaporation, or more freshwater run-off, resulting in decreasing or increasing saline conditions. The soft bottom of shallow water coastal zones is typically inhabited by benthic diatoms which cover as photosynthetic biofilms extensive areas of sediments. Cylindrotheca closterium is a cosmopolitan and abundant taxon of such communities, and is widely used as a benthic diatom model system. Nevertheless, comprehensive ecophysiological data on the salinity tolerance of this ecologically important benthic species are still missing. Therefore, the main goal was to investigate the salinity tolerance in 6 strains of C. closterium from 5 different clades and from marine to brackish habitats. An analysis of growth as function of salinity allowed the evaluation of tolerance limits, growth optima, and acclimation abilities of individual strains. The data documented isolate-specific growth response patterns and rather broad tolerance widths among the six strains of C. closterium, which point to strong genotypic differentiation. The results of the phylogenetic network analysis indicate several well separated grades within C. closterium, thereby supporting the earlier suggestion of a cryptic species complex.
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References
Apoya-Horton MD, Yin L, Underwood GJ, Gretz MR (2006) Movement modalities and responses to environmental changes of the mudflat diatom Cylindrotheca closterium (Bacillariophyceae). J Phycol 42:379–390
Araújo CV, Romero-Romero S, Lourençato LF, Moreno-Garrido I, Blasco J, Gretz MR, Moreira-Santos M, Ribeiro R (2013) Going with the flow: detection of drift in response to hypo-saline stress by the estuarine benthic diatom Cylindrotheca closterium. PloS One 8:e81073
Armbrust EV (2009) The life of diatoms in the world’s oceans. Nature 459:185–192
Balzano S, Sarno D, Kooistra WHCF (2011) Effects of salinity on the growth rate and morphology of ten Skeletonema strains. J Plankton Res 33:937–945
Brand LE (1984) The salinity tolerance of forty-six marine phytoplankton isolates. Estuar Coast Shelf Sci 18:543–556
Cahoon LB (1999) The role of benthic microalgae in neritic ecosystems. Oceanogr Mar Biol Annu Rev 37:47–86
Casteleyn G, Leliaert F, Backeljau T, Debeer AE, Kotaki Y, Rhodes L, Vyverman W (2010) Limits to gene flow in a cosmopolitan marine planktonic diatom. Proc Natl Acad Sci USA 107:12952–12957
Cermeño P, Falkowski PG (2009) Controls on diatom biogeography in the ocean. Science 325:1539–1541
Clavero E, Hernández-Mariné M, Grimalt JO, Garcia-Pichel F (2000) Salinitry tolerance of diatoms from thalassic hypersaline environments. J Phycol 36:1021–1034
Clement M, Snell Q, Walke P, Posada D, Crandall K (2002) TCS: estimating gene genealogies. Proc 16th Int Parallel Distrib Process Symp 2:184
De Brouwer JD, Wolfstein K, Ruddy GK, Jones TER, Stal LJ (2005) Biogenic stabilization of intertidal sediments: the importance of extracellular polymeric substances produced by benthic diatoms. Microb Ecol 49:501–512
De Miranda M, Gaviano M, Serra E (2005) Changes in the cell size of the diatom Cylindrotheca closterium in a hyperhaline pond. Chem Ecol 21:77–81
Degerlund M, Huseby S, Zingone A, Sarno D, Landfald B (2012) Functional diversity in cryptic species of Chaetoceros socialis Lauder (Bacillariophyceae). J Plankton Res 34:416–431
Gilstad M, Sakshaug E (1990) Growth rates of ten diatom species from the Barents Sea at different irradiances and day lengths. Mar Ecol Prog Ser 64:169–173
Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Springer, Boston, pp 29–60
Gustavs L, Schumann R, Eggert A, Karsten U (2009) In vivo growth fluorometry: accuracy and limits of microalgal growth rate measurements in ecophysiological investigations. Aquat Microb Ecol 55:95–104
Karsten U (2012) Seaweed acclimation to salinity and desiccation stress. In: Wiencke C, Bischof K (eds) Seaweed biology – novel insights into ecophysiology, ecology and utilization. Springer, Berlin, p 87–107
Kooistra WHCF, Sarno D, Balzano S, Gu H, Andersen RA, Zingone A (2008) Global diversity and biogeography of Skeletonema species (Bacillariophyta). Protist 159:177–193
Lüning K (1990) Seaweeds. Seaweeds. Their Environment, Biogeography, and Ecophysiology. John Wiley & Sons Ltd., Chichester, p 544
Malviya S, Scalco E, Audic S, Vincent F, Veluchamy A, Poulain J et al (2016) Insights into global diatom distribution and diversity in the world’s ocean. Proc Natl Acad Sci USA 113:1516–1525
Najdek M, Blazina M, Djakovac T, Kraus R (2005) The role of the diatom Cylindrotheca closterium in a mucilage event in the northern Adriatic Sea: coupling with high salinity water intrusions. J Plankton Res 27:851–862
Rad-Menéndez C, Stanley M, Green DH, Cox EJ, Day JG (2015) Exploring cryptic diversity in publicly available strains of the model diatom Thalassiosira pseudonana (Bacillariophyceae). J Mar Biol Assoc UK 95:1081–1090
Rijstenbil JW (2005) UV- and salinity induced oxidative effects in the marine diatom Cylindrotheca closterium during simulated emersion. Mar Biol 147:1063–1073
Roncarati F, Rijstenbil JW, Pistocchi R (2008) Photosynthetic performance, oxidative damage and antioxidants in Cylindrotheca closterium in response to high irradiance, UVB radiation and salinity. Mar Biol 153:965–973
Scholz B, Liebezeit G (2012) Growth responses of 25 benthic marine Wadden Sea diatoms isolated from the Solthörn tidal flat (southern North Sea) in relation to varying culture conditions. Diatom Res 27:65–73
Stock W, Vanelslander B, Rüdiger F, Sabbe K, Vyverman W, Karsten U (2019) Thermal niche differentiation in the benthic diatom Cylindrotheca closterium (Bacillariophyceae) complex. Front Microbiol 10:1395
Underwood GJC, Kromkamp JC (1999) Primary production by phytoplankton and microphytobenthos in estuaries. Adv Ecol Res 29:93–153
Underwood GJC, Provot L (2000) Determining the environmental preferences of four epipelic diatom taxa: growth across a range of salinities, nitrate and ammonium conditions. Eur J Phycol 35:173–182
Van Bergeijk SA, Van der Zee C, Stal LJ (2003) Uptake and excretion of dimethyl-sulphoniopropionate is driven by salinity changes in the marine benthic diatom Cylindrotheca closterium. Eur J Phycol 38:341–349
Van Damme S, Struyf E, Maris T, Ysebaert T, Dehairs F, Tackx M, Heip C, Meire P (2005) Spatial and temporal patterns of water quality along the estuarine salinity gradient of the Scheldt estuary (Belgium and The Netherlands): results of an integrated monitoring approach. Hydrobiologia 540:29–45
Vanelslander B, De Wever A, Van Oostende N, Kaewnuratchadasorn P, Vanormelingen P, Hendrickx F et al (2009) Complementarity effects drive positive diversity effects on biomass production in experimental benthic diatom biofilms. J Ecol 97:1075–1082
Vanormelingen P, Vanelslander B, Sato S, Gillard J, Trobajo R, Sabbe K, Vyverman W (2013) Heterothallic sexual reproduction in the model diatom Cylindrotheca. Eur J Phycol 48:93–105
von Quillfeldt CH, Ambrose WG Jr, Clough LM (2003) High number of diatom species in first-year ice from the Chukchi Sea. Polar Biol 26:806–818
Vuorinen I, Hänninen J, Rajasilta M, Laine P, Eklund J, Montesino-Pouzols F, Corona F, Junker K, Meier HEM, Dippner JW (2015) Scenario simulations of future salinity and ecological consequences in the Baltic Sea and adjacent North Sea areas–implications for environmental monitoring. Ecol Indic 50:196–205
Wolfstein K, Stal LJ (2002) Production of extracellular polymeric substances (EPS) by benthic diatoms: effect of irradiance and temperature. Mar Ecol Prog Ser 236:13–22
Wright DG, Pawlowicz R, McDougall TJ, Feistel R, Marion GM (2010) Absolute salinity, “density salinity” and the reference-composition salinity scale: present and future use in the seawater standard TEOS-10. Ocean Sci Discuss 7:1559–1625
Acknowledgments
The authors gratefully acknowledge the provision of diatom strains by J. Woelfel, B. Vanelslander, and I. Moreno-Garrido. We are grateful to F. Rüdiger who performed part of the ecophysiological experiments. The work on the Spitsbergen isolate has been performed at the Ny-Ålesund International Arctic Environmental Research and Monitoring Facility and under the agreement on scientific cooperation between the Alfred Wegener Institute and the University of Rostock. The authors thank the crew at the AWIPEV-base in Ny-Ålesund and the German dive team (Anita Flohr, Peter Leopold, Max Schwanitz) for assistance in the field, sample collection, and further support, as well as Juliane Müller for maintaining the stock collection of Arctic benthic diatoms at the University of Rostock.
Funding
The research of K. Glaser was funded by the DFG priority program 1991 “Taxonomics” (GL 909/1-1, K.G.), that of U. Karsten by the DFG priority program 1158 “Antarctic Research” (DFG, KA899/12, KA899/15).
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Glaser, K., Karsten, U. Salinity tolerance in biogeographically different strains of the marine benthic diatom Cylindrotheca closterium (Bacillariophyceae). J Appl Phycol 32, 3809–3816 (2020). https://doi.org/10.1007/s10811-020-02238-6
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DOI: https://doi.org/10.1007/s10811-020-02238-6