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Recovery dynamics of prokaryotes and extracellular enzymes during sediment rewetting after desiccation

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Abstract

Intermittent flow of headwaters occurs with increasing frequency in temperate regions over last decades. Here, we assessed the effects of rewetting process on benthic prokaryotic communities from the Breitenbach (Hesse, Germany) for 10 days following experimental drought of different duration and intensity, by measuring the abundance of selected prokaryotic groups and potential extracellular enzyme activities (EEA). Desiccation time and intensity affected the recovery of the microbial community structure and the utilization of organic substrates in sediments, but recovery differed among prokaryotic groups and enzymes. Prokaryotes grew moderately to levels above the initial wet state, whereas Alphaproteobacteria were promoted. The EEA increased rapidly with overshoots within the first days of rewetting indicating high activation after desiccation. The ratios between the EEA changed with the duration of desiccation indicating changes of macromolecular organic matter utilization. The prokaryotic community and its functions were still distinctly different from the initial stream situation, and thus no resilience could be considered after short time (10 days) of recovery from desiccation. We propose that desiccation effects might be enhanced, if desiccation events occur under the effect of changing climate more often, more regularly, and/or for longer time spans.

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References

  • Allison, S. D. & J. B. H. Martiny, 2008. Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences of the United States of America 105: 11512–11519.

    Article  PubMed  PubMed Central  Google Scholar 

  • Amalfitano, S., S. Fazi, A. Zoppini, A. B. Caracciolo, P. Grenni & A. Puddu, 2008. Responses of benthic bacteria to experimental drying in sediments from Mediterranean temporary rivers. Microbial Ecology 55: 270–279.

    Article  PubMed  CAS  Google Scholar 

  • Barnard, R. L., C. A. Osborne & M. K. Firestone, 2013. Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. Isme Journal 7(11): 2229–2241.

    Article  PubMed  CAS  Google Scholar 

  • Barthes, A., L. Ten-Hage, A. Lamy, J. L. Rols & J. Leflaive, 2015. Resilience of aggregated microbial communities subjected to drought—small-scale studies. Microbial Ecology. https://doi.org/10.1007/s00248-014-0532-0.

    Article  PubMed  Google Scholar 

  • Billi, D. & M. Potts, 2002. Life and death of dried prokaryotes. Research in Microbiology 153(1): 7–12.

    Article  PubMed  CAS  Google Scholar 

  • Buesing, N. & M. O. Gessner, 2002. Comparison of detachment procedures for direct counts of bacteria associated with sediment particles, plant litter and epiphytic biofilms. Aquatic Microbial Ecology 27(1): 29–36.

    Article  Google Scholar 

  • Buesing, N. & J. Marxsen, 2005. Theoretical and empirical conversion factors for determining bacterial production in freshwater sediments via leucine incorporation. Limnology and Oceanography-Methods 3: 221.

    Google Scholar 

  • Butturini, A., A. Guarch, A. M. Romani, 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.

    Article  PubMed  CAS  Google Scholar 

  • Chrost, R. J., 1992. Significance of bacterial ectoenzymes in aquatic environments. Hydrobiologia 243: 61–70.

    Article  Google Scholar 

  • Donot, F., A. Fontana, J. C. Baccou & S. Schorr-Galindo, 2012. Microbial exopolysaccharides: main examples of synthesis, excretion, genetics and extraction. Carbohydrate Polymers 87(2): 951–962.

    Article  CAS  Google Scholar 

  • Fazi, S., S. Amalfitano, H. Pizzetti & J. Pernthaler, 2007. Efficiency of fluorescence in situ hybridization for bacterial cell identification in temporary river sediments with contrasting water content. Systematic and Applied Microbiology 30(6): 463–470.

    Article  PubMed  Google Scholar 

  • Fazi, S., S. Amalfitano, C. Piccini, A. Zoppini, A. Puddu & J. Pernthaler, 2008. Colonization of overlaying water by bacteria from dry river sediments. Environmental Microbiology 10(10): 2760–2772.

    Article  PubMed  CAS  Google Scholar 

  • Fiebig, D. M. & J. Marxsen, 1992. Immobilization and mineralization of dissolved free amino-acids by stream-bed biofilms. Freshwater Biology 28(1): 129–140.

    Article  CAS  Google Scholar 

  • Fierer, N., J. P. Schimel & P. A. Holden, 2003. Influence of drying-rewetting frequency on soil bacterial community structure. Microbial Ecology 45(1): 63–71.

    Article  PubMed  CAS  Google Scholar 

  • Fredrickson, J. K., S.-M. W. Li, E. K. Gaidamakova, V. Y. Matrosova, M. Zhai, H. M. Sulloway, J. C. Scholten, M. G. Brown, D. L. Balkwill & M. J. Daly, 2008. Protein oxidation: key to bacterial desiccation resistance? Isme Journal 2(4): 393–403.

    Article  PubMed  CAS  Google Scholar 

  • Fritsche, W., 1998. Umwelt-Mikrobiologie Grundlagen und Anwendung, Vol. 1. Gustav Fischer Verlag, Jena.

    Google Scholar 

  • Fromin, N., G. Pinay, B. Montuelle, D. Landais, J. M. Ourcival, R. Joffre & R. Lensi, 2010. Impact of seasonal sediment desiccation and rewetting on microbial processes involved in greenhouse gas emissions. Ecohydrology 3(3): 339–348.

    Article  CAS  Google Scholar 

  • Holling, C. S., 1973. Resilience and stability of ecological systems. Annual Review of Ecology and Systematics 4: 1–24.

    Article  Google Scholar 

  • Holling, C. S., 1996. Engineering resilience versus ecological resilience. In Schulze, P. (ed), Engineering within ecological constraints. National Academy, Washington, DC: 31–44.

    Google Scholar 

  • Hoppe, H.-G., 1983. Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Marine Ecology Progress Series 11: 299–308.

    Article  CAS  Google Scholar 

  • Hoshino, T., L. S. Yilmaz, D. R. Noguera & M. Wagner, 2008. Quantification of target molecules needed to detect microorganisms by fluorescence in situ hybridization (FISH) and catalyzed reporter deposition-FISH. Applied and Environmental Microbiology 74(16): 5068–5077.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kirchman, D. L., A. I. Dittel, S. E. G. Findlay & D. Fischer, 2004. Changes in bacterial activity and community structure in response to dissolved organic matter in the Hudson River, New York. Aquatic Microbial Ecology 35(3): 243–257.

    Article  Google Scholar 

  • Marxsen, J. & K. P. Witzel, 1990. Measurement of exoenzymatic activity in streambed sediments using methylumbelliferyl-substrates. Archiv für Hydrobiologie 34: 21–28.

    Google Scholar 

  • Marxsen, J. & K. P. Witzel, 1991. Significance of extracellular enzymes of organic matter degradation and nutrient regeneration in small streams. In Chrost, R. J. (ed), Microbial Enzymes in Aquatic Environments. Springer-Verlag, New York: 270–285.

    Chapter  Google Scholar 

  • Marxsen, J. & D. M. Fiebig, 1993. Use of perfused cores for evaluating extracellular enzyme-activity in stream-bed sediments. Fems Microbiology Ecology 13(1): 1–11.

    Article  CAS  Google Scholar 

  • Marxsen, J. & H. H. Schmidt, 1993. Extracellular phosphatase-activity in sediments of the Breitenbach, a Central-European mountain stream. Hydrobiologia 253(1–3): 207–216.

    Article  CAS  Google Scholar 

  • Marxsen, J., A. Zoppini & S. Wilczek, 2010. Microbial communities in streambed sediments recovering from desiccation. Fems Microbiology Ecology 71(3): 374–386.

    Article  PubMed  CAS  Google Scholar 

  • Marxsen, J., 2011. Bacteria and fungi. In Wagner, R., J. Marxsen, P. Zwick & E. J. Cox (eds), Central European stream ecosystems. The long term study of the Breitenbach. Wiley-VCH, Weinheim: 131–194.

    Google Scholar 

  • Marxsen, J., R. Wagner & H.-H. Schmidt, 2011. The Breitenbach and its catchment. In Wagner, R., J. Marxsen, P. Zwick & E. J. Cox (eds), Central European stream ecosystems the long term study of the Breitenbach. Wiley-VCH, Weinheim: 694.

    Google Scholar 

  • McKew, B. A., J. D. Taylor, T. J. McGenity & G. J. C. Underwood, 2011. Resistance and resilience of benthic biofilm communities from a temperate saltmarsh to desiccation and rewetting. Isme Journal 5(1): 30–41.

    Article  PubMed  Google Scholar 

  • Misic, C., P. Povero & M. Fabiano, 2002. Ectoenzymatic ratios in relation to particulate organic matter distribution (Ross Sea, Antarctica). Microbial Ecology 44(3): 224–234.

    Article  PubMed  CAS  Google Scholar 

  • Perez-Mateos, M., M. D. Busto & J. C. Rad, 1991. Stability and properties of alkaline phosphate immobilized by a rendzina soil. Journal of the Science of Food and Agriculture 55(2): 229–240.

    Article  CAS  Google Scholar 

  • Pernthaler, A., J. Pernthaler & R. Amann, 2004. Sensitive multi-color fluorescence in situ hybridisation for the identification of environmental microorganisms. Molecular Microbial Ecology Manual, Second Edition 3(11): 711–726.

    Google Scholar 

  • Pohlon, E., J. Marxsen & K. Küsel, 2010. Pioneering bacterial and algal communities and potential extracellular enzyme activities of stream biofilms. Fems Microbiology Ecology 71(3): 364–373.

    Article  PubMed  CAS  Google Scholar 

  • Pohlon, E., A. O. Fandino & J. Marxsen, 2013a. Bacterial community composition and extracellular enzyme activity in temperate streambed sediment during drying and rewetting. Plos One 8(12): e83365.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pohlon, E., C. Maetzig & J. Marxsen, 2013b. Desiccation affects bacterial community structure and function in temperate stream sediments. Fundamental and Applied Limnology 182(2): 123–134.

    Article  CAS  Google Scholar 

  • Rier, S. T., K. A. Kuehn & S. N. Francoeur, 2007. Algal regulation of extracellular enzyme activity in stream microbial communities associated with inert substrata and detritus. Journal of the North American Benthological Society 26(3): 439–449.

    Article  Google Scholar 

  • Rier, S. T., K. S. Nawrocki & J. C. Whitley, 2011. Response of biofilm extracellular enzymes along a stream nutrient enrichment gradient in an agricultural region of north central Pennsylvania, USA. Hydrobiologia 669: 119–131.

    Article  CAS  Google Scholar 

  • Romani, A. M. & S. Sabater, 1997. Metabolism recovery of a stromatolitic biofilm after drought in a Mediterranean stream. Archiv für Hydrobiologie 140(2): 261–271.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Rulik, M. & R. Spacil, 2004. Extracellular enzyme activity within hyporheic sediments of a small lowland stream. Soil Biology & Biochemistry 36(10): 1653–1662.

    Article  CAS  Google Scholar 

  • Schimel, J., T. C. Balser & M. Wallenstein, 2007. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88(6): 1386–1394.

    Article  PubMed  Google Scholar 

  • Schlief, J. & M. Mutz, 2011. Leaf decay processes during and after a supra-seasonal hydrological drought in a temperate lowland stream. International Review of Hydrobiology 96(6): 633–655.

    Article  CAS  Google Scholar 

  • Sirova, D., J. Vrba & E. Rejmankova, 2006. Extracellular enzyme activities in benthic cyanobacterial mats: comparison between nutrient-enriched and control sites in marshes of northern Belize. Aquatic Microbial Ecology 44(1): 11–20.

    Article  Google Scholar 

  • Timoner, X., C. M. Borrego, V. Acuna & S. Sabater, 2014. The dynamics of biofilm bacterial communities is driven by flow wax and wane in a temporary stream. Limnology and Oceanography 59(6): 2057–2067.

    Article  Google Scholar 

  • Vadher, A. N., J. Millett & P. J. Wood, 2018. Direct observations of the effects of fine sediment deposition on the vertical movement of Gammarus pulex (Crustacea: Amphipoda) during substratum drying. Hydrobiologia 815: 73–82.

    Google Scholar 

  • Wagner, R., J. Marxsen, P. Zwick & E. J. Cox, 2011. Central European stream ecosystems. The long term study of the Breitenbach. Wiley-VCH, Weinheim.

    Book  Google Scholar 

  • Ylla, I., I. Sanpera-Calbet, I. Munoz, A. M. Romani & S. Sabater, 2011. Organic matter characteristics in a Mediterranean stream through amino acid composition: changes driven by intermittency. Aquatic Sciences 73(4): 523–535.

    Article  CAS  Google Scholar 

  • Zoppini, A., S. Amalfitano, S. Fazi & A. Puddu, 2010. Dynamics of a benthic microbial community in a riverine environment subject to hydrological fluctuations (Mulargia River, Italy). Hydrobiologia 657(1): 37–51.

    Article  CAS  Google Scholar 

  • Zoppini, A. & J. Marxsen, 2010. Importance of extracellular enzymes for biogeochemical processes in temporary river sediments during fluctuating dry-wet conditions. Soil Enzymology 22: 103–117.

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to Janine Groh for preparing the CARD-FISH samples and to Charlotte Mätzig for measuring the EEA. The work was supported by a grant from the Deutsche Forschungsgemeinschaft to E.P.

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Authors and Affiliations

  1. Institute of Animal Ecology, Justus Liebig University, Heinrich-Buff-Ring 26 (IFZ), 35392, Giessen, Germany

    Elisabeth Pohlon, Nora K. Rütz, Klemens Ekschmitt & Jürgen Marxsen

  2. Limnological River Station of the Max Planck Institute for Limnology, 36110, Schlitz, Germany

    Jürgen Marxsen

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  1. Elisabeth Pohlon
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  2. Nora K. Rütz
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  3. Klemens Ekschmitt
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  4. Jürgen Marxsen
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Correspondence to Elisabeth Pohlon.

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Pohlon, E., Rütz, N.K., Ekschmitt, K. et al. Recovery dynamics of prokaryotes and extracellular enzymes during sediment rewetting after desiccation. Hydrobiologia 820, 255–266 (2018). https://doi.org/10.1007/s10750-018-3662-4

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  • DOI: https://doi.org/10.1007/s10750-018-3662-4

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