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Influence of water temperature and water depth on macrophyte–bacterioplankton interaction in a groundwater-fed river

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Abstract

Biotic interactions shape the community structure and function of ecosystems and thus play an important role in ecosystem management and restoration. To investigate how water temperature (related to the season) and water depth (related to spatial patterns of river morphology) affect macrophyte–bacterioplankton interactions in a groundwater-fed river, we conducted the structural equation modeling on datasets grouped by hydrological conditions. In addition to direct effects on macrophyte growth and/or bacterioplankton development, water temperature and water depth could both regulate the role of different nutrients (inorganic and organic) on affecting these biological indicators. Deeper water depth intensified the positive relationship between macrophytes and bacterioplankton, while higher temperature switched the relationship from being positive to negative. Our study provides empirical evidences that abiotic variables, even with relatively low fluctuations, play a critical role in regulating the patterns and strengths of interaction between macrophytes and bacterioplankton.

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References

  • Ambasht RS (1991) Relationship of nutrients in water with biomass and nutrient accumulation of submerged macrophytes of a tropical wetland. New Phytol 117:493–500

    Google Scholar 

  • APHA (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, Baltimore, MD

    Google Scholar 

  • Baker A (2002) Spectrophotometric discrimination of river dissolved organic matter. Hydrol Process 16:3203–3213

    Google Scholar 

  • Barko JW, Hardin DG, Matthews MS (1982) Growth and morphology of submersed freshwater macrophytes in relation to light and temperature. Can J Bot 60:877–887.

  • Barko JW, Smart R M (1981) Comparative Influences of Light and Temperature on the Growth and Metabolism of Selected Submersed Freshwater Macrophytes. Ecol Monog 51:219–236

  • Barnes AD, Jochum M, Lefcheck JS, Eisenhauer N, Scherber C, O’Connor MI, de Ruiter P, Brose U (2018) Energy flux: the link between multitrophic biodiversity and ecosystem functioning. Trends Ecol Evol 33:186–197

    Google Scholar 

  • Barrón C, Apostolaki ET, Duarte CM (2012) Dissolved organic carbon release by marine macrophytes. Biogeosci Discuss 9:1529–1555

    Google Scholar 

  • Berney M, Hammes F, Bosshard F, Weilenmann HU, Egli T (2007) Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight Kit in combination with flow cytometry. Appl Environ Microbiol 73:3283–3290

    CAS  Google Scholar 

  • Bullock JM, Aronson J, Newton AC, Pywell RF, Rey-Benays JM (2011) Restoration of ecosystem services and biodiversity: conflicts and opportunities. Trends Ecol Evol 26:541–549

    Google Scholar 

  • Bornette G, Puijalon S (2009) Macrophytes: ecology of aquatic plants. In: Hetherington AM (ed) Encyclopedia of life sciences (ELS). John Wiley & Sons, Ltd, Chichester

    Google Scholar 

  • Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Google Scholar 

  • Caissie D (2006) The thermal regime of rivers: a review. Freshw Biol 51:1389–1406

    Google Scholar 

  • Cantarel AA, Pommier T, Desclos-Theveniau M, Diquélou S, Dumont M, Grassein F, Kastl EM, Grigulis K, Laîné P, Lavorel S, Lemauviel-Lavenant S (2015) Using plant traits to explain plant–microbe relationships involved in nitrogen acquisition. Ecology 96:788–799

    Google Scholar 

  • Caron DA (1994) Inorganic nutrients, bacteria, and the microbial loop. Microb Ecol 28:295–298

    CAS  Google Scholar 

  • Carr GM, Duthie HC, Taylor WD (1997) Models of aquatic plant productivity: a review of the factors that influence growth. Aquat Bot 59:195–215

    Google Scholar 

  • Clark DB, Olivas PC, Oberbauer SF, Clark DA, Ryan MG (2008) First direct landscape-scale measurement of tropical rain forest leaf area index, a key driver of global primary productivity. Ecol Lett 11:163–172

    Google Scholar 

  • Chambers PA, Prepas EE, Hamilton HR, Bothwell ML (1991) Current velocity and its effect on aquatic macrophytes in flowing waters. Ecol Appl 1:249–257

    CAS  Google Scholar 

  • Compant S, Van Der Heijden MG, Sessitsch A (2010) Climate change effects on beneficial plant–microorganism interactions. FEMS Microbiol Ecol 73:197–214

    CAS  Google Scholar 

  • Cory RM, McKnight DM (2005) Fluorescence spectroscopy reveals ubiquitous presence of oxidized and reduced quinones in dissolved organic matter. Environ Sci Technol 39:8142–8149

    CAS  Google Scholar 

  • De Kluijver A, Ning J, Liu Z, Jeppesen E, Gulati RD, Middelburg JJ (2015) Macrophytes and periphyton carbon subsidies to bacterioplankton and zooplankton in a shallow eutrophic lake in tropical China. Limnol Oceanogr 60:375–385

    Google Scholar 

  • Del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541

    Google Scholar 

  • Dillon ME, Wang G, Huey RB (2010) Global metabolic impacts of recent climate warming. Nature 467:704–706

    CAS  Google Scholar 

  • Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694

    CAS  Google Scholar 

  • Donadi S, Westra J, Weerman EJ, van der Heide T, van der Zee EM, van de Koppel J, Olff H, Piersma T, van der Veer HW, Eriksson BK (2013) Non-trophic interactions control benthic producers on intertidal flats. Ecosystems 16:1325–1335

    CAS  Google Scholar 

  • Farjalla VF, Azevedo DA, Esteves FA, Bozelli RL, Roland F, Enrich-Prast A (2006) Influence of hydrological pulse on bacterial growth and DOC uptake in a clear-water Amazonian lake. Microb Ecol 52:334–344

    Google Scholar 

  • Finlay BJ, Maberly SC, Cooper JI (1997) Microbial diversity and ecosystem function. Oikos 80:209–213

    Google Scholar 

  • Findlay S, Pace ML, Lints D, Howe K (1992) Bacterial metabolism of organic carbon in the tidal freshwater Hudson Estuary. Mar Ecol Prog Ser 89:147–153

    CAS  Google Scholar 

  • Findlay S, Sinsabaugh RL (2003) Aquatic ecosystems: interactivity of dissolved organic matter, vol 15. Elsevier, New York, p 348

    Google Scholar 

  • Fourquez M, Obernosterer I, Davies DM, Trull TW, Blain S (2015) Microbial iron uptake in the naturally fertilized waters in the vicinity of the Kerguelen Islands: phytoplankton–bacteria interactions. Biogeosciences 12:1893–1906

    CAS  Google Scholar 

  • Goulder R (1984) Downstream increase in the abundance and heterotrophic activity of suspended bacteria in an intermittent calcareous headstream. Freshwater Bio 14:611–619

    Google Scholar 

  • Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge

    Google Scholar 

  • Hall EK, Neuhauser C, Cotner JB (2008) Toward a mechanistic understanding of how natural bacterial communities respond to changes in temperature in aquatic ecosystems. ISME J 2:471–481

    CAS  Google Scholar 

  • Hammill E, Kratina P, Vos M, Petchey OL, Anholt BR (2015) Food web persistence is enhanced by non-trophic interactions. Oecologia 178:549–556

    Google Scholar 

  • Harmon JP, Moran NA, Ives AR (2009) Species response to environmental change: impacts of food web interactions and evolution. Science 323:1347–1350

    CAS  Google Scholar 

  • He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16:695–706

  • Houston AC (1914) The effect of temperature on the vitality of B. coli and B. typhi in water. 10th Research Report, Metr. Water Board, London

  • Huguet A, Vacher L, Relexans S, Saubusse S, Froidefond JM, Parlanti E (2009) Properties of fluorescent dissolved organic matter in the Gironde Estuary. Org Geochem 40:706–719

    CAS  Google Scholar 

  • Huss AA, Wehr JD (2004) Strong indirect effects of a submersed aquatic macrophyte, Vallisneria americana, on bacterioplankton densities in a mesotrophic lake. Microb Ecol 47:305–315

    CAS  Google Scholar 

  • Iriondo JM, Albert MJ, Escudero A (2003) Structural equation modelling: an alternative for assessing causal relationships in threatened plant populations. Biodivers Conserv 113:367–377

    Google Scholar 

  • Jardillier L, Basset M, Domaizon I, Belan A, Amblard C, Richardot M (2004) Bottom-up and top-down control of bacterial community composition in the euphotic zone of a reservoir. Aquat Microb Ecol 35:259–273

    Google Scholar 

  • Jassey VE, Chiapusio G, Binet P, Buttler A, Laggoun-Défarge F, Delarue F, Bernard N, Mitchell EA, Toussaint ML, Francez AJ, Gilbert D (2013) Above- and belowground linkages in sphagnum peatland: climate warming affects plant-microbial interactions. Glob Chang Biol 19:811–823

    Google Scholar 

  • Juan M, Casas JJ, Elorrieta MA, Bonachela S, Gallego I, Fuentes-Rodríguez F, Fenoy E (2014) Can submerged macrophytes be effective for controlling waterborne phytopathogens in irrigation ponds? An experimental approach using microcosms. Hydrobiologia 732:183–196

    Google Scholar 

  • Kawasaki N, Benner R (2006) Bacterial release of dissolved organic matter during cell growth and decline: molecular origin and composition. Limnol Oceanogr 51:2170–2180

    CAS  Google Scholar 

  • Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143

    CAS  Google Scholar 

  • Kirchman DL (1994) The uptake of inorganic nutrients by heterotrophic bacteria. Microb Ecol 28:255–271

    CAS  Google Scholar 

  • Kiørboe T, Tang K, Grossart HP, Ploug H (2003) Dynamics of microbial communities on marine snow aggregates: colonization, growth, detachment, and grazing mortality of attached bacteria. Appl Environ Microbiol 69:3036–3047

    Google Scholar 

  • Kéfi S, Berlow EL, Wieters EA, Navarrete SA, Petchey OL, Wood SA, Boit A, Joppa LN, Lafferty KD, Williams RJ, Martinez ND (2012) More than a meal…integrating non-feeding interactions into food webs. Ecol Lett 15:291–300

    Google Scholar 

  • Kollmann J, Meyer ST, Bateman R, Conradi T, Gossner MM, de Souza Mendonça Jr M, Fernandes GW, Hermann JM, Koch C, Müller SC, Oki Y (2016) Integrating ecosystem functions into restoration ecology-recent advances and future directions. Restor Ecol 24:722-730

  • Lamers LP, Van Diggelen JM, Op Den Camp HJ, Visser EJ, Lucassen EC, Vile MA, Jetten MS, Smolders AJ, Roelofs JG (2012) Microbial transformations of nitrogen, sulfur, and iron dictate vegetation composition in wetlands: a review. Front Microbiol 3:156

    CAS  Google Scholar 

  • Lau YL, Liu D (1993) Effect of flow rate on biofilm accumulation in open channels. Water Res 27:355–360

    CAS  Google Scholar 

  • Levi PS, Starnawski P, Poulsen B, Baattrup-Pedersen A, Schramm A, Riis T (2017) Microbial community diversity and composition varies with habitat characteristics and biofilm function in macrophyte-rich streams. Oikos 126:398–409

    CAS  Google Scholar 

  • Lindström ES, Kamst-Van Agterveld MP, Zwart G (2005) Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl Environ Microbiol 71:8201–8206

    Google Scholar 

  • Logue JB, Stedmon CA, Kellerman AM, Nielsen NJ, Andersson AF, Laudon H, Lindström ES, Kritzberg ES (2016) Experimental insights into the importance of aquatic bacterial community composition to the degradation of dissolved organic matter. ISME J 10:533–545

    CAS  Google Scholar 

  • Maberly SC (1993) Morphological and photosynthetic characteristics of Potamogeton obtusifolius from different depths. J Aquat Plant Manag 31:34–39

    Google Scholar 

  • Marie D, Partensky F, Jacquet S, Vaulot D (1997) Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl Environ Microbiol 63:186–193

    CAS  Google Scholar 

  • McKnight DM, Boyer EW, Westerhoff PK, Doran PT, Kulbe T, Andersen DT (2001) Spectrofluorometric characterization of dissolved organic matter for indication of precursor organic material and aromaticity. Limnol Oceanogr 46:38–48

    CAS  Google Scholar 

  • Mukamolova GV, Kaprelyants AS, Kell DB, Young M (2003) Adoption of the transiently non-culturable state—a bacterial survival strategy? Adv Microb Physiol 47:66–131

    Google Scholar 

  • Oberski D (2014) lavaan.survey: an R package for complex survey analysis of structural equation models. J Stat Softw 57:1–27

    Google Scholar 

  • Panikov N (1994) Population dynamics of microorganisms with different life strategies. In: Bazin MJ, Lynch JM (eds) Environmental gene release: models, experiments and risk assessment. Springer Science & Business Media, Berlin

    Google Scholar 

  • Preston CD, Croft JM (1997) Aquatic plants in Britain and Ireland. Harley Books, London

    Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org/

    Google Scholar 

  • Ram ASP, Boucher D, Sime-Ngando T, Debroas D, Romagoux JC (2005) Phage bacteriolysis, protistan bacterivory potential, and bacterial production in a freshwater reservoir: coupling with temperature. Microb Ecol 50:64–72

    Google Scholar 

  • Reitsema RE, Meire P, Schoelynck J (2018) The future of freshwater macrophytes in a changing world: dissolved organic carbon quantity and quality and its interactions with macrophytes. Front Plant Sci 9:629

    Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    CAS  Google Scholar 

  • Rier ST, Stevenson RJ (2002) Effects of light, dissolved organic carbon, and inorganic nutrients on the relationship between algae and heterotrophic bacteria in stream periphyton. Hydrobiologia 489:179–184

    CAS  Google Scholar 

  • Rosseel Y (2012) Lavaan: an R package for structural equation modelling. J Stat Softw 48:1–36

    Google Scholar 

  • Roszak DB, Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol Re 51:365–379

    CAS  Google Scholar 

  • Rubin MA, Leff LG (2007) Nutrients and other abiotic factors affecting bacterial communities in an Ohio River (USA). Microb Ecol 54:374–383

    Google Scholar 

  • Schoelynck J, De Groote T, Bal K, Vandenbruwaene W, Meire P, Temmerman S (2012) Self-organised patchiness and scale-dependent biogeomorphic feedbacks in aquatic river vegetation. Ecography 35:760–768

    Google Scholar 

  • Schulz M, Kozerski HP, Pluntke T, Rinke K (2003) The influence of macrophytes on sedimentation and nutrient retention in the lower River Spree (Germany). Water Res 37:569–578

    CAS  Google Scholar 

  • Shiah FK, Ducklow HW (1994) Temperature regulation of heterotrophic bacterioplanktopn abundance, production, and specific growth rate in Chesapeake Bay. Limnol Oceanogr 39:1243–1258

    Google Scholar 

  • Stace C (2010) New flora of the British Isles. Cambridge University Press, Cambridge

    Google Scholar 

  • Stanley EH, Powers SM, Lottig NR, Buffam I, Crawford JT (2012) Contemporary changes in dissolved organic carbon (DOC) in human-dominated rivers: is there a role for DOC management? Freshw Biol 57:26–42

    Google Scholar 

  • Stepanauskas R, Farjalla VF, Tranvik LJ, Svensson JM, Esteves FA, Granéli W (2000) Bioavailability and sources of DOC and DON in macrophyte stands of a tropical coastal lake. Hydrobiologia 436:241–248

    CAS  Google Scholar 

  • Šolić M, Krstulović N, Vilibić I, Bojanić N, Kušpilić G, Šestanović S, Šantić D, Ordulj M (2009) Variability in the bottom-up and top-down controls of bacteria on trophic and temporal scales in the middle Adriatic Sea. Aquat Microb Ecol 58:15–29

    Google Scholar 

  • Švanys A, Paškauskas R, Hilt S (2014) Effects of the allelopathically active macrophyte Myriophyllum spicatum on a natural phytoplankton community: a mesocosm study. Hydrobiologia 737:57–66

    Google Scholar 

  • Thomas JD (1997) The role of dissolved organic matter, particularly free amino acids and humic substances, in freshwater ecosystems. Freshw Biol 38:1–36

    CAS  Google Scholar 

  • Tockner, Pusch M, Gessner J, Wolter C (2011) Domesticated ecosystems and novel communities: challenges for the management of large rivers. Ecohydrol Hydrobiol 11:167–174

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    Google Scholar 

  • Ushio M, Hsieh CH, Masuda R, Deyle ER, Ye H, Chang CW, Sugihara G, Kondoh M (2018) Fluctuating interaction network and time-varying stability of a natural fish community. Nature 554:360

    CAS  Google Scholar 

  • Vitvar T, Newman BD, Aggarwal P, Garner A (2007) Application of environmental isotopes for studying stream/aquifer interactions in the Danube basin. Water Sci Tech W Sup 7:25–30

    Google Scholar 

  • Warnecke F, Sommaruga R, Sekar R, Hofer JS, Pernthaler J (2005) Abundances, identity, and growth state of Actinobacteria in mountain lakes of different UV transparency. Appl Environ Microbiol 71:5551–5559

    CAS  Google Scholar 

  • Wootton JT, Emmerson M (2005) Measurement of interaction strength in nature. Annu Rev Ecol Evol Syst 36:419–444

    Google Scholar 

  • Wu Y, Wang F, Xiao X, Liu J, Wu C, Chen H, Kerr P, Shurin J (2017) Seasonal changes in phosphorus competition and allelopathy of a benthic microbial assembly facilitate prevention of cyanobacterial blooms. Environ Microbiol 19:2483–2494

    CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    CAS  Google Scholar 

  • Zeng J, Bian Y, Xing P, Wu QL (2012) Macrophyte species drive the variation of bacterioplankton community composition in a shallow freshwater lake. Appl Environ Microbiol 78:177–184

    CAS  Google Scholar 

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Acknowledgments

We are grateful to R. Debbaut and D. Van Pelt for their help in the field, and to B. Pitzl and G. Steniczka for the analyses of nutrients and DOC. This research was executed within the project FLASHMOB “Fluxes Affected by Stream Hydrophytes: Modelling of Biogeochemistry” (Research Foundation-Flanders (FWO): No. G0F3217N and Austrian Science Fund (FWF): No. I3216-N29 and supported by National Natural Science Foundation of China (NSFC): No. 51609238. J. Schoelynck is a postdoctoral fellow of FWO (No. 12H8616N).

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Authors and Affiliations

  1. Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Yanran Dai

  2. WasserCluster Lunz (WCL), Inter-university Research Institute, Lunz am See, Austria

    Yanran Dai, Thomas Hein & Stefan Preiner

  3. Institute of Hydrobiology and Aquatic Ecosystem Management, University of Natural Resource and Life Sciences, Vienna, Austria

    Thomas Hein & Stefan Preiner

  4. Department of Biology, Ecosystem Management Research Group, University of Antwerp, 9 Universiteitsplein 1C, B–2610, Wilrijk, Belgium

    Rosanne E. Reitsema & Jonas Schoelynck

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  1. Yanran Dai
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  2. Thomas Hein
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  4. Rosanne E. Reitsema
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  5. Jonas Schoelynck
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Correspondence to Yanran Dai.

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Dai, Y., Hein, T., Preiner, S. et al. Influence of water temperature and water depth on macrophyte–bacterioplankton interaction in a groundwater-fed river. Environ Sci Pollut Res 27, 13166–13179 (2020). https://doi.org/10.1007/s11356-020-07921-2

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