Skip to main content

Advertisement

Log in

Ecological assessment of groundwater ecosystems disturbed by recharge systems using organic matter quality, biofilm characteristics, and bacterial diversity

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Recharge of aquifers by urban stormwater may trigger significant ecological changes that can be detrimental to the biodiversity and functioning of groundwater ecosystems. Here, the effects of aquifer recharge (AR) on three levels of parameters were investigated: dissolved organic carbon (DOC) quantity and quality, global biofilm characteristics, and diversity changes of bacterial communities. As DOC enrichment by AR can be mitigated by vadose zone (VZ) thickness, three AR sites with thin VZ (< 3 m) and three sites with thick VZ (> 10 m) were selected. For each AR site, clay beads were incubated over a 10-day-long rainy period through wells in recharged and non-recharged groundwaters. Total proteins, dehydrogenase, and hydrolytic activities were monitored from clay beads to assess biofilm development. Bacterial richness on beads was estimated by 16S rRNA-based metabarcoding. AR was found to significantly increase DOC and biodegradable DOC (BDOC) concentrations, biofilm development, and bacterial richness especially in sites with thin VZ. VZ thickness was inversely related to microbial growth indicators and bacterial richness in groundwater, through a control of DOC availability. The proportion of Bacteroidetes 16S rRNA gene reads was higher in recharged groundwater than in non-recharged groundwater, suggesting that this phylum could be used as an indicator of DOC enrichment associated with AR. Quantitative PCR assays for Bacteroides DNA confirmed these trends and showed an enrichment of this bacterial group in DOC-rich aquifer waters. The positive linear relationships between BDOC concentrations and biofilm variables highlighted a strong C-limitation of groundwater impacting bacterial species sorting and activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alonso C, Warnecke F, Amann R, Pernthaler J (2007) High local and global diversity of Flavobacteria in marine plankton. Environ Microbiol 9:1253–1266

    Article  CAS  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Baker MA, Valett HM, Dahm CN (2000) Organic carbon supply and metabolism in a shallow groundwater ecosystem. Ecology 81:3133–3148

    Article  Google Scholar 

  • Battin TJ (1997) Assessment of fluorescein diacetate hydrolysis as a measure of total esterase activity in natural stream sediment biofilms. Sci Total Environ 198:51–60

    Article  CAS  Google Scholar 

  • Bengtsson G (1989) Growth and metabolic flexibility in groundwater bacteria. Microb Ecol 18:235–248

    Article  CAS  Google Scholar 

  • Bernardin-Souibgui C, Barraud S, Bourgeois E, Aubin JB, Becouze-Lareure C, Wiest L, Marjolet L, Colinon C, Lipeme Kouyi G, Cournoyer B, Blaha D (2018) Incidence of hydrological, chemical, and physical constraints on bacterial pathogens, Nocardia cells, and fecal indicator bacteria trapped in an urban stormwater detention basin in Chassieu, France. Environ Sci Pollut Res 25:24860–24881

    Article  CAS  Google Scholar 

  • Bernstein HC, Brislawn C, Renslow RS, Dana K, Morton B, Lindemann SR, Song H-S, Atci E, Beyenal H, Fredrickson JK, Jansson JK, Morand JJ (2017) Trade-offs between microbiome diversity and productivity in a stratified microbial mat. ISME J 11:405–414

    Article  Google Scholar 

  • Bienhold C, Boetius A, Ramette A (2012) The energy–diversity relationship of complex bacterial communities in Arctic deep-sea sediments. ISME J 6:724–732

    Article  CAS  Google Scholar 

  • Cardinale BJ, Hillebrand H, Harpole WS, Gross K, Ptacnik R (2009) Separating the influence of resource "availability" from resource "imbalance" on productivity-diversity relationships. Ecol Lett 12:475–487

    Article  Google Scholar 

  • Chapelle FH (2001) Groundwater microbiology and geochemistry. Wiley Press, New York

    Google Scholar 

  • Chapelle FH, Lovley DR (1990) rates of microbial metabolism in deep coastal plain aquifers. Appl Environ Microbiol 56:1865–1874

    Article  CAS  Google Scholar 

  • Cooney TJ, Simon KS (2009) Influence of dissolved organic matter and invertebrates on the function of microbial films in groundwater. Microb Ecol 58:599–610

    Article  Google Scholar 

  • Cottrell MT, Kirchman DL (2000) Community composition of marine bacterioplankton determined by 16S rRNA gene clone libraries and fluorescence in situ hybridization. Appl Environ Microbiol 66:5116–5122

    Article  CAS  Google Scholar 

  • Datry T, Malard F, Gibert J (2004) Dynamics of solutes and dissolved oxygen in shallow urban groundwater below a stormwater infiltration basin. Sci Total Environ 329:215–229

    Article  CAS  Google Scholar 

  • Datry T, Malard F, Gibert J (2005) Response of invertebrate assemblages to increased groundwater recharge rates in a phreatic aquifer. J North Am Benthol Soc 24:461–477

    Article  Google Scholar 

  • Datry T, Malard F, Gibert J (2006) Effect of artificial stormwater infiltration on urban groundwater ecosystems. In: Tellam JH, Rivett MO, Israfilov RG, Herringshaw LG (eds) Urban groundwater management and sustainability. Springer, Dordrecht, pp 331–345

    Chapter  Google Scholar 

  • Díez-Vives C, Gasol JM, Acinas SG (2014) Spatial and temporal variability among marine Bacteroidetes populations in the NW Mediterranean Sea. Syst Appl Microbiol 37:68–78

    Article  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  Google Scholar 

  • Evans KL, Warren PH, Gaston KJ (2005) Species–energy relationships at the macroecological scale: a review of the mechanisms. Biol Rev 80:1–25

    Article  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  Google Scholar 

  • Fontvieille DA, Outaguerouine A, Thevenot DR (1992) Fluorescein diacetate hydrolysis as a measure of microbial activity in aquatic systems: application to activated sludges. Environ Technol 13:531–540

    Article  CAS  Google Scholar 

  • Foulquier A, Malard F, Barraud S, Gibert J (2009) Thermal influence of urban groundwater recharge from stormwater infiltration basins. Hydrol Proced 23:1701–1713

    Article  Google Scholar 

  • Foulquier A, Malard F, Mermillod-Blondin F, Datry T, Simon L, Montuelle B, Gibert J (2010) Vertical change in dissolved organic carbon and oxygen at the water table region of an aquifer recharged with stormwater: biological uptake or mixing? Biogeochemistry 99:31–47

    Article  CAS  Google Scholar 

  • Foulquier A, Malard F, Mermillod-Blondin F, Montuelle B, Dolédec S, Volat B, Gibert J (2011) Surface water linkages regulate trophic interactions in a groundwater food web. Ecosystems 14:1339–1353

    Article  CAS  Google Scholar 

  • Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459:193–199

    Article  CAS  Google Scholar 

  • Gibert J, Danielopol DL, Stanford JA (1994) Groundwater ecology. Academic Press, San Diego

    Google Scholar 

  • Goldscheider N, Hunkeler D, Rossi P (2006) Review: microbial biocenoses in pristine aquifers and an assessment of investigative methods. Hydrogeol J 14:926–941

    Article  CAS  Google Scholar 

  • Gómez-Pereira PR, Fuchs BM, Alonso C, Oliver MJ, Van Beusekom JE, Amann R (2010) Distinct flavobacterial communities in contrasting water masses of the North Atlantic Ocean. ISME J 4:472–487

    Article  CAS  Google Scholar 

  • Griebler C, Lueders T (2009) Microbial biodiversity in groundwater ecosystems. Freshw Biol 54:649–677

    Article  Google Scholar 

  • Hershey OS, Kallmeyer J, Wallace A, Barton MD, Barton HA (2018) High microbial diversity despite extremely low biomass in a deep karst aquifer. Front Microbiol 9 https://www.frontiersin.org/articles/10.3389/fmicb.2018.02823/full

  • Houri-Davignon J-C, Etcheber HC (1989) Measurement of actual electron transport system (ETS) activity in marine sediments by incubation with INT. Environ Technol 10:91–100

    CAS  Google Scholar 

  • Hug LA, Thomas BC, Brown CT, Frischkorn KR, Williams KH, Tringe SG, Banfield JF (2015) Aquifer environment selects for microbial species cohorts in sediment and groundwater. ISME J 9:1846–1856

    Article  CAS  Google Scholar 

  • Hunt W, Traver R, Davis A, Emerson CH, Collins KA, Stagge JH (2010) Low impact development practices: designing to infiltrate in urban environments. In: Chang NB (Ed). Effects of urbanization on groundwater. American Society of Civil Engineers, 308–343

  • Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898

    Article  CAS  Google Scholar 

  • Kalbitz K, Solinger S, Park J-H, Michalzik B, Matzner E (2000) Controls on the dynamics of dissolved organic matter in soils: a review. Soil Sci 165:277–304

    Article  CAS  Google Scholar 

  • Kazumi J, Capone D (1994) Heterotrophic microbial activity in shallow aquifer sediments of Long Island, New York. Microb Ecol 28:19–37

    Article  CAS  Google Scholar 

  • Kolehmainen RE, Langwaldt JH, Puhakka JA (2007) Natural organic matter (NOM) removal and structural changes in the bacterial community during artificial groundwater recharge with humic lake water. Water Res 41:2715–2725

    Article  CAS  Google Scholar 

  • Landa M, Cottrell MT, Kirchman DL, Blain S, Obernosterer I (2013) Changes in bacterial diversity in response to dissolved organic matter supply in a continuous culture experiment. Aquat Microb Ecol 69:157–168

    Article  Google Scholar 

  • Layton A, McKay L, Williams D, Garrett V, Gentry R, Sayler G (2006) Development of Bacteroides 16S rRNA gene TaqMan-based real-time PCR assays for estimation of total, human, and bovine fecal pollution in water. Appl Environ Microbiol 72:4214–4224

    Article  CAS  Google Scholar 

  • Lever MA, Rogers KL, Lloyd KG, Overmann J, Schink B, Thauer RK, Hoehler TM, Jørgensen BB (2015) Life under extreme energy limitation: a synthesis of laboratory and field-based investigations. FEMS Microbiol Rev 39:688–728

    Article  CAS  Google Scholar 

  • Li D, Alidina M, Ouf M, Sharp JO, Saikaly P, Drewes JE (2013) Microbial community evolution during simulated managed aquifer recharge in response to different biodegradable dissolved organic carbon (BDOC) concentrations. Water Res 47:2421–2430

    Article  CAS  Google Scholar 

  • Marsalek J, Chocat B (2002) International report: Stormwater management. Water Sci Technol 46:1–17

    Article  CAS  Google Scholar 

  • Marschner B, Kalbitz K (2003) Controls of bioavailability and biodegradability of dissolved organic matter in soils. Geoderma 113:211–235

    Article  CAS  Google Scholar 

  • Marti R, Ribun S, Aubin J-B, Colinon C, Petit S, Marjolet L, Gourmelon M, Schmitt L, Breil P, Cottet M, Cournoyer B (2017) Human-driven microbiological contamination of benthic and hyporheic sediments of an intermittent peri-urban river assessed from MST and 16S rRNA genetic structure analyses. Front Microbiol 8:19

    Google Scholar 

  • McKnight DM, Bencaia KE, Zeiiweger GW, Aiken GR, Feder GL, Thorn KA (1992) Sorption of dissolved organic carbon by hydrous aluminum and iron oxides occurring at the confluence of deer creek with the Snake River, Summit County, Colorado. Environ Sci Technol 26:1388–1396

    Article  CAS  Google Scholar 

  • Mermillod-Blondin F, Foulquier A, Maazouzi C, Navel S, Negrutiu Y, Vienney A, Simon L, Marmonier P (2013) Ecological assessment of groundwater trophic status by using artificial substrates to monitor biofilm growth and activity. Ecol Indic 25:230–238

    Article  CAS  Google Scholar 

  • Mermillod-Blondin F, Simon L, Maazouzi C, Foulquier A, Delolme C, Marmonier P (2015) Dynamics of dissolved organic carbon (DOC) through stormwater basins designed for groundwater recharge in urban area: assessment of retention efficiency. Water Res 81:27–37

    Article  CAS  Google Scholar 

  • Mermillod-Blondin F, Voisin J, Marjolet L, Marmonier P, Cournoyer B (2019) Clay beads as artificial trapping matrices for monitoring bacterial distribution among urban stormwater infiltration systems and their connected aquifers. Env Monitor Assess 191:58

    Article  CAS  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O'Hara BV (2007) The vegan package. Community ecology package, R package version 1

  • Pabich WJ, Valiela I, Hemond HF (2001) Relationship between DOC concentration and vadose zone thickness and depth below water table in groundwater of Cape Cod, USA. Biogeochemistry 55:247–268

    Article  Google Scholar 

  • Park J-W, Crowley DE (2006) Dynamic changes in nahAc gene copy numbers during degradation of naphthalene in PAH-contaminated soils. Appl Microbiol Biotechnol 72:1322–1329

    Article  CAS  Google Scholar 

  • Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346–356

    Article  CAS  Google Scholar 

  • Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol O, Malits A, Marrasé C (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70:6753–6766

    Article  CAS  Google Scholar 

  • Prosser JI, Bohannan BJ, Curtis TP, Ellis RJ, Firestone MK, Freckleton RP, Green JL, Green LE, Killham K, Lennon JJ, Osborn AM, Solan M, van der Gast CJ, Young JPW (2007) The role of ecological theory in microbial ecology. Nat Rev Microbiol 5:384–392

    Article  CAS  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  CAS  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Saidy AR, Smernik RJ, Baldock JA, Kaiser K, Sanderman J (2013) The sorption of organic carbon onto differing clay minerals in the presence and absence of hydrous iron oxide. Geoderma 209–210:15–21

    Article  CAS  Google Scholar 

  • Schauer R, Bienhold C, Ramette A, Harder J (2010) Bacterial diversity and biogeography in deep-sea surface sediments of the South Atlantic Ocean. ISME J 4:159–170

    Article  CAS  Google Scholar 

  • Schloss PD, Westcott SL (2011) Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl Environ Microbiol 77:3219–3226

    Article  CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  Google Scholar 

  • Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310

    Article  CAS  Google Scholar 

  • Servais P, Billen G, Hascoët MC (1987) Determination of the biodegradable fraction of dissolved organic matter in waters. Water Res 21:445–450

    Article  CAS  Google Scholar 

  • Servais P, Anzil A, Ventresque C (1989) Simple method for determination of biodegradable dissolved organic carbon in water. Appl Environ Microbiol 55:2732–2734

    Article  CAS  Google Scholar 

  • Seurinck S, Defoirdt T, Verstraete W, Siciliano SD (2005) Detection and quantification of the human-specific HF183 Bacteroides 16S rRNA genetic marker with real-time PCR for assessment of human faecal pollution in freshwater. Environ Microbiol 7:249–259

    Article  CAS  Google Scholar 

  • Shen Y, Chapelle FH, Strom EW, Benner R (2015) Origins and bioavailability of dissolved organic matter in groundwater. Biogeochemistry 122:61–78

    Article  CAS  Google Scholar 

  • Smith VH (2007) Microbial diversity-productivity relationships in aquatic ecosystems. FEMS Microbiol Ecol 62:181–186

    Article  CAS  Google Scholar 

  • Srivastava DS, Lawton JH (1998) Why more productive sites have more species: an experimental test of theory using tree-hole communities. Am Nat 152:510–529

    Article  CAS  Google Scholar 

  • Tada Y, Taniguchi A, Nagao I, Miki T, Uematsu M, Tsuda A, Hamasaki K (2011) Differing growth responses of major phylogenetic groups of marine bacteria to natural phytoplankton blooms in the Western North Pacific Ocean. Appl Environ Microbiol 77:4055–4065

    Article  CAS  Google Scholar 

  • Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, Kassabgy M, Huang S, Mann AJ, Waldmann J, Weber M, Klindworth A, Otto A, Lange J,  Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann FD, Callies U, Gerdts G, Wichels A, Wiltshire KH, Glockner FO, Schweder T, Amann R (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608–611

    Article  CAS  Google Scholar 

  • Voisin J, Cournoyer B, Mermillod-Blondin F (2016) Assessment of artificial substrates for evaluating groundwater microbial quality. Ecol Indic 71:577–586

    Article  CAS  Google Scholar 

  • Voisin J, Cournoyer B, Vienney A, Mermillod-Blondin F (2018) Aquifer recharge with stormwater runoff in urban areas: influence of vadose zone thickness on nutrient and bacterial transfers from the surface of infiltration basins to groundwater. Sci Total Environ 637:1496–1507

    Article  CAS  Google Scholar 

  • Wang Q (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  Google Scholar 

  • Williamson WM, Close ME, Leonard MM, Webber JB, Lin S (2012) Groundwater biofilm dynamics grown in situ along a nutrient gradient. Ground Water 50:690–703

    Article  CAS  Google Scholar 

  • Wright DH (1983) Species–energy theory: an extension of species-area theory. Oikos 41:496–506

    Article  Google Scholar 

  • Zhang X, Zhao X, Zhang M (2012) Functional diversity changes of microbial communities along a soil aquifer for reclaimed water recharge. FEMS Microbiol Ecol 80:9–18

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Léa Dantony, Mathilde Pigneret, and Felix Vallier for their support and advice during field and laboratory work and Pierre Marmonier for editing an earlier draft of this manuscript. This work was performed within the framework of the EUR H2O’Lyon (ANR-17-EURE-0018) of Université de Lyon (UdL), within the program “Investissements d'Avenir” operated by the French National Research Agency (ANR).

Funding

The Auvergne-Rhône-Alpes region for Jérémy Voisin’s Ph.D provided grant. This work was supported by l’Agence Nationale de la Recherche [ANR-16-CE32–0006 FROG], Lyon Metropole and Agence de l’Eau Rhône-Méditerranée-Corse within the framework of the experimental observatory for urban hydrology (OTHU, http://www.graie.org/othu) and Rhône Basin LTER (ZABR), and the French national research program for environmental and occupational health of Anses under the terms of project “Iouqmer” EST 2016/1/120.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Florian Mermillod-Blondin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Diane Purchase

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(XLSX 10 kb)

ESM 2

(XLSX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Voisin, J., Cournoyer, B., Marjolet, L. et al. Ecological assessment of groundwater ecosystems disturbed by recharge systems using organic matter quality, biofilm characteristics, and bacterial diversity. Environ Sci Pollut Res 27, 3295–3308 (2020). https://doi.org/10.1007/s11356-019-06971-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-06971-5

Keywords

Navigation