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Biofilm microbial community structure in an urban lake utilizing reclaimed water

Abstract

Analyses of biofilm community structure may potentially be employed for aquatic ecosystem health assessment, however, to date, biofilm diversity within urban lakes using reclaimed water has not been examined. Accordingly, the microbial community diversity and structure of biofilms from the surface of multiple matrices with varying roughness (0.1, 1.0 and 10.0 μm) were characterized using a suite of molecular techniques including scanning electron microscopy, genetic fingerprinting and phospholipid-derived fatty acid analyses. Samples were largely comprised of inorganic particles, algae and numerous bacterial species; 12 phospholipid-derived fatty acid (PLFA) types were identified, significantly less than typically associated with sewage. Both growth matrix surface roughness and biofilm growth phase were shown to concur with significantly different microbial quantity and community structures. Gram-negative bacteria bacillus i15:03OH and 18:0 were the dominant bacterial genera, collectively comprising ≈75 % of identified PLFA species content. Calculated species diversity (H) and species dominance (D) exhibited identical correlational patterns with measured water quality parameters; significant positive correlations were exhibited with respect to Mg2, while significant negative correlations were found for NO3, TP, BOD, COD, SP, PO4, SO4 and pH. Results indicate that analyses of biofilm formation and structure could be effectively used to undertake integrated assessments of the ecological health of lake systems using reclaimed water. Further work is required to elucidate the optimum conditions for sample collection and analytical interpretation.

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References

  • APHA, AWWA, WEF (2005) Standard methods for the examination of water and waste water, 21st edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Atlas RM, Cerniglia CE (1995) Bioremediation of petroleum pollutants—diversity and environmental aspects of hydrocarbon biodegradation. Bioscience 45(5):332–338

    Article  Google Scholar 

  • Bailey D, Billeter R, Aviron S, Schweiger O, Herzong F (2007) The influence of thematic resolution on metric selection for biodiversity monitoring in agricultural landscapes. Landscape Ecol 22(3):461–473

    Article  Google Scholar 

  • Baty AM, Frølund B, Geesey GG, Langille S, Quintero EJ, Suci PA, Weiner RM (1996) Adhesion of bioflims to insert surfaces: a molecular level approach directed at the marine environment. Biofouling 10(1–3):111–121

    Article  Google Scholar 

  • Dong D, Yang F, Li Y, Hua X, Lǚ X, Zhang J (2005) Adsorption of Pb, Cd to Fe, Mn oxides in natural freshwater surface coatings developed in different seasons. J Environ Sci 17(1):30–36

    Google Scholar 

  • Fdz-Polanco F, Villaverd S, Garcia PA (1996) Nitrite accumulation in submerged biofilters—combined effects. Water Science Tech 34(3–4):371–378

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fernandez N, Diaz EE, Amils R, Sanz JL (2008) Analysis of microbial community during biofilm development in an anaerobic wastewater treatment reactor. Micro Ecol 56(1):121–132

    Article  Google Scholar 

  • Gan YP, Bai Y (2010) Advanced treatment and recycling technologies in Sewage treatment plants. China Build Ind Press 7(1):198–314

    Google Scholar 

  • Gibbs RA, Scutt JE, Croll BT (1993) Assimilable organic carbon concentrations and bacterial numbers in a distribution system. Water Sci Technol 27(3–4):159–166

    Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    Article  Google Scholar 

  • Hill GT, Mitkowski NA, Aldrich-Wolfe L, Emele LR, Jurkonie DD, Ficke A, Maldonado-Ramirez S, Lynch ST, Nelson EB (2000) Methods for assessing the composition and diversity of soil microbial communities. Appl Soil Ecol 15:25–36

    Article  Google Scholar 

  • Hill TCJ, Walsh KA, Harris JA, Moffett BF (2003) Using ecological diversity measures with bacterial communities, FEMS Micro. Ecology 43:1–11

    Google Scholar 

  • Hills JM, Thomason JC (1998) The effect of scales of surface roughness on the settlement of barnacle (Semibalanus balanoides) cyrids. Biofouling 12(1):57–69

    Article  Google Scholar 

  • Juanico M, Friedler E (1999) Wastewater reuse for river recovery in semi-arid Israel. Water Sci Tech 40:43–50

    Article  Google Scholar 

  • Kaurl A, Chaudhary A, Kaurl A (2005) Phospholipid fatty acid—a bioindicator of environment monitoring and assessment in soil ecosystem. Curr Sci 89(7):1102–1112

    Google Scholar 

  • Kinney CA, Furlong ET, Werner SL, Cahill JD (2006) Presence and distribution of wastewater- derived pharmaceuticals in soil irrigated with reclaimed water. Environ Toxicol Chem 25(2):317–326

    Article  Google Scholar 

  • Kinnunen PK, Kaarniranta K, Mahalka AK (2012) Protein-oxidized phospholipid interactions in cellular signaling for cell death: from biophysics to clinical correlations. Biochim Biophys Acta 18(10):2446–2455

    Article  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  Google Scholar 

  • Lear G, Niyogi D, Harding J, Dong Y, Lewis G (2009) Biofilm bacterial community structure in streams affected by acid mine drainage. Appl Env Micro 75(11):3455–3460

    Article  Google Scholar 

  • Lee YK, Powers JM (2007) Combined effect of staining substances on the discoloration of esthetic Class V dental restorative materials. J Mat Sci Mat Med 18(1):165–170

    Article  Google Scholar 

  • Liang MC, Wang TZ, Li YK, Yang PL, Liu CC, Li PX, Zhao W (2013) Structural and fractal characteristics of biofilm attached on the surfaces of aquatic plants and gravels in the rivers and lakes reusing reclaimed wastewater. Environ Earth Sci 70(5):2319–2333

    Article  Google Scholar 

  • Liu H, Fang HH (2002) Extraction of extracurricular polymeric substances (EPS) of sludges. J Biotechnol 95(3):249–256

    Article  Google Scholar 

  • Lünsdorf H, Wenderoth DF, Abraham WR (2002) Composite biofilms grown in acidic mining lakes and assessed by electron microscopy and molecular techniques. Water Air Soil Pollut 2(3):69–79

    Article  Google Scholar 

  • Marrie TJ, Costerton JW (1984) Scanning and transmission electron microscopy of in situ bacterial colonization of intravenous and intra-arterial catheters. J Clin Micro 19(5):687–693

    Google Scholar 

  • McClain JE, Williams CF (2014) Sustainability of water reclamation: long-term recharge with reclaimed wastewater does not enhance antibiotic resistance in sediment bacteria. Sustainability 6(3):1313–1327

    Article  Google Scholar 

  • Minna M, Keinanen PJ, Martikainen MH (2004) Microbial community structure and biomass in developing drinking water biofilms. Can J Micro 50:183–191

    Article  Google Scholar 

  • Morin S, Pesce S, Tlili A, Coste M, Montuelle B (2010) Recovery potential of periphytic communities in a river impacted by a vineyard watershed. Ecol Ind 10(2):419–426

    Article  Google Scholar 

  • Nozhevnikova AN, Litti YV, Nekrasova VK, Kulichevakava IS, Grigoryeva NV, Kulikov NI, Zubov MG (2012) Anaerobic ammonium oxidation (Anammox) in immobilized activated sludge biofilms during the treatment of weak wastewater. Microbiology 81(1):25–34

    Article  Google Scholar 

  • Pennanen T, Liski J, Bååth E, Kitunen VV, Uotila J, Westman CJ, Fritze H (1999) Structure of the microbial communities in Coniferous forest soils in relation to site fertility and stand development stage. Microb Ecol 38(2):168–179

    Article  Google Scholar 

  • Percival SL, Knapp JS, Wales DS, Edyvean RG (1999) The effect of turbulent flow and surface roughness on biofilm formation in drinking water. J Ind Microbiol Biotechnol 22(3):152–159

    Article  Google Scholar 

  • Qin SY (2008). Study on morphology and biodiversity of biofilm of river order (Unpublished PhD thesis). Harbin Institute of Technology, Heilongjiang, China

  • Qiu LP, Ma J (2005) Characters of biofilm and its microorganism population in biological aerobic filter. China Environ Sci 25(2):214–217

    Google Scholar 

  • Rousseau R, Van Hecke P, Nilssen D, Bogaert J (1999) The relationship between diversity profiles, evenness and species richness based on partial ordering. Environ Ecol Stat 6(2):211–223

    Article  Google Scholar 

  • Sandhu A, Halverson LJ, Beattie GA (2009) Identification and genetic characterization of phenol-degrading bacteria from leaf microbial communities. Microb Ecol 57(2):276–285

    Article  Google Scholar 

  • Scardino AJ, Harvey ER, De NR (2006) Testing attachment point theory: diatom attachment on microtextured polyimide biomimics. Biofouling 22(1):55–60

    Article  Google Scholar 

  • Schumacher JF, Carman ML, Estes TG (2007) Engineered antifouling microtopographies-effect of feature size, geometry, and roughness on settlement of zoospores of the green alga Ulva. Biofouling 23:55–62

    Article  Google Scholar 

  • Schumacher JF, Christopher J, Callow ME (2008) Engineered nanoforce gradients for inhibition of settlement (attachment) of swimming algal spores. Langmuir 24:4931–4937

    Article  Google Scholar 

  • Sekar R, Venugopalan VP, Nandakumar K, Nair KVK, Rao VN (2004) Early stages of biofilm succession in a lentic freshwater environment. Hydrobiologia 512(1–3):97–108

    Article  Google Scholar 

  • Song B, Leff LG (2006) Influence of magnesium ions on biofilm formation by Pseudomonas fluorescens. Micro Res 161(4):355–361

    Article  Google Scholar 

  • Sun HX, Liu XL (2004) Microbes studies of tea rhizosphere. Acta Ecologica Sinica 24(7):1353–1357

    Google Scholar 

  • Wagner M, Loy A (2002) Bacterial community composition and function in sewage treatment systems. Curr Opin Biotechnol 13:218–227

    Article  Google Scholar 

  • Waldrop MP, Firestone MK (2004) Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138(2):275–284

    Article  Google Scholar 

  • Wang TZ, Li YK, Liang MC, Yang PL, Bai ZH (2014) Biofilms on the surface of gravels and aquatic plants in rivers and lakes reusing reclaimed water. Environ Earth Sci 72(3):743–755

    Article  Google Scholar 

  • Wu YC, Xiang Y, Wang J, Zhong JH, He JH, Wu QL (2010) Heterogeneity of archaeal and bacterial ammonia-oxidizing communities in Lake Taihu. China Env Micro Rep 2(4):569–576

    Article  Google Scholar 

  • Zhang Z, Lei Z, Zhang Z, Sugiura N, Xu X, Yin D (2007) Organics removal of combined wastewater through shallow soil infiltration treatment: a field and laboratory study. J Hazard Mater 149:657–665

    Article  Google Scholar 

Download references

Acknowledgments

The authors acknowledge financial support provided by the National Natural Science Fund of China (Grant No. 51321001), the Beijing Eleventh Five-Year Research Program (Grant No. D090409004009004) and the Special Fund for Scientific Research of Water Conservancy in the Public Interest (Grant No. 201001067).

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Correspondence to Yunkai Li or Paul Hynds.

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Wang, T., Li, Y., Xu, T. et al. Biofilm microbial community structure in an urban lake utilizing reclaimed water. Environ Earth Sci 75, 314 (2016). https://doi.org/10.1007/s12665-015-5197-6

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  • DOI: https://doi.org/10.1007/s12665-015-5197-6

Keywords

  • Biofilm
  • Growth matrices
  • Microbial community structure
  • Reclaimed water
  • Urban Lake