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Insights into Biodegradation Through Depth-Resolved Microbial Community Functional and Structural Profiling of a Crude-Oil Contaminant Plume

  • Environmental Microbiology
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Abstract

Small-scale geochemical gradients are a key feature of aquifer contaminant plumes, highlighting the need for functional and structural profiling of corresponding microbial communities on a similar scale. The purpose of this study was to characterize the microbial functional and structural diversity with depth across representative redox zones of a hydrocarbon plume and an adjacent wetland, at the Bemidji Oil Spill site. A combination of quantitative PCR, denaturing gradient gel electrophoresis, and pyrosequencing were applied to vertically sampled sediment cores. Levels of the methanogenic marker gene, methyl coenzyme-M reductase A (mcrA), increased with depth near the oil body center, but were variable with depth further downgradient. Benzoate degradation N (bzdN) hydrocarbon-degradation gene, common to facultatively anaerobic Azoarcus spp., was found at all locations, but was highest near the oil body center. Microbial community structural differences were observed across sediment cores, and bacterial classes containing known hydrocarbon degraders were found to be low in relative abundance. Depth-resolved functional and structural profiling revealed the strongest gradients in the iron-reducing zone, displaying the greatest variability with depth. This study provides important insight into biogeochemical characteristics in different regions of contaminant plumes, which will aid in improving models of contaminant fate and natural attenuation rates.

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References

  1. Winderl C, Anneser B, Griebler C, Meckenstock RU, Lueders T (2008) Depth-resolved quantification of anaerobic toluene degraders and aquifer microbial community patterns in distinct redox zones of a tar oil contaminant plume. Appl Environ Microbiol 74(3):792–801. doi:10.1128/aem.01951-07

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Bekins BA, Cozzarelli IM, Godsy EM, Warren E, Essaid HI, Tuccillo ME (2001) Progression of natural attenuation processes at a crude oil spill site: II. Controls on spatial distribution of microbial populations. J Contam Hydrol 53(3–4):387–406. doi:10.1016/s0169-7722(01)00175-9

    Article  CAS  PubMed  Google Scholar 

  3. Bekins BA, Godsy EM, Warren E (1999) Distribution of microbial physiologic types in an aquifer contaminated by crude oil. Microb Ecol 37(4):263–275. doi:10.1007/s002489900149

    Article  PubMed  Google Scholar 

  4. Haack SK, Bekins BA (2000) Microbial populations in contaminant plumes. Hydrogeol J 8(1):63–76. doi:10.1007/s100400050008

    Article  Google Scholar 

  5. Bauer RD, Rolle M, Kürzinger P, Grathwohl P, Meckenstock RU, Griebler C (2009) Two-dimensional flow-through microcosms—versatile test systems to study biodegradation processes in porous aquifers. J Hydrol 369(3–4):284–295. doi:10.1016/j.jhydrol.2009.02.037

    Article  CAS  Google Scholar 

  6. Anneser B, Pilloni G, Bayer A, Lueders T, Griebler C, Einsiedl F, Richters L (2010) High resolution analysis of contaminated aquifer sediments and groundwater—what can be learned in terms of natural attenuation? Geomicrobiol J 27(2):130–142. doi:10.1080/01490450903456723

    Article  CAS  Google Scholar 

  7. Cozzarelli IM, Bekins BA, Baedecker MJ, Aiken GR, Eganhouse RP, Tuccillo ME (2001) Progression of natural attenuation processes at a crude-oil spill site: I. Geochemical evolution of the plume. J Contam Hydrol 53(3–4):369–385

    Article  CAS  PubMed  Google Scholar 

  8. Essaid HI, Bekins BA, Herkelrath WN, Delin GN (2011) Crude oil at the Bemidji site: 25 years of monitoring, modeling, and understanding. Ground Water 49(5):706–726. doi:10.1111/j.1745-6584.2009.00654.x

    Article  CAS  PubMed  Google Scholar 

  9. Cozzarelli IM, Bekins BA, Eganhouse RP, Warren E, Essaid HI (2010) In situ measurements of volatile aromatic hydrocarbon biodegradation rates in groundwater. J Contam Hydrol 111:48–64

    Article  CAS  PubMed  Google Scholar 

  10. Cozzarelli IM, McGuire J, Kneeshaw TA, Lorah, MM, Bekins BA Using in situ microcosms to simulate hydrocarbon biodegradation rates when a contaminant plume discharges into a wetland. In: 2010 Geological Society of America Annual Meeting, Denver, CO, 2010

  11. Rooney-Varga JN, Anderson RT, Fraga JL, Ringelberg D, Lovley DR (1999) Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Appl Environ Microbiol 65(7):3056–3063

    PubMed Central  CAS  PubMed  Google Scholar 

  12. Bauer RD, Maloszewski P, Zhang Y, Meckenstock RU, Griebler C (2008) Mixing-controlled biodegradation in a toluene plume—results from two-dimensional laboratory experiments. J Contam Hydrol 96(1–4):150–168. doi:10.1016/j.jconhyd.2007.10.008

    Article  CAS  PubMed  Google Scholar 

  13. Murphy F, Herkelrath W (1996) A sample-freezing drive shoe for a wire line piston core sampler. Ground Water Monit Remediat 16(3):86–90

    Article  Google Scholar 

  14. Suzuki MT, Taylor LT, DeLong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Appl Environ Microbiol 66(11):4605–4614. doi:10.1128/aem.66.11.4605-4614.2000

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Pereyra LP, Hiibel SR, Prieto Riquelme MV, Reardon KF, Pruden A (2010) Detection and quantification of functional genes of cellulose-degrading, fermentative, and sulfate-reducing bacteria and methanogenic archaea. Appl Environ Microbiol 76(7):2192–2202. doi:10.1128/aem.01285-09

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Kuntze K, Vogt C, Richnow H-H, Boll M (2011) Combined application of PCR-based functional assays for the detection of aromatic-compound-degrading anaerobes. Appl Environ Microbiol 77(14):5056–5061. doi:10.1128/aem.00335-11

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703

    PubMed Central  CAS  PubMed  Google Scholar 

  18. Watanabe K, Kodama Y, Harayama S (2001) Design and evaluation of PCR primers to amplify bacterial 16S ribosomal DNA fragments used for community fingerprinting. J Microbiol Meth 44(3):253–262. doi:10.1016/S0167-7012(01)00220-2

    Article  CAS  Google Scholar 

  19. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS ONE 6(12):e27310. doi:10.1371/journal.pone.0027310

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Baedecker MJ, Cozzarelli IM (1992) The determination and fate of unstable constituents in contaminated groundwater. In: Lesage S, Jackson RE (eds) Groundwater quality and analysis at hazardous waste sites. Marcel Dekker, New York, pp 425–461

    Google Scholar 

  21. Eganhouse RP, Baedecker MJ, Cozzarelli IM, Aiken GR, Thorn KA, Dorsey TF (1993) Crude oil in a shallow sand and gravel aquifer—II. Organic geochemistry. Appl Geochem 8(6):551–567. doi:10.1016/0883-2927(93)90013-7

    Article  CAS  Google Scholar 

  22. Yun J, Ueki T, Miletto M, Lovley DR (2011) Monitoring the metabolic status of Geobacter species in contaminated groundwater by quantifying key metabolic proteins with Geobacter-specific antibodies. Appl Environ Microbiol 77(13):4597–4602. doi:10.1128/aem.00114-11

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Bennett PC, Siegel DE, Baedecker MJ, Holt MF (1993) Crude oil in a shallow sand and gravel aquifer—I. Hydrogeology and inorganic geochemistry. Appl Geochem 8(6):529–549. doi:10.1016/0883-2927(93)90012-6

    Article  CAS  Google Scholar 

  24. Aklujkar M, Young N, Holmes D, Chavan M, Risso C, Kiss H, Han C, Land M, Lovley D (2010) The genome of Geobacter bemidjiensis, exemplar for the subsurface clade of Geobacter species that predominate in Fe(III)-reducing subsurface environments. BMC Genomics 11(1):490. doi:10.1186/1471-2164-11-490

    Article  PubMed Central  PubMed  Google Scholar 

  25. Campbell BJ, Yu L, Heidelberg JF, Kirchman DL (2011) Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci 108(31):12776–12781. doi:10.1073/pnas.1101405108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Tyson GW, Lo I, Baker BJ, Allen EE, Hugenholtz P, Banfield JF (2005) Genome-directed isolation of the key nitrogen fixer Leptospirillum ferrodiazotrophum sp. nov. from an acidophilic microbial community. Appl Environ Microbiol 71(10):6319–6324. doi:10.1128/aem.71.10.6319-6324.2005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was funded by the Virginia Tech Institute for Critical Technology and Applied Science and the NSF Research Experience for Undergraduates site award 1062860. This research was also supported by the USGS Toxic Substances Hydrology Program and the USGS National Research Program. Any opinions, findings, and conclusions or recommendations expressed in this paper are those of the author(s) and do not necessarily reflect the views of Virginia Tech or the NSF. Helpful review comments were provided by Denise Akob and Barbara Bekins, analytical support was provided by Jeanne Jaeschke, and GIS support provided by Melinda Erickson. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Authors and Affiliations

  1. Civil and Environmental Engineering, Rutgers, The State University of New Jersey, 96 Frelinghuysen Rd, Piscataway, NJ, USA

    Nicole Fahrenfeld

  2. U.S. Geological Survey National Research Program, 12201 Sunrise Valley Drive, Reston, VA, USA

    Isabelle M. Cozzarelli

  3. Biomedical Engineering and Sciences, Virginia Tech, 317 Kelly Hall, Blacksburg, VA, USA

    Zach Bailey

  4. Civil and Environmental Engineering, Virginia Tech, 418 Durham Hall, Blacksburg, VA, USA

    Amy Pruden

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  1. Nicole Fahrenfeld
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  2. Isabelle M. Cozzarelli
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  3. Zach Bailey
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  4. Amy Pruden
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Corresponding author

Correspondence to Nicole Fahrenfeld.

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Fahrenfeld, N., Cozzarelli, I.M., Bailey, Z. et al. Insights into Biodegradation Through Depth-Resolved Microbial Community Functional and Structural Profiling of a Crude-Oil Contaminant Plume. Microb Ecol 68, 453–462 (2014). https://doi.org/10.1007/s00248-014-0421-6

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  • DOI: https://doi.org/10.1007/s00248-014-0421-6

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