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Temporal bacterial diversity associated with metal-contaminated river sediments

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Abstract

The temporal activity, abundance and diversity of microbial communities were evaluated across a metal-contamination gradient around a Superfund site in Montana. In order to analyze short-term variability, samples were collected from six sites on four occasions over 12 months. Measurements of community activity, diversity and richness, quantified by dehydrogenase activity and through denaturant gradient gel electrophoresis (DGGE), respectively, were higher at contaminated sites adjacent to the smelter, relative to reference sites. 16S rRNA gene copy numbers, measured by quantitative PCR, showed seasonal variability, yet were generally higher within polluted sediments. Jaccard similarity coefficients of DGGE profiles, found sites to cluster based primarily on geographical proximity rather than geochemical similarities. Intra-site clustering of the most polluted sites also suggests a stable metal-tolerant community. Sequences from DGGE-extracted bands were predominantly Beta and Gammaproteobacteria, although the communities at all sites generally maintained a diverse phylogeny changing in composition throughout the sampling period. Spearman’s rank correlations analysis found statistically significant relationships between community composition and organic carbon (r-value = 0.786) and metals (r-values As = 0.65; Cu = 0.63; Zn = 0.62). A diverse and abundant community at the most polluted site indicates that historical contamination selects for a metal-resistant microbial community, a finding that must be accounted for when using the microbial community within ecosystem monitoring studies. This study highlights the importance of using multiple time-points to draw conclusions on the affect of metal contamination.

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References

  • Atekwana EA, Atekwana E, Legall FD, Krishnamurthy RV (2004) Field evidence for geophysical detection of subsurface zones of enhanced microbial activity. Geophys Res Lett 31:L23603

    Article  Google Scholar 

  • Barkay T, Miller SM, Summer AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384

    Article  CAS  Google Scholar 

  • Bouskill NJ, Handy RD, Ford TE, Galloway TS (2006) Differentiating copper and arsenic toxicity using biochemical biomarkers in Aseullus aquaticus and Driessena polymorpha. Ecotoxicol Environ Saf 65:342–349

    Article  CAS  Google Scholar 

  • Bouskill NJ, Barnhart EP, Galloway TS, Handy RD, Ford TE (2007) Quantification of changing Pseudomonas aeruginosa soda, htpX and mt gene abundance in response to trace metal toxicity: a potential in situ biomarker of environmental health. FEMS Microbiol Ecol 60:276–286

    Article  CAS  Google Scholar 

  • Bowen ZH, Bouee KD, Waddle TJ (2003) Effects of flow regulation on shallow water habitat dynamics and floodplain connectivity. Trans Am Fish Soc 132:809–823

    Article  Google Scholar 

  • Brick CM, Moore JN (1996) Diel variation of aqueous trace metals in the upper Clark Fork River, Montana. Environ Sci Technol 30:1953–1960

    Article  CAS  Google Scholar 

  • Cain DJ, Luoma SN, Wallace WG (2004) Linking metal bioaccumulation of aquatic insects to their distribution patterns in a mining-impacted river. Environ Toxicol Chem 23:1463–1473

    Article  CAS  Google Scholar 

  • Cole JR, Chai B, Farris RJ et al (2006) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35:D169–D172

    Article  Google Scholar 

  • Crump B, Hobbie J (2005) Synchrony and seasonality in bacterioplankton communities of two temperate rivers. Limnol Oceanogr 50:1718–1729

    CAS  Google Scholar 

  • Davis A, Atkins D (2001) Metal distribution in Clark Fork River sediments. Environ Sci Technol 35:3501–3506

    Article  CAS  Google Scholar 

  • De Mesel I, Derycke S, Moens T, Van der Gucht K, Vincx M, Swings J (2004) Top down impact of bacterivorous nematodes on the bacterial community structure: a microcosm study. Environ Microbiol 6:733–744

    Article  Google Scholar 

  • Del Giorgio PA, Bouvier TC (2002) Linking the physiologic and phylogenetic successions in free-living bacterial communities along an estuarine gradient. Limnol Oceanogr 47:471–486

    CAS  Google Scholar 

  • DePlessis KR, Botha A, Joubert L, Bester R, Conradie WJ, Wolfaardt GM (2005) Response of the microbial community to copper oxychloride in acidic sandy loam soil. J Appl Microbiol 98:901

    Article  CAS  Google Scholar 

  • Ellis RJ, Morgan P, Weightman AJ, Fry JC (2003) Cultivation-dependent and -independent approaches for determining bacterial diversity in heavy-metal contaminated soil. Appl Environ Microbiol 69:3223–3230

    Article  CAS  Google Scholar 

  • Feris KP, Ramsey PW, Frazar C, Moore JN, Gannon JE, Holben WE (2003) Differences in hyporheic-zone microbial community structure along a heavy-metal contamination gradient. Appl Environ Microbiol 69:5563–5573

    Article  CAS  Google Scholar 

  • Ferris MJ, Muyzer G, Ward DM (1996) Denaturant gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Appl Environ Microbiol 62:340–346

    CAS  Google Scholar 

  • Finlay BJ (2002) Global dispersion of free-living microbial eukaryote species. Science 296:1061–1063

    Article  CAS  Google Scholar 

  • Ford TE, Jay J, Patel A, Kile M, Prommasith P, Galloway T, Sanger R, Smith K, Depledge M (2005) Use of ecotoxicological tools to evaluate the health of New Bedford Harbor sediments: a microbial biomarker approach. Environ Health Perspect 113:186–191

    CAS  Google Scholar 

  • Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S (2006) Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci USA 103:13104–13109

    Article  CAS  Google Scholar 

  • Gadd G (2004) Microbial influence on metal mobility and application for bioremediation. Geoderma 122:109–119

    Article  CAS  Google Scholar 

  • Ganguly S, Jana BB (2002) Cadmium induced adaptive responses of certain biogeochemical cycling bacteria in an aquatic system. Water Res 36:1667–1676

    Article  CAS  Google Scholar 

  • Gillan DC, Danis B, Pernet P, Joly G, Dubois P (2005) Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Appl Environ Microbiol 72:679–690

    Article  CAS  Google Scholar 

  • Griffiths BS, Kuan HL, Ritz K, Glover LA, McCaig AE, Fenwick C (2004) The relationship between microbial community structure and functional stability tested experimentally in an upland pasture soil. Microb Ecol 47:104–113

    Article  CAS  Google Scholar 

  • Hamamura N, Macur RE, Korf S, Ackerman G, Taylor WP, Kozubal M, Reysenbach AL, Inskeep WP (2009) Linking microbial oxidation of arsenic with detection and phylogenetic analysis of arsenite oxidase genes in diverse geothermal environments. Environ Sci Technol 11:421–431

    CAS  Google Scholar 

  • Heidelberg JF, Seshadri R, Haveman SA et al (2004) The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22:554–559

    Article  CAS  Google Scholar 

  • Hullar MAJ, Kaplan LA, Stahl DA (2006) Recurring seasonal dynamics of microbial communities in stream habitats. Appl Environ Microbiol 72:713–722

    Article  CAS  Google Scholar 

  • Irha N, Slet J, Petersell V (2003) Effect of heavy metals and PAH on soil assessed via dehydrogenase assay. Environ Int 28:779–782

    Article  CAS  Google Scholar 

  • Janse I, Bok J, Zwart G (2004) A simple remedy against artifactual double bands in denaturant gradient gel electrophoresis. J Microbiol Meth 57:279–281

    Article  CAS  Google Scholar 

  • Jessup CM, Kassen R, Forde SE, Kerr B, Buckling A, Rainey PB, Bohannan BJ (2004) Big questions, small worlds: microbial model systems in ecology. Trends Ecol Evol 19:189–197

    Article  Google Scholar 

  • Knight BP, McGrath SP, Chaudri AM (1997) Biomass carbon measurements and substrate utilization patterns of microbial populations from soils amended with cadmium, copper or zinc. Appl Environ Microbiol 63:39–43

    CAS  Google Scholar 

  • Korthals GW, Bongers M, Fokkema A, Dueck TA, Lexmond TM (2000) Joint toxicity of copper and zinc to a terrestrial nematode community in an acid sandy soil. Ecotoxicology 9:219–228

    Article  CAS  Google Scholar 

  • Maindonald J, Braun J (2003) Data analysis and graphics using R. An example-based approach. Cambridge University Press, Cambridge

    Google Scholar 

  • Mathew M, Obbard JF (2001) Optimization of the dehydrogenase assay for measurement of indigenous microbial activity in beach sediments contaminated with petroleum. Biotechnol Lett 23:227–230

    Article  CAS  Google Scholar 

  • Middleton SS, Latmani RB, Mackey MR, Ellisman MH, Tebo BM, Criddle CS (2003) Cometabolism of Cr(VI) by Shewanella oneidensis MR-1 produces cell-associated reduced chromium and inhibits growth. Biotechnol Bioeng 83:627–637

    Article  CAS  Google Scholar 

  • Moore JN, Luoma SN, Peters D (1991) Downstream effects of mine effluents on an intermontane riparian system. Can J Fish Aquat Sci 48:222–232

    Article  Google Scholar 

  • Mukhopadhyay R, Rosen BP, Phung LT, Silver S (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26:311–325

    Article  CAS  Google Scholar 

  • Nies D (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339

    Article  CAS  Google Scholar 

  • Radojkovic D, Kusic J (2000) Silver staining of denaturing gradient electrophoresis gels. Clin Chem 46:883–884

    CAS  Google Scholar 

  • Rasmussen LD, Sorensen SJ (2001) Effects of mercury contamination on the culturable heterotrophic, functional and genetic diversity of the bacterial community in soil. FEMS Microbiol Ecol 36:1–9

    Article  CAS  Google Scholar 

  • Rhine ED, Garcia-Dominguez E, Phelps CD, Young LY (2005) Environmental microbes can speciate and cycle arsenic. Environ Sci Technol 39:9569–9573

    Article  CAS  Google Scholar 

  • Rossel D, Tarradellas J, Bitton G, Morel JL (1997) Use of enzymes in ecotoxicology: a case for dehydrogenase and hydrolytic enzymes. CRC Lewis, Boca Raton

    Google Scholar 

  • Rusk JA, Hamon RE, Stevens DP, McLaughlin MJ (2004) Adaptation of soil biological nitrification to heavy metals. Environ Sci Technol 38:3092–3097

    Article  CAS  Google Scholar 

  • Sanchez-Moreno S, Camargo JA, Navas A (2006) Ecotoxicological assessment of the impact of residual heavy metals on soil nematodes in the Guadiamar River Basin (Southern Spain). Environ Monit Assess 116:245–262

    Article  CAS  Google Scholar 

  • Sandaa R, Torsvik VV, Enger Daae FL, Castberg T, Hahn D (1999) Analysis of bacterial communities in heavy metal-contaminated sediments a different levels of resolution. FEMS Microbiol Ecol 30:237–251

    Article  CAS  Google Scholar 

  • Silver S (1998) Genes for all metals—a bacterial view of the periodic table. The 1996 Thom award lecture. J Ind Microbiol Biotechnol 20:1–12

    Article  CAS  Google Scholar 

  • Sorci J, Paulauskis JD, Ford T (1999) 16S rRNA restriction fragment length polymorphism analysis of bacterial diversity as a biomarker of ecological health in polluted sediments from New Bedford Harbor, Massachusetts, USA. Mar Pollut Bull 38:663–675

    Article  CAS  Google Scholar 

  • Stephenson FH (2003) Quantitation of nucleic acids. In: Stephenson FH (ed) Calculations for molecular biology and biotechnology. Academic Press, London

    Google Scholar 

  • Swofford DL (1991) PAUP: Phylogenetic Analysis Using Parsimony. Sinauer, Fitchberg

    Google Scholar 

  • Weinbauer MG, Rassoulzadegan F (2004) Are viruses driving microbial diversification and diversity? Environ Microbiol 6:1–11

    Article  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    CAS  Google Scholar 

  • Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976–978

    Article  CAS  Google Scholar 

  • Wong KW, Toh BA, Ting YP, Obbard JP (2005) Biodegradation of phenanthrene by the indigenous microbial biomass in a zinc amended soil. Lett Appl Microbiol 40:50–55

    Article  CAS  Google Scholar 

  • Xu R, Obbard JP (2004) Biodegradation of polycyclic aromatic hydrocarbons in oil-contaminated beach sediments treated with nutrient amendments. J Environ Qual 33:861–867

    Article  CAS  Google Scholar 

  • Zhou J, Xia B, Treves DS, Wu L-Y, Marsh TL, O’Neill RV, Palumbo AV, Tiedje JM (2002) Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microbiol 68:326–334

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to acknowledge the assistance of Mark Skidmore, Steve Hamner, Elliot Barnhart and Sue Broadaway (MSU) for help with sample collection and chemical analysis. The constructive comments of two anonymous reviewers helped improve the manuscript. This publication was made possible by grant number 5 P42 ES05947 from the National Institute of Environmental Health Sciences, NIH, and through grants from the Montana ideas network for biomedical research excellence (INBRE). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of NIEHS, NIH.

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Correspondence to Nicholas J. Bouskill.

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Bouskill, N.J., Barker-Finkel, J., Galloway, T.S. et al. Temporal bacterial diversity associated with metal-contaminated river sediments. Ecotoxicology 19, 317–328 (2010). https://doi.org/10.1007/s10646-009-0414-2

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