Advertisement

Hydrobiologia

, Volume 800, Issue 1, pp 145–154 | Cite as

Tracing particulate matter and associated microorganisms in freshwaters

  • Stefano AmalfitanoEmail author
  • Gianluca Corno
  • Ester Eckert
  • Stefano Fazi
  • Shira Ninio
  • Cristiana Callieri
  • Hans-Peter Grossart
  • Werner Eckert
TRENDS IN AQUATIC ECOLOGY II Review Paper

Abstract

Sediment resuspension represents a key process in all natural aquatic systems, owing to its role in nutrient cycling and transport of potential contaminants. Although suspended solids are generally accepted as an important quality parameter, current monitoring programs cover quantitative aspects only. Established methodologies do not provide information on origin, fate, and risks associated with uncontrolled inputs of solids in waters. Here we discuss the analytical approaches to assess the occurrence and ecological relevance of resuspended particulate matter in freshwaters, with a focus on the dynamics of associated contaminants and microorganisms. Triggered by the identification of specific physical–chemical traits and community structure of particle-associated microorganisms, recent findings suggest that a quantitative determination of microorganisms can be reasonably used to trace the origin of particulate matter by means of nucleic acid-based assays in different aquatic systems.

Keywords

Total suspended solids Resuspended particulate Turbidity Sediment traps Particle-associated microorganisms Pathogens 

Introduction

Freshwater particulate matter (PM) refers to the bulk inorganic and organic non-dissolved material, which stays suspended in waters of streams, rivers, lakes and reservoirs, e.g., by turbulence (Chapman, 1996). Conventionally characterized as particles with a nominal diameter larger than 0.45 µm, PM represents a fundamental structural component in freshwaters and an important quality parameter in current monitoring plans worldwide (Bartram & Ballance, 1996). PM acts as both source and sink for nutrients and contaminants, therefore, knowledge concerning particle dynamics and inflow, suspended matter concentration, sinking flux, resuspension and settling processes has become crucial for environmental impact studies and watershed models aimed at optimizing water resource management at a catchment level (Grathwohl et al., 2013). The direct impact on human activities is obvious, since turbid waters can, e.g., reduce underwater visibility, adversely affect recreational uses, contribute to clogging tanks and pipes in industrial settings, erode impellers of pumps and can cause damage to water-treating machines. Moreover, PM sedimentation and accumulation in reservoirs gradually reduce the water storage capacity, and probably represent the most serious technical problem faced by the dam industry (Fox et al., 2016).

An increase in turbidity is also associated with potential pollution risks and human health-related issues, in particular when contaminated sediments are frequently resuspended, since pollutants of various origins can be transported in association with suspended particles and follow their remobilization/sedimentation dynamics in water (Mahler et al., 2000; Bai & Lung, 2005). Many countries and organizations have established recommended turbidity levels assessed on site by probe-based techniques, such as sensors measuring the light scattering properties of the particles in liquid. Beside the traditional assessment by Secchi disk, total suspended solids (TSS in mg/l) and turbidity (nephelometric turbidity units—NTU) are common PM-related indicators of water quality (Kemker, 2014). The most accurate but time-consuming method of quantifying suspended solids in a water sample is filtering, drying, and weighing (ISO5667-3, 2012). TSS can also be estimated directly from turbidity sensors, upon linear regression modeling, and calculation for each sampling period and location (Bertrand-Krajewski, 2004). According to European water directives, member states should strive for a parametric value not exceeding 1 NTU upon surface water treatment, and 0.2 NTU in the case of drinking water (European Union, 1998; European Communities Environmental Objectives, 2009; Official Journal of the European Union, 2009). Turbidity levels below 1 NTU are generally recommended for human consumption, while a level of 5 NTU or lower is acceptable for recreational purposes according to the American Water Works Association (Bartram & Ballance, 1996).

Unlike the impact on human-related issues, consequences of high and highly variable turbidity levels on aquatic ecosystem functioning are multiple, site-specific, and rather unpredictable from an ecological point of view (Bilotta & Brazier, 2008). Physical and chemical conditions may be completely altered by reduced light penetration, unsuitable for efficient photoautotrophic metabolic processes of planktonic and benthic organisms (Sobolev et al., 2009). It was also reported that PM-associated toxicants can be harmful for aquatic life (Gordon & Palmer, 2015; Quinteiro et al., 2015). In contrast, PM-associated nutrients and organic matter such as proteins can stimulate microbial growth and facilitate development of algal blooms (Cole et al., 2006).

The contrasting ecological effects of freshwater PM inputs are even exacerbated when referring to climate change models, by which extreme weather events (e.g., drought, storms, heavy rains) are expected to increase in intensity and frequency in near future (García-Ruiz et al., 2011; Coumou & Rahmstorf, 2012). When extended dry periods are followed by extreme rain events (i.e., a global-warming scenario in arid and semi-arid regions worldwide), both solutes and particle fluxes increase dramatically for a short period, thus impairing water quality for aquatic life and/or humans, and increasing flooding risks (Wood, 2014; Butturini et al., 2016; Ejarque et al., 2017; Vercruysse et al., 2017).

Nowadays, PM quantification with established methodologies does not offer detailed indications on origins and risks associated with uncontrolled inputs of solids in waters. One of the on-going tasks for limnologists is to determine the dynamics and fate of suspended PM (e.g., allochthonous vs. autochthonous, allogenic vs. authigenic). The ability to distinguish settling authigenic particles from those originating from bottom sediment resuspension represents a prerequisite to assess the ecological relevance of PM in aquatic systems and to distinguish its functional relevance. However, there is a lack of literature in this regard, and consideration of PM in either fundamental ecological theories or current monitoring plans rarely exceeds the black-box parameter, termed turbidity.

This article presents an approach on how our knowledge of PM could be considerably improved by studying particle-associated microorganisms. Assuming that specific physiological traits and community structure vary depending on PM origin, their analysis could play a key role in defining potential biomarkers that will allow resuspended sediment particles to be identified within the bulk particulate load in freshwater systems.

Origin, fate, and significance of resuspended particulate matter in freshwaters

Suspended particles can originate from different processes (e.g., resuspension, erosion, runoff, discharge, flocculation, algal blooms, microbial aggregation), all of which contribute to determine their physical (e.g., particle size and morphology), chemical (e.g., organic and inorganic components), and biological properties (e.g., associated biofilm and microorganisms). The most common method to estimate the contribution of sediment resuspension to the total settling flux is to deploy sediment traps at various depths and to compare the measured particle flux in bottom and epilimnion traps (Rosa, 1985; Bloesch & Uehlinger, 1986). Gasith (1975) used the organic matter fraction of seston as an indicator for resuspension by comparing it to tripton and to the amount of inorganic settling material. A second parameter likely to reveal differences between resuspended and authigenic material is the chemical composition of collected particles. Previous studies aimed at the different particulate phosphorus (PP) fractions in seston and sediments indicating that settling matter is relatively enriched in labile and organic PP when compared to the P-distribution in the sediment (Eckert et al., 2003; Eckert & Nishri, 2014). To which extent this difference can be useful in the resuspension studies on P-pool is a matter of debate. Bloesch (1994) concluded that for reliable in situ studies a combination of sediment traps, sediment cores, near bottom current meters, and turbidity meters need to be employed to better measure the occurrence of suspended particulate matter. Other authors explained resuspension as the difference between sediment trap catch and bottom sediment accumulation (Dillon et al., 1990).

An advanced approach for measuring and modeling resuspension is based on the detection of radionuclides and stable isotopes (Bloesch, 1994; Cornett et al., 1994). Cesium (137Cs) accumulates in sediments, thus an increase of its activity in the PM fraction let infer for resuspension (Ritchie & McHenry, 1990). Beryllium (7Be) decays rapidly in sediments and it is typically indicative for fresh settled material (Fitzgerald et al., 2001). Thorium isotopes (e.g., 228Th, 230Th) give indications of autochthonous sinking particles (Yang et al., 2013). Although the list of informative PM-related isotopes is rather long, all these approaches are mainly based on empirical considerations with the lack of explicit tracers and means to specifically distinguish between authigenic and resuspended material.

In rivers and shallow lakes, bottom sediment resuspension has long been recognized as the most important factor providing PM to the water column, and its quantification as a critical precondition for the understanding of biogeochemical processes, modeling, and restoration actions (Weyhenmeyer, 1996; Hakanson, 2004; Kleeberg et al., 2013). In large deep lakes, the nearshore sediment resuspension, focusing, and settling are the main processes responsible for particle dynamics in deep layers (Bloesch, 1995). By comparing different aquatic systems all over the US, Evans (1994) estimated a long-term contribution of resuspended material to the total PM flux of about 85%. Weyhenmeyer (1996) calculated a value close to 75% in seven Swedish lakes. Koski-Vähälä et al. (2000) estimated the portion of resuspended matter in a Finnish lake from 56 to 99% of the gross sedimentation.

The extent of resuspension depends on many physical, chemical, and biological properties, and contribution to particle settling flux can vary greatly among aquatic systems with different geomorphologies and at different times of the year. In general, the effects of sediment remobilization processes are case sensitive and site-specific (Evans, 1994). For example, wind-driven surface waves can promote sediment resuspension in all exposed surfaces of shallow lakes, but only in nearshore areas of deep lakes (Hamilton & Mitchell, 1996; Reardon et al., 2016).

Stream flows and subsurface currents are generally sufficient to remobilize unconsolidated sediments when bottom shear exceeds the critical shear velocity (Evans, 1994). Thus, any additional factor upholding particle cohesiveness at the sediment–water interface can effectively absorb turbulent energy and increase critical shear stress limits (Grabowski et al., 2011). By coating sediment grains and bridging interstitial pores, intra-sediment biofilms and extracellular polymeric substances (EPS) were reported to modify hydraulic properties of cohesive sediments (Staats et al., 2000; Romani et al., 2013; Gerbersdorf & Wieprecht, 2015), with a 150% increase in erosion threshold where the benthic microbial assemblages consisted of diatoms and bacteria (Lundkvist et al., 2007). Microbial adhesiveness, arising from EPS secretion, was reported to lead to a cohesive network in river sediments under variable hydrological regimes (Gerbersdorf et al., 2009; Kleeberg et al., 2013). Thus, the contribution of microbes to the overall sediment cohesiveness is by far relevant and could be also theorized within the classical sedimentology models (Fig. 1).
Fig. 1

Hjulström’s diagram showing how freshwater sediments behave at varying grain size and water turbulence. Sediment particles are mobilized and transported when turbulence exceeds the settling velocity (lower solid curve). Particle resuspension in water occurs over a critical shear velocity (upper solid curve) that depends on sediment cohesiveness. Clay and silt require considerably higher velocities for resuspension than for transportation, because of a stronger electrostatic attraction in comparison to that among coarser particles. The microbial adhesiveness (dashed curve), arising from EPS secretion and biofilm growth, can increase sediment cohesion (gray area) by progressively coating finer particles and bridging smaller interstitial pores (adapted from Hjulström, 1935)

Resuspended particles as vehicle for microbial propagation

Kleeberg et al. (2013) reported that numbers of particle-associated bacteria directly followed PM dynamics in a resuspension experiment of river sediments. Consequently, hydrodynamic forces to entrain particle-associated bacteria equaled those necessary to resuspended cohesive sediments. Moreover, when rapidly settling particles overtake and intercept more slowly sinking particles, both will collide if the distances of their flow streamlines are smaller than the sum of the particle radii. As a result, scavenging of small particles will occur (Kepkay, 1994) and free-living bacteria will be lost via settling. On the other hand, sediment-borne microorganisms can even survive in open waters when associated to particles thanks to favorable ecological conditions (e.g., limited competition for nutrients, optimal light exposure, cooperation favored by cells proximity), thus finding transitorily opportunities for dispersal (Drummond et al., 2015). Sediment resuspended particles can constitute “hot-spots” for microbial growth and intimate associations among microorganisms with different functions, as it was reported for planktonic microbial aggregates (Simon et al., 2002; Wotton, 2007; Lyons et al., 2010). Compared to the pelagic zone (free-water), particle-associated bacteria might have a selective advantage due to higher nutrient and organic matter availability similar to biofilm-like structures (Hall-Stoodley & Stoodley, 2005; Grossart, 2010). It was found that stream biofilms and aggregates form distinct communities under varying hydraulic conditions, with higher number of resident taxa associated with aggregate communities (Niederdorfer et al., 2016). Owing to improved light exposure, photoautotrophic cells can grow on particle surfaces and contribute to foraging heterotrophic microbial biomass development (Battin et al., 2003; Romani et al., 2013).

Moreover, the vicinity in which bacteria can grow on particles allows horizontal transferring of genetic material between microorganisms and might enable a persistence of resistance genes, including those of human health-related concern (Costerton, 1999; Allen et al., 2010). The spread and persistence of antibiotic-resistant bacteria and resistance genes in suspended aggregates was reported recently (Corno et al., 2014). Such multi-resistant bacteria might be remobilized with sediments, since sediments harbor heavy metal contaminations, which can select for heavy metal resistance genes that can co-occur with antibiotic resistance genes (Di Cesare et al., 2016a, b). It is worth noting that suspended aggregates and particles may also offer protection to microbial species susceptible to stressing factors, such as chemical disinfectants, high PAR radiation, UV radiation, and predation pressure (Mamane, 2008; Callieri et al., 2011; Tang et al., 2011; Callieri et al., 2016a).

Consequently, typical PM-associated microorganisms may also comprise human pathogens such as Vibrio cholerae, Salmonella spp., Shigella spp., and diarrheagenic strains of Escherichia coli, and toxic cyanobacteria that can grow and persist when attached to particles (Du Preez et al., 2010; Singh et al., 2010; Walters et al., 2014). Turbid waters, whether due to organic or inorganic material, cannot be easily sanitized by conventional treatments (e.g., chlorination, UV irradiation, heating), as the suspended particles can “hide” microbial pathogens and invasive species (Amalfitano et al., 2015), thus causing great concerns from PM contaminated waters (Tang et al., 2011; Edge et al., 2013; Jacob et al., 2015). Higher concentrations of Enterococcus sp. and E. coli coincided with the increase in particles following resuspension of sediments during storm events (Fries et al., 2006). Stormwater-suspended particles were found to prolong survival of fecal indicator organisms for several days prior to reduction to background levels (Jeng et al., 2005). It was postulated that the risk of an E. coli infection increases approximately tenfold if there is a disturbance of sediments, because attached bacteria are more persistent within the aquatic environment than free-floating bacteria (Abia et al., 2016). A further critical factor in determining human health risk is the partitioning of bacterial pathogenic organisms between particle-attached and free-living cells in the water column (Colwell et al., 1985; Characklis et al., 2005; Fries et al., 2006). Regrettably, such effects are largely disregarded because current regulations for microbiological quality evaluations are based on standardized cultivation techniques and set on the number of microorganisms (e.g., heterotrophic plate count and coliforms), regardless of how many cells are found attached on particles.

Detection of particle-associated microorganisms and indicator taxa of sediment resuspension

Although several studies have identified association with PM as a critical factor in predicting the transport and fate of aquatic microorganisms, no generally accepted method exists for identifying the particle-associated microbial fraction emanating from sediment resuspension. A large body of studies has traditionally attempted to classify planktonic microorganisms into particle-attached and free-living cells by using a one-size filtration to separate the two fractions (Crump et al., 1999; Riemann & Winding, 2001; Grossart, 2010; Ortega-Retuerta et al., 2013; Rieck et al., 2015). By claiming the lack of consensus on the filter pore-size, studies tested different sized filters to fractionate bacterioplankton samples and showed that the phylogenetic composition of the particle-associated bacterial community differed among the filtered size fractions (Zhang et al., 2016; Mestre et al., 2017). The centrifugation approach was also reported as a reasonable means of separating settling particles and associated microbes from free-living ones, and allowed assessing that the fraction of PM-associated microorganisms varied by the type of microbes (Characklis et al., 2005). Overall, numerous findings suggest that existing methodologies and data published to-date might not be definitive with respect to all of the states in which PM-interacting microbial cells may exist in aquatic systems. Thus, an urgent task will be to test novel advanced approaches to physically separate floating particles with different properties and origins prior to any further microbiological analysis.

Among the promising technologies readily applicable to partly address this methodological gap, flow cytometry has been proven as a suitable tool to monitor the dynamics of free-living microbes and microbially colonized particles in natural and engineered aquatic systems (Boi et al., 2016; Casentini et al., 2016; Liu et al., 2016). Because hundreds of thousands of events can be analyzed in a few minutes with a large statistical significance, flow cytometry can reduce the analytical time and increase the accuracy needed for cell and particle quantification. The capability of resolving particle-associated fluorescence induced by attached microbial cells, simultaneously offering the possibility to physically identify targeted events (Gasol & Moran, 2015), makes the technique promising for the characterization of suspended sediment particles. Similarly, but yet with very limited applicability to environmental studies, rapid microfluidic-based technologies, in combination with emulsion oil droplet and other entrapping procedures, were used to characterize particles in a liquid suspension according to their size and chemical properties (Sajeesh & Sen, 2014). Discrimination and separation of different PM fractions can also be critical to identify specific interactions between microbes and particles by the large suite of microscopy applications, spanning from epifluorescence microscopy to further high-resolution techniques including electron microscopy (transmission, TEM; and scanning, SEM) and scanning-proximity probe microscopy (atomic force microscopy, AFM) (Ransom et al., 1999; Malfatti & Azam, 2009).

Furthermore, over the last years, descriptive and comparative genomics contributed to shed light on the genetic bases and the functional processes involved in cell-to-particle associations. Molecular microbiological methods based on nucleic acid (DNA and RNA) analysis can simultaneously yield information about the in situ distribution and activities of multiple microbial groups. Bacterial colonization of authigenic limnetic organic aggregates has been studied intensively in the past decades indicating a dominance of Alpha- and Beta-Proteobacteria and to a minor extend of Gamma-Proteobacteria or Actinobacteria (Grossart & Simon, 1998; Kiørboe et al., 2002; Simon et al., 2002; Niederdorfer et al., 2016). This observation is so far relevant to resuspension studies as the presence of sediment specific microbial consortia in planktonic material can represent a potential indicator for PM resuspension (Rink et al., 2008; Kleeberg et al., 2013) (Fig. 2). According to the relative increase of Thaumarchaeota found in the deep hypolimnion of six subalpine lakes (Callieri et al., 2016b), Thaumarchaeota of MG1 group were proposed as one possible “microbial tracer” of lake deep layers, in which riverine PM inputs are more likely to be collected (Coci et al., 2015).
Fig. 2

Schematic cross section view of a freshwater system. Settling and resuspension dynamics of particulate matter (PM) depend on e.g., water turbulence, allochthonous inputs, and sediment properties. Aquatic microorganisms, with specific functional and phylogenetic traits, colonize and mediate the interaction among different PM fractions in the water column. The presence of sediment specific microbial tracers can represent a potential indicator for the distinction between authigenic and resuspended PM

The presence of sulfate-reducing bacteria (SRB belonging to Delta-Proteobacteria) was verified either in aggregates or in the uppermost oxic sediment layers of different environments (Sass et al., 1997; Grossart & Ploug, 2000; Freese et al., 2008; Freixa et al., 2016). Studies on the microbial community structure in the anoxic sulfate-reducing and methanogenic sediment layers of deep lakes demonstrated PCR-based techniques as useful methods to rapidly quantify bacterial and archaeal cell numbers in surface layers of bottom sediments (Schwarz et al., 2007a, b; Frindte et al., 2016). The results pointed towards Delta-Proteobacteria (i.e., sulfate reducers and syntrophs), and to Methanomicrobiales and Methanosaeta (i.e., hydrogenotrophic and acetoclastic methanogens) as the dominant groups within the sediment bacterial and archaeal communities (MacGregor et al., 2001; Briée et al., 2007; Frindte et al., 2015). These findings suggest that a quantitative determination of a bottom sediment specific phylogenic group of microorganisms, such as SRB or Methanogens, can be used to trace the origin of PM by means of nucleic acid-based assays. By using metagenomic analysis of PM-associated microbial communities together with chemical characterization of the particles themselves, a specific or universal indicator may emerge that will allow for the distinction between authigenic and resuspended particles.

Conclusions

Despite the growing awareness of the importance of suspended particles in aquatic systems, the knowledge on factors and conditions favoring sediment resuspension and, hence, the presence of PM-associated bacteria is still very limited. Consequently, it is necessary to further investigate the dynamics of suspended particles and their associated microorganisms in aquatic systems, and those factors potentially able to promote growth and distribution of pathogenic bacteria. When exploring aquatic systems increasingly subjected to contrasting local and climate conditions, PM-targeting surveys can contribute to address fundamental ecological assumptions in linking water and sediment processes, to provide a novel glimpse of potential physical, chemical, and microbiological threats associated with sediment resuspension events, and to help the implementation of control measures for improved resource management actions.

Notes

Acknowledgements

This work was partially supported by the Short-Term Mobility programme of the CNR (Italy). HPG was supported by two Grants from the German Science Foundation (DFG GR1540/23-1 and GR1540/28-1).

References

  1. Abia, A. L. K., E. Ubomba-Jaswa, B. Genthe & M. N. B. Momba, 2016. Quantitative microbial risk assessment (QMRA) shows increased public health risk associated with exposure to river water under conditions of riverbed sediment resuspension. Science of The Total Environment 566: 1143–1151.CrossRefPubMedGoogle Scholar
  2. Allen, H. K., J. Donato, H. H. Wang, K. A. Cloud-Hansen, J. Davies & J. Handelsman, 2010. Call of the wild: antibiotic resistance genes in natural environments. Nature Reviews Microbiology 8: 251–259.CrossRefPubMedGoogle Scholar
  3. Amalfitano, S., M. Coci, G. Corno & G. M. Luna, 2015. A microbial perspective on biological invasions in aquatic ecosystems. Hydrobiologia 746: 13–22.CrossRefGoogle Scholar
  4. Bai, S. & W.-S. Lung, 2005. Modeling sediment impact on the transport of fecal bacteria. Water Research 39: 5232–5240.CrossRefPubMedGoogle Scholar
  5. Bartram, J. & R. Ballance, 1996. Water quality monitoring: a practical guide to the design and implementation of freshwater quality studies and monitoring programmes. CRC Press, Boca Raton.Google Scholar
  6. Battin, T. J., L. A. Kaplan, J. Denis Newbold & C. M. E. Hansen, 2003. Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426: 439–442.CrossRefPubMedGoogle Scholar
  7. Bertrand-Krajewski, J. L., 2004. TSS concentration in sewers estimated from turbidity measurements by means of linear regression accounting for uncertainties in both variables. Water Science and Technology 50: 81–88.PubMedGoogle Scholar
  8. Bilotta, G. S. & R. E. Brazier, 2008. Understanding the influence of suspended solids on water quality and aquatic biota. Water Research 42: 2849–2861.CrossRefPubMedGoogle Scholar
  9. Bloesch, J., 1994. A review of methods used to measure sediment resuspension. Hydrobiologia 284: 13–18.CrossRefGoogle Scholar
  10. Bloesch, J., 1995. Mechanisms, measurement and importance of sediment resuspension in lakes. Marine and Freshwater Research 46: 295–304.Google Scholar
  11. Bloesch, J. & U. Uehlinger, 1986. Horizontal sedimentation differences in a eutrophic Swiss lake. Limnology and Oceanography 31: 1094–1109.CrossRefGoogle Scholar
  12. Boi, P., S. Amalfitano, A. Manti, F. Semprucci, D. Sisti, M. B. Rocchi, M. Balsamo & S. Papa, 2016. Strategies for water quality assessment: a multiparametric analysis of microbiological changes in river waters. River Research and Applications 32: 490–500.CrossRefGoogle Scholar
  13. Briée, C., D. Moreira & P. López-García, 2007. Archaeal and bacterial community composition of sediment and plankton from a suboxic freshwater pond. Research in Microbiology 158: 213–227.CrossRefPubMedGoogle Scholar
  14. Butturini, A., A. Guarch, A. M. Romaní, A. Freixa, S. Amalfitano, S. Fazi & E. Ejarque, 2016. Hydrological conditions control in situ DOM retention and release along a Mediterranean river. Water Research 99: 33–45.CrossRefPubMedGoogle Scholar
  15. Callieri, C., A. Lami & R. Bertoni, 2011. Microcolony formation by single-cell Synechococcus strains as a fast response to UV radiation. Applied and Environmental Microbiology 77: 7533–7540.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Callieri, C., S. Amalfitano, G. Corno, & R. Bertoni, 2016a. Grazing-induced Synechococcus microcolony formation: experimental insights from two freshwater phylotypes. FEMS Microbiology Ecology 92: fiw154.Google Scholar
  17. Callieri, C., S. Hernández-Avilés, M. M. Salcher, D. Fontaneto & R. Bertoni, 2016b. Distribution patterns and environmental correlates of Thaumarchaeota abundance in six deep subalpine lakes. Aquatic Sciences 78: 215–225.CrossRefGoogle Scholar
  18. Casentini, B., F. T. Falcione, S. Amalfitano, S. Fazi & S. Rossetti, 2016. Arsenic removal by discontinuous ZVI two steps system for drinking water production at household scale. Water Research 106: 135–145.CrossRefPubMedGoogle Scholar
  19. Chapman, D. V., 1996. Water quality assessments: a guide to the use of biota, sediments, and water in environmental monitoring. E & Fn Spon, London.CrossRefGoogle Scholar
  20. Characklis, G. W., M. J. Dilts, O. D. Simmons, C. A. Likirdopulos, L. A. H. Krometis & M. D. Sobsey, 2005. Microbial partitioning to settleable particles in stormwater. Water Research 39: 1773–1782.CrossRefPubMedGoogle Scholar
  21. Coci, M., N. Odermatt, M. M. Salcher, J. Pernthaler & G. Corno, 2015. Ecology and distribution of Thaumarchaea in the deep hypolimnion of Lake Maggiore. Archaea 2015: 1–12.CrossRefGoogle Scholar
  22. Cole, J. J., S. R. Carpenter, M. L. Pace, M. C. de Bogert, J. L. Kitchell & J. R. Hodgson, 2006. Differential support of lake food webs by three types of terrestrial organic carbon. Ecology Letters 9: 558–568.CrossRefPubMedGoogle Scholar
  23. Colwell, R. R., P. R. Brayton, D. J. Grimes, D. B. Roszak, S. A. Huq & L. M. Palmer, 1985. Viable but non-culturable Vibrio cholerae and related pathogens in the environment: implications for release of genetically engineered microorganisms. Nature Biotechnology 3: 817–820.CrossRefGoogle Scholar
  24. Cornett, R. J., L. A. Chant, B. A. Risto & E. Bonvin, 1994. Identifying resuspended particles using isotope ratios. Hydrobiologia 284: 69–77.CrossRefGoogle Scholar
  25. Corno, G., M. Coci, M. Giardina, S. Plechuk, F. Campanile & S. Stefani, 2014. Antibiotics promote aggregation within aquatic bacterial communities. Frontiers in Microbiology. doi: 10.3389/fmicb.2014.00297.PubMedPubMedCentralGoogle Scholar
  26. Costerton, J. W., 1999. Bacterial bofilms: a common cause of persistent infections. Science 284: 1318–1322.CrossRefPubMedGoogle Scholar
  27. Coumou, D. & S. Rahmstorf, 2012. A decade of weather extremes. Nature Climate Change Nature Research 2: 491–496.Google Scholar
  28. Crump, B. C., E. V. Armbrust & J. A. Baross, 1999. Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia river, its estuary, and the adjacent coastal ocean. Applied and Environmental Microbiology 65: 3192–3204.PubMedPubMedCentralGoogle Scholar
  29. Di Cesare, A., E. M. Eckert & G. Corno, 2016a. Co-selection of antibiotic and heavy metal resistance in freshwater bacteria. Journal of Limnology 75: 59–66.CrossRefGoogle Scholar
  30. Di Cesare, A., E. M. Eckert, S. D’Urso, R. Bertoni, D. C. Gillan, R. Wattiez & G. Corno, 2016b. Co-occurrence of integrase 1, antibiotic and heavy metal resistance genes in municipal wastewater treatment plants. Water Research 94: 208–214.CrossRefPubMedGoogle Scholar
  31. Dillon, P. J., R. D. Evans & L. A. Molot, 1990. Retention and resuspension of phosphorus, nitrogen, and iron in a central Ontario lake. Canadian Journal of Fisheries and Aquatic Sciences 47: 1269–1274.CrossRefGoogle Scholar
  32. Drummond, J. D., R. J. Davies-Colley, R. Stott, J. P. Sukias, J. W. Nagels, A. Sharp & A. I. Packman, 2015. Microbial transport, retention, and inactivation in streams: a combined experimental and stochastic modeling approach. Environmental Science & Technology 49: 7825–7833.CrossRefGoogle Scholar
  33. Du Preez, M., M. R. der Merwe, A. Cumbana & W. Le Roux, 2010. A survey of Vibrio cholerae O1 and O139 in estuarine waters and sediments of Beira, Mozambique. Water SA 36: 615–620.Google Scholar
  34. Eckert, W. & A. Nishri, 2014. The phosphorus cycle. In Zohary, T., A. Sukenik, T. Berman & A. Nishri (eds), Lake Kinneret: Ecology and Management, Chapter 20. Springer, The Netherlands: 347–363.Google Scholar
  35. Eckert, W., J. Didenko, E. Uri & D. Eldar, 2003. Spatial and temporal variability of particulate phosphorus fractions in seston and sediments of Lake Kinneret under changing loading scenario. Hydrobiologia 494: 223–229.CrossRefGoogle Scholar
  36. Edge, T. A., I. U. H. Khan, R. Bouchard, J. Guo, S. Hill, A. Locas, L. Moore, N. Neumann, E. Nowak, P. Payment, R. Yang, R. Yerubandi & S. Watson, 2013. Occurrence of waterborne pathogens and Escherichia coli at offshore drinking water intakes in lake Ontario. Applied and Environmental Microbiology 79: 5799–5813.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ejarque, E., A. Freixa, E. Vazquez, A. Guarch, S. Amalfitano, S. Fazi, A. M. Romaní & A. Butturini, 2017. Quality and reactivity of dissolved organic matter in a Mediterranean river across hydrological and spatial gradients. Science of The Total Environment 599–600: 1802–1812.CrossRefPubMedGoogle Scholar
  38. European Communities Environmental Objectives, 2009. Surface waters regulations. 272Google Scholar
  39. European Union, 1998. 98/83/EC on the quality of water intented for human consumption. Adopted by the Council, on 3: 32–54.Google Scholar
  40. Evans, R. D., 1994. Empirical evidence of the importance of sediment resuspension in lakes. Hydrobiologia 284: 5–12.CrossRefGoogle Scholar
  41. Fitzgerald, S. A., J. V. Klump, P. W. Swarzenski, R. A. Mackenzie & K. D. Richards, 2001. Beryllium-7 as a tracer of short-term sediment deposition and resuspension in the Fox River, Wisconsin. Environmental Science & Technology 35: 300–305.CrossRefGoogle Scholar
  42. Fox, G. A., A. Sheshukov, R. Cruse, R. L. Kolar, L. Guertault, K. R. Gesch & R. C. Dutnell, 2016. Reservoir sedimentation and upstream sediment sources: perspectives and future research needs on streambank and gully erosion. Environmental Management 57: 945–955.CrossRefPubMedGoogle Scholar
  43. Freese, E., J. Köster & J. Rullkötter, 2008. Origin and composition of organic matter in tidal flat sediments from the German Wadden Sea. Organic Geochemistry 39: 820–829.CrossRefGoogle Scholar
  44. Freixa, A., E. Ejarque, S. Crognale, S. Amalfitano, S. Fazi, A. Butturini & A. M. Romaní, 2016. Sediment microbial communities rely on different dissolved organic matter sources along a Mediterranean river continuum. Limnology and Oceanography 61: 1389–1405.CrossRefGoogle Scholar
  45. Fries, J. S., R. T. Noble & G. W. Characklis, 2006. Attachment of fecal indicator bacteria to particles in the Neuse River Estuary, N.C. Journal of Environmental Engineering American Society of Civil Engineers 132: 1338–1345.CrossRefGoogle Scholar
  46. Frindte, K., M. Allgaier, H. P. Grossart & W. Eckert, 2015. Microbial response to experimentally controlled redox transitions at the sediment water interface. PLoS ONE 10: 1–17.CrossRefGoogle Scholar
  47. Frindte, K., M. Allgaier, H. P. Grossart & W. Eckert, 2016. Redox stability regulates community structure of active microbes at the sediment-water interface. Environmental Microbiology Reports 8: 798–804.CrossRefGoogle Scholar
  48. García-Ruiz, J. M., J. I. López-Moreno, S. M. Vicente-Serrano, T. Lasanta–Martínez & S. Beguería, 2011. Mediterranean water resources in a global change scenario. Earth-Science Reviews 105: 121–139.CrossRefGoogle Scholar
  49. Gasith, A., 1975. Tripton sedimentation in Eutrophic Lakes-sample correction for the resuspended matter. Verhandlungen Internationale Vereinigung Limnologie 19: 116–122.Google Scholar
  50. Gasol, J. M., & X. A. G. Moran, 2015. Flow Cytometric Determination of Microbial Abundances and Its Use to Obtain Indices of Community Structure and Relative Activity. Hydrocarbon and Lipid Microbiology Protocols – Springer Protocols Handbooks 1–29.Google Scholar
  51. Gerbersdorf, S. U. & S. Wieprecht, 2015. Biostabilization of cohesive sediments: revisiting the role of abiotic conditions, physiology and diversity of microbes, polymeric secretion, and biofilm architecture. Geobiology 13: 68–97.CrossRefPubMedGoogle Scholar
  52. Gerbersdorf, S. U., B. Westrich & D. M. Paterson, 2009. Microbial extracellular polymeric substances (EPS) in fresh water sediments. Microbial Ecology 58: 334–349.CrossRefPubMedGoogle Scholar
  53. Gordon, A. K. & C. G. Palmer, 2015. Defining an exposure-response relationship for suspended kaolin clay particulates and aquatic organisms: work toward defining a water quality guideline for suspended solids. Environmental Toxicology and Chemistry 34: 907–912.CrossRefPubMedGoogle Scholar
  54. Grabowski, R. C., I. G. Droppo & G. Wharton, 2011. Erodibility of cohesive sediment: the importance of sediment properties. Earth-Science Reviews 105: 101–120.CrossRefGoogle Scholar
  55. Grathwohl, P., H. Rügner, T. Wöhling, K. Osenbrück, M. Schwientek, S. Gayler, U. Wollschläger, B. Selle, M. Pause, J.-O. Delfs, M. Grzeschik, U. Weller, M. Ivanov, O. A. Cirpka, U. Maier, B. Kuch, W. Nowak, V. Wulfmeyer, K. Warrach-Sagi, T. Streck, S. Attinger, L. Bilke, P. Dietrich, J. H. Fleckenstein, T. Kalbacher, O. Kolditz, K. Rink, L. Samaniego, H.-J. Vogel, U. Werban & G. Teutsch, 2013. Catchments as reactors: a comprehensive approach for water fluxes and solute turnover. Environmental Earth Sciences 69: 317–333.CrossRefGoogle Scholar
  56. Grossart, H. P., 2010. Ecological consequences of bacterioplankton lifestyles: changes in concepts are needed. Environmental Microbiology Reports 2: 706–714.CrossRefPubMedGoogle Scholar
  57. Grossart, H.-P. & H. Ploug, 2000. Bacterial production and growth efficiencies: direct measurements on riverine aggregates. Limnology and Oceanography 45: 436–445.CrossRefGoogle Scholar
  58. Grossart, H.-P. & M. Simon, 1998. Bacterial colonization and microbial decomposition of limnetic organic aggregates (lake snow). Aquatic Microbial Ecology 15: 127–140.CrossRefGoogle Scholar
  59. Hakanson, L., 2004. Internal loading: a new solution to an old problem in aquatic sciences. Lakes & Reservoirs: Research & Management 9: 3–23.CrossRefGoogle Scholar
  60. Hall-Stoodley, L. & P. Stoodley, 2005. Biofilm formation and dispersal and the transmission of human pathogens. Trends in Microbiology 13: 7–10.CrossRefPubMedGoogle Scholar
  61. Hamilton, D. P. & S. F. Mitchell, 1996. An empirical model for sediment resuspension in shallow lakes. Hydrobiologia 317: 209–220.CrossRefGoogle Scholar
  62. Hjulström, F., 1935. Studies of the morphological activity of rivers as illustrated by the River Fyris: Inaugural Dissertation. Almqvist & Wiksells.Google Scholar
  63. ISO5667-3, E., 2012. 5667-3: 2012. Water Quality–Sampling, Part A.Google Scholar
  64. Jacob, P., A. Henry, G. Meheut, N. Charni-Ben-Tabassi, V. Ingrand & K. Helmi, 2015. Health risk assessment related to waterborne pathogens from the river to the tap. International Journal of Environmental Research and Public Health 12: 2967–2983.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Jeng, H. C., A. J. England & Henry B. Bradford, 2005. Indicator organisms associated with stormwater suspended particles and estuarine sediment. Journal of Environmental Science and Health, Part A 40: 779–791.CrossRefGoogle Scholar
  66. Kemker, C., 2014. Turbidity, total suspended solids and water clarity. Fundamentals of Environmental Measurements. Fondriest Environmental, Inc 13.Google Scholar
  67. Kepkay, P. E., 1994. Particle aggregation and the biological reactivity of colloids. Marine Ecology Progress Series 109: 293–304.CrossRefGoogle Scholar
  68. Kiørboe, T., H.-P. Grossart, H. Ploug & K. Tang, 2002. Mechanisms and rates of bacterial colonization of sinking aggregates. Applied and Environmental Microbiology 68: 3996–4006.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Kleeberg, A., M. Hupfer, G. Gust, I. Salka, K. Pohlmann & H.-P. Grossart, 2013. Intermittent riverine resuspension: effects on phosphorus transformations and heterotrophic bacteria. Limnology and Oceanography 58: 635–652.CrossRefGoogle Scholar
  70. Koski-Vähälä, J., H. Hartikainen & T. Kairesalo, 2000. Resuspension in regulating sedimentation dynamics in Lake Vesijärvi. Archiv für Hydrobiologie 148: 357–381.CrossRefGoogle Scholar
  71. Liu, G., F. Q. Ling, E. J. van der Mark, X. D. Zhang, A. Knezev, J. Q. J. C. Verberk, W. G. J. van der Meer, G. J. Medema, W. T. Liu & J. C. van Dijk, 2016. Comparison of particle-associated bacteria from a drinking water treatment plant and distribution reservoirs with different water sources. Scientific Reports 6: 20367.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Lundkvist, M., M. Grue, P. L. Friend & M. R. Flindt, 2007. The relative contributions of physical and microbiological factors to cohesive sediment stability. Continental Shelf Research 27: 1143–1152.CrossRefGoogle Scholar
  73. Lyons, M. M., J. E. Ward, H. Gaff, R. E. Hicks, J. M. Drake & F. C. Dobbs, 2010. Theory of island biogeography on a microscopic scale: organic aggregates as islands for aquatic pathogens. Aquatic Microbial Ecology 60: 1–13.CrossRefGoogle Scholar
  74. MacGregor, B. J., D. P. Moser, B. J. Baker, E. W. Alm, M. Maurer, K. H. Nealson & D. A. Stahl, 2001. Seasonal and spatial variability in Lake Michigan sediment small-subunit rRNA concentrations. Applied and environmental microbiology 67: 3908–3922.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Mahler, B. J., J. C. Personn, G. F. Lods & C. Drogue, 2000. Transport of free and particulate-associated bacteria in karst. Journal of Hydrology 238: 179–193.CrossRefGoogle Scholar
  76. Malfatti, F. & F. Azam, 2009. Atomic force microscopy reveals microscale networks and possible symbioses among pelagic Marine Bacteria. Aquatic Microbial Ecology 58: 1–14.CrossRefGoogle Scholar
  77. Mamane, H., 2008. Impact of particles on UV disinfection of water and wastewater effluents: a review. Reviews in Chemical Engineering 24: 67.CrossRefGoogle Scholar
  78. Mestre, M., E. Borrull, M. M. Sala & J. M. Gasol, 2017. Patterns of bacterial diversity in the marine planktonic particulate matter continuum. The ISME Journal 11: 999–1010.CrossRefPubMedGoogle Scholar
  79. Niederdorfer, R., H. Peter & T. J. Battin, 2016. Attached biofilms and suspended aggregates are distinct microbial lifestyles emanating from differing hydraulics. Nature Microbiology 1: 161–178.CrossRefGoogle Scholar
  80. Official Journal of the European Union, 2009. Commission Directive 2009/90/EC laying down, pursuant to Directive 2000/60/EC of the European Parliament and of the Council, technical specifications for chemical analysis and monitoring of water status. 201: 36–38.Google Scholar
  81. Ortega-Retuerta, E., F. Joux, W. H. Jeffrey & J.-F. Ghiglione, 2013. Spatial variability of particle-attached and free-living bacterial diversity in surface waters from the Mackenzie River to the Beaufort Sea (Canadian Arctic). Biogeosciences 10: 2747–2759.CrossRefGoogle Scholar
  82. Quinteiro, P., A. C. Dias, A. Araújo, J. L. T. Pestana, B. G. Ridoutt & L. Arroja, 2015. Suspended solids in freshwater systems: characterisation model describing potential impacts on aquatic biota. International Journal of Life Cycle Assessment 20: 1232–1242.CrossRefGoogle Scholar
  83. Ransom, B., R. H. Bennett, R. Baerwald, M. H. Hulbert & P. J. Burkett, 1999. In situ conditions and interactions between microbes and minerals in fine-grained marine sediments: a TEM microfabric perspective. American Mineralogist 84: 183–192.CrossRefGoogle Scholar
  84. Reardon, K. E., P. A. Moreno-Casas, F. A. Bombardelli & S. G. Schladow, 2016. Seasonal nearshore sediment resuspension and water clarity at Lake Tahoe. Lake and Reservoir Management 32: 132–145.CrossRefGoogle Scholar
  85. Rieck, A., D. P. R. Herlemann, K. Jürgens & H.-P. Grossart, 2015. Particle-associated differ from free-living bacteria in surface waters of the Baltic Sea. Frontiers in Microbiology 6: 1297.CrossRefPubMedPubMedCentralGoogle Scholar
  86. Riemann, L. & A. Winding, 2001. Community dynamics of free-living and particle-associated bacterial assemblages during a freshwater phytoplankton bloom. Microbial Ecology 42: 274–285.CrossRefPubMedGoogle Scholar
  87. Rink, B., T. Martens, D. Fischer, A. Lemke, H.-P. Grossart, M. Simon & T. Brinkhoff, 2008. Short-term dynamics of bacterial communities in a tidally affected coastal ecosystem. FEMS Microbiology Ecology 66: 306–319.CrossRefPubMedGoogle Scholar
  88. Ritchie, J. C. & J. R. McHenry, 1990. Application of radioactive fallout cesium-137 for measuring soil erosion and sediment accumulation rates and patterns: a review. Journal of Environmental Quality 19: 215–233.CrossRefGoogle Scholar
  89. Romani, A. M., S. Amalfitano, J. Artigas, S. Fazi, S. Sabater, X. Timoner, I. Ylla & A. Zoppini, 2013. Microbial biofilm structure and organic matter use in mediterranean streams. Hydrobiologia 719: 43–58.CrossRefGoogle Scholar
  90. Rosa, F., 1985. Sedimentation and sediment resuspension in Lake Ontario. Journal of Great Lakes Research 11: 13–25.CrossRefGoogle Scholar
  91. Sajeesh, P. & A. K. Sen, 2014. Particle separation and sorting in microfluidic devices: a review. Microfluidics and Nanofluidics 17: 1–52.CrossRefGoogle Scholar
  92. Sass, H., H. Cypionka & H.-D. Babenzien, 1997. Vertical distribution of sulfate-reducing bacteria at the oxic-anoxic interface in sediments of the oligotrophic Lake Stechlin. FEMS Microbiology Ecology 22: 245–255.CrossRefGoogle Scholar
  93. Schwarz, J. I. K., W. Eckert & R. Conrad, 2007a. Community structure of Archaea and Bacteria in a profundal lake sediment Lake Kinneret (Israel). Systematic and Applied Microbiology 30: 239–254.CrossRefPubMedGoogle Scholar
  94. Schwarz, J. I. K., T. Lueders, W. Eckert & R. Conrad, 2007b. Identification of acetate-utilizing Bacteria and Archaea in methanogenic profundal sediments of Lake Kinneret (Israel) by stable isotope probing of rRNA. Environmental Microbiology 9: 223–237.CrossRefPubMedGoogle Scholar
  95. Simon, M., H. P. Grossart, B. Schweitzer & H. Ploug, 2002. Microbial ecology of organic aggregates in aquatic ecosystems. Aquatic Microbial Ecology 28: 175–211.CrossRefGoogle Scholar
  96. Singh, G., P. Vajpayee, S. Ram & R. Shanker, 2010. Environmental reservoirs for enterotoxigenic Escherichia coli in south Asian Gangetic riverine system. Environmental Science & Technology 44: 6475–6480.CrossRefGoogle Scholar
  97. Sobolev, D., K. Moore & A. L. Morris, 2009. Nutrients and light limitation of phytoplankton biomass in a turbid southeastern reservoir: implications for water quality. Southeastern Naturalist 8: 255–266.CrossRefGoogle Scholar
  98. Staats, N., L. J. Stal & L. R. Mur, 2000. Exopolysaccharide production by the epipelic diatom Cylindrotheca closterium: effects of nutrient conditions. Journal of Experimental Marine Biology and Ecology 249: 13–27.CrossRefPubMedGoogle Scholar
  99. Tang, K. W., C. Dziallas & H. P. Grossart, 2011. Zooplankton and aggregates as refuge for aquatic bacteria: protection from UV, heat and ozone stresses used for water treatment. Environmental Microbiology 13: 378–390.CrossRefPubMedGoogle Scholar
  100. Vercruysse, K., R. C. Grabowski & R. J. Rickson, 2017. Suspended sediment transport dynamics in rivers: multi-scale drivers of temporal variation. Earth-Science Reviews 166: 38–52.CrossRefGoogle Scholar
  101. Walters, E., K. Schwarzwälder, P. Rutschmann, E. Müller & H. Horn, 2014. Influence of resuspension on the fate of fecal indicator bacteria in large-scale flumes mimicking an oligotrophic river. Water Research 48: 466–477.CrossRefPubMedGoogle Scholar
  102. Weyhenmeyer, G. A., 1996. The influence of stratification on the amount and distribution of different settling particles in Lake Erken. Canadian Journal of Fisheries and Aquatic Sciences 53: 1254–1262.CrossRefGoogle Scholar
  103. Wood, M. S., 2014. Estimating suspended sediment in rivers using acoustic Doppler meters. US Geological Survey Fact Sheet 3038Google Scholar
  104. Wotton, R. S., 2007. Do benthic biologists pay enough attention to aggregates formed in the water column of streams and rivers? Journal of the North American Benthological Society 26: 1–11.CrossRefGoogle Scholar
  105. Yang, W., M. Chen, X. Zhang, Z. Guo, G. Li, Q. Ma, J. Yang & Y. Huang, 2013. Thorium isotopes (228Th, 230Th, 232Th) and applications in reconstructing the Yangtze and Yellow River floods. International Journal of Sediment Research 28: 588–595.CrossRefGoogle Scholar
  106. Zhang, Y., W. Xiao & N. Jiao, 2016. Linking biochemical properties of particles to particle-attached and free-living bacterial community structure along the particle density gradient from freshwater to open ocean. Journal of Geophysical Research G: Biogeosciences 121: 2261–2274.Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Water Research Institute (CNR-IRSA)MonterotondoItaly
  2. 2.Microbial Ecology GroupInstitute of Ecosystem Study (CNR-ISE)VerbaniaItaly
  3. 3.The Yigal Allon Kinneret Limnological Laboratory (KLL)Israel Oceanographic and Limnological ResearchMigdalIsrael
  4. 4.Department of Experimental LimnologyLeibniz Institute of Freshwater Ecology and Inland FisheriesBerlinGermany
  5. 5.Institute for Biochemistry and BiologyPotsdam UniversityPotsdamGermany

Personalised recommendations