Skip to main content
SpringerLink
Log in

Response of Archaeal Communities to Oil Spill in Bioturbated Mudflat Sediments

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The response of archaeal community to oil spill with the combined effect of the bioturbation activity of the polychaetes Hediste diversicolor was determined in mudflat sediments from the Aber-Benoît basin (Brittany, French Atlantic coast), maintained in microcosms. The dynamics of the archaeal community was monitored by combining comparative terminal restriction fragment length polymorphism (T-RFLP) fingerprints and sequence library analyses based on 16S rRNA genes and 16S cDNA. Methanogens were also followed by targeting the mcrA gene. Crenarchaeota were always detected in all communities irrespective of the addition of H. diversicolor and/or oil. In the presence of oil, modifications of archaeal community structures were observed. These modifications were more pronounced when H. diversicolor was added resulting in a more diverse community especially for the Euryarchaeota and Thaumarchaeota. The analysis of mcrA transcripts showed a specific structure for each condition since the beginning of the experiment. Overall, oiled microcosms showed different communities irrespective of H. diversicolor addition, while similar hydrocarbon removal capacities were observed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Aller RC (1994) Bioturbation and remineralization of sedimentary organic matter: effects of redox oscillation. Chem Geol 114(3–4):331–345

    Article  CAS  Google Scholar 

  2. Aller RC, Blair NE, Xia Q, Rude PD (1996) Remineralization rates, recycling, and storage of carbon in Amazon shelf sediments. Cont Shelf Res 16(5–6):753–786

    Article  Google Scholar 

  3. Chung WK, King GM (1999) Biogeochemical transformations and potential polyaromatic hydrocarbon degradation in macrofaunal burrow sediments. Aquat Microb Ecol 19(3):285–295

    Article  Google Scholar 

  4. Christensen M, Banta GT, Andersen O (2002) Effects of the polychaetes Nereis diversicolor and Arenicola marina on the fate and distribution of pyrene in sediments. Mar Ecol Prog Ser 237:159–172

    Article  CAS  Google Scholar 

  5. Mermillod-Blondin F, Rosenberg R, François-Carcaillet F, Norling K, Mauclaire L (2004) Influence of bioturbation by three benthic infaunal species on microbial communities and biogeochemical processes in marine sediment. Aquat Microb Ecol 36(3):271–284

    Article  Google Scholar 

  6. Laverock B, Smith CJ, Tait K, Osborn AM, Widdicombe S, Gilbert JA (2010) Bioturbating shrimp alter the structure and diversity of bacterial communities in coastal marine sediments. ISME J 4(12):1531–1544

    Article  PubMed  Google Scholar 

  7. Holmer M, Forbes VE, Forbes TL (1997) Impact of the polychaete Capitella sp. I on microbial activity in an organic-rich marine sediment contaminated with the polycyclic aromatic hydrocarbon fluoranthene. Mar Biol 128(4):679–688

    Article  CAS  Google Scholar 

  8. Gilbert F, Stora G, Desrosiers G, Deflandre B, Bertrand JC, Poggiale JC, Gagné JP (2001) Alteration and release of aliphatic compounds by the polychaete Nereis virens (Sars) experimentally fed with hydrocarbons. J Exp Mar Biol Ecol 256(2):199–213

    Article  CAS  PubMed  Google Scholar 

  9. Hickman ZA, Reid BJ (2008) Earthworm assisted bioremediation of organic contaminants. Environ Int 34(7):1072–1081

    Article  CAS  PubMed  Google Scholar 

  10. Monard C, Vandenkoornhuyse P, Le Bot B, Binet F (2010) Relationship between bacterial diversity and function under biotic control: the soil pesticide degraders as a case study. ISME J 5(6):1048–1056

    Article  PubMed Central  PubMed  Google Scholar 

  11. Liu YJ, Zaprasis A, Liu SJ, Drake HL, Horn MA (2011) The earthworm Aporrectodea caliginosa stimulates abundance and activity of phenoxyalkanoic acid herbicide degraders. ISME J 5(3):473–485

    Article  PubMed Central  PubMed  Google Scholar 

  12. Monard C, Martin-Laurent F, Vecchiato C, Francez AJ, Vandenkoornhuyse P, Binet F (2008) Combined effect of bioaugmentation and bioturbation on atrazine degradation in soil. Soil Biol Biochem 40(9):2253–2259

    Article  CAS  Google Scholar 

  13. Dollhopf SL, Hyun JH, Smith AC, Adams HJ, O'Brien S, Kostka JE (2005) Quantification of ammonia-oxidizing bacteria and factors controlling nitrification in salt marsh sediments. Appl Environ Microbiol 71(1):240–246

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Laverock B, Gilbert JA, Tait K, Osborn AM, Widdicombe S (2011) Bioturbation: impact on the marine nitrogen cycle. Biochem Soc Trans 39(1):315–320

    Article  CAS  PubMed  Google Scholar 

  15. Näslund J, Nascimento FJ, Gunnarsson JS (2010) Meiofauna reduces bacterial mineralization of naphthalene in marine sediment. ISME J 4(11):1421–1430

    Article  PubMed  Google Scholar 

  16. Stauffert M, C-L C, Jézéquel R, Barantal S, Cuny P, Gilbert F, Cagnon C, Militon C, Amouroux D, Mahdaoui F, Bouyssiere B, Stora G, Merlin F-X, Duran R (2013) Impact of crude oil on bacterial communities' structure in bioturbated sediments. Plos One 8(6):e65347. doi:10.61371/journal.pone.0065347

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89(12):5685–5689

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Chaban B, Ng SYM, Jarrell KF (2006) Archaeal habitats—from the extreme to the ordinary. Can J Microbiol 52(2):73–116

    Article  CAS  PubMed  Google Scholar 

  19. Delong EF (1998) Everything in moderation: Archaea as ‘non-extremophiles’. Curr Opin Genet Dev 8(6):649–654

    Article  CAS  PubMed  Google Scholar 

  20. Jarrell KF, Walters AD, Bochiwal C, Borgia JM, Dickinson T, Chong JPJ (2011) Major players on the microbial stage: why archaea are important. Microbiology 157(4):919–936

    Article  CAS  PubMed  Google Scholar 

  21. Al-Mailem DM, Sorkhoh NA, Al-Awadhi H, Eliyas M, Radwan SS (2010) Biodegradation of crude oil and pure hydrocarbons by extreme halophilic archaea from hypersaline coasts of the Arabian Gulf. Extremophiles 14(3):321–328

    Article  CAS  PubMed  Google Scholar 

  22. Tapilatu YH, Grossi V, Acquaviva M, Militon C, Bertrand JC, Cuny P (2010) Isolation of hydrocarbon-degrading extremely halophilic archaea from an uncontaminated hypersaline pond (Camargue, France). Extremophiles 14(2):225–231

    Article  CAS  PubMed  Google Scholar 

  23. Anderson RT, Lovley DR (2000) Hexadecane decay by methanogenesis. Nature 404(6779):722–723

    Article  CAS  PubMed  Google Scholar 

  24. Chang W, Um Y, Holoman TRP (2006) Polycyclic aromatic hydrocarbon (PAH) degradation coupled to methanogenesis. Biotechnol Lett 28(6):425–430

    Article  CAS  PubMed  Google Scholar 

  25. Cetecioglu Z, Ince BK, Kolukirik M, Ince O (2009) Biogeographical distribution and diversity of bacterial and archaeal communities within highly polluted anoxic marine sediments from the Marmara Sea. Mar Pollut Bull 58(3):384–395

    Article  CAS  PubMed  Google Scholar 

  26. Orcutt BN, Joye SB, Kleindienst S, Knittel K, Ramette A, Reitz A, Samarkin V, Treude T, Boetius A (2010) Impact of natural oil and higher hydrocarbons on microbial diversity, distribution, and activity in Gulf of Mexico cold-seep sediments. Deep-Sea Res II Top Stud Oceanogr 57(21–23):2008–2021

    Article  CAS  Google Scholar 

  27. Liu R, Zhang Y, Ding R, Li D, Gao Y, Yang M (2009) Comparison of archaeal and bacterial community structures in heavily oil-contaminated and pristine soils. J Biosci Bioeng 108(5):400–407

    Article  CAS  PubMed  Google Scholar 

  28. Miralles G, Acquaviva M, Bertrand JC, Cuny P (2010) Response of an archaeal community from anoxic coastal marine sediments to experimental petroleum contamination. Aquat Microb Ecol 59(1):25–31

    Article  Google Scholar 

  29. Taketani RG, Franco NO, Rosado AS, van Elsas JD (2010) Microbial community response to a simulated hydrocarbon spill in mangrove sediments. J Microbiol 48(1):7–15

    Article  PubMed  Google Scholar 

  30. Röling WFM, Couto De Brito IR, Swannell RPJ, Head IM (2004) Response of archaeal communities in beach sediments to spilled oil and bioremediation. Appl Environ Microbiol 70(5):2614–2620

    Article  PubMed Central  PubMed  Google Scholar 

  31. Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148(11):3521–3530

    Article  CAS  PubMed  Google Scholar 

  32. Hales BA, Edwards C, Ritchie DA, Hall G, Pickup RW, Saunders JR (1996) Isolation and identification of methanogen-specific DNA from blanket bog peat by PCR amplification and sequence analysis. Appl Environ Microbiol 62(2):668–675

    PubMed Central  CAS  PubMed  Google Scholar 

  33. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5(2):150–163

    Google Scholar 

  36. Good IJ (1953) The population frequencies of species and the estimation of the population parameters. Biometrika 40:237–264

    Article  Google Scholar 

  37. Singleton DR, Furlong MA, Rathbun SL, Whitman WB (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67(9):4374–4376

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Bordenave S, Goñi-Urriza MS, Caumette P, Duran R (2007) Effects of heavy fuel oil on the bacterial community structure of a pristine microbial mat. Appl Environ Microbiol 73(19):6089–6097

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Teske AP (2006) Microbial communities of deep marine subsurface sediments: molecular and cultivation surveys. In: Barceló, Damià, Kostianoy, Andrey G (eds) Handbook of environmental chemistry, volume 5: water pollution, vol. 23. Springer, Berlin

  40. Teske A, Sørensen KB (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J 2(1):3–18

    Article  CAS  PubMed  Google Scholar 

  41. Inagaki F, Nunoura T, Nakagawa S, Teske A, Lever M, Lauer A, Suzuki M, Takai K, Delwiche M, Colwell FS, Nealson KH, Horikoshi K, D'Hondt S, Jørgensen BB (2006) Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proc Natl Acad Sci U S A 103(8):2815–2820

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Watson AJ, Orr JC (2003) Carbon dioxide fluxes in the global ocean. In: Fasham M, Field J, Platt T, Zeitzschel B (eds) Ocean biogeochemistry: the role of the ocean carbon cycle in global change (a JGOFS Synthesis). Springer, Berlin, pp 123–141

    Chapter  Google Scholar 

  43. Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sørensen KB, Anderson R, Fredricks HF, Elvert M, Kelly TJ, Schrag DP, Sogin ML, Brenchley JE, Teske A, House CH, Hinrichs KU (2006) Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci U S A 103(10):3846–3851

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Llirós M, Gich F, Plasencia A, Auguet JC, Darchambeau F, Casamayor EO, Descy JP, Borrego C (2010) Vertical distribution of ammonia-oxidizing crenarchaeota and methanogens in the epipelagic waters of Lake Kivu (Rwanda-Democratic Republic of the Congo). Appl Environ Microbiol 76(20):6853–6863

    Article  PubMed Central  PubMed  Google Scholar 

  45. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437(7058):543–546

    Article  PubMed  Google Scholar 

  46. Preston CM, Wu KY, Molinski TF, Delong EF (1996) A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci U S A 93(13):6241–6246

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6(3):245–252

    Article  CAS  PubMed  Google Scholar 

  48. Mussmann M, Brito I, Pitcher A, Damste JSS, Hatzenpichler R, Richter A, Nielsen JL, Nielsen PH, Muller A, Daims H, Wagner M, Head IM (2011) Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc Natl Acad Sci U S A 108(40):16771–16776

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Xu MZ, Schnorr J, Keibler B, Simon HM (2012) Comparative analysis of 16S rRNA and amoA genes from Archaea selected with organic and inorganic amendments in enrichment culture. Appl Environ Microbiol 78(7):2137–2146

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Kristensen E (1984) Effect of natural concentrations on nutrient exchange between a polychaete burrow in estuarine sediment and the overlying water. J Exp Mar Biol Ecol 75(2):171–190

    Article  Google Scholar 

  51. Fenchel T (1996) Worm burrows and oxic microniches in marine sediments. 1. Spatial and temporal scales. Mar Biol 127(2):289–295

    Article  Google Scholar 

  52. Gilbert F, Stora G, Bonin P (1998) Influence of bioturbation on denitrification activity in Mediterranean coastal sediments: an in situ experimental approach. Mar Ecol Prog Ser 163:99–107

    Article  CAS  Google Scholar 

  53. Porat I, Vishnivetskaya TA, Mosher JJ, Brandt CC, Yang ZK, Brooks SC, Liang L, Drake MM, Podar M, Brown SD, Palumbo AV (2010) Characterization of archaeal community in contaminated and uncontaminated surface stream sediments. Microb Ecol 60(4):784–795

    Article  PubMed Central  PubMed  Google Scholar 

  54. Urakawa H, Garcia JC, Barreto PD, Molina GA, Barreto JC (2012) A sensitive crude oil bioassay indicates that oil spills potentially induce a change of major nitrifying prokaryotes from the Archaea to the Bacteria. Environ Pollut 164C:42–45

    Article  Google Scholar 

  55. Bonin P, Gilewicz M, Rambeloarisoa E, Mille G, Bertrand JC (1990) Effect of crude oil on denitrification and sulfate reduction in marine sediments. Biogeochemistry 10(2):161–174

    Article  CAS  Google Scholar 

  56. Heijs SK, Haese RR, van der Wielen PWJJ, Forney LJ, Van Elsas JD (2007) Use of 16S rRNA gene based clone libraries to assess microbial communities potentially involved in anaerobic methane oxidation in a Mediterranean cold seep. Microb Ecol 53(3):384–398

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Sowers KR, Ferry JG (1983) Isolation and characterization of a methylotrophic marine methanogen, Methanococcoides methylutens gen. nov., sp. nov. Appl Environ Microbiol 45(2):684–690

    PubMed Central  CAS  PubMed  Google Scholar 

  58. Lueders T, Chin KJ, Conrad R, Friedrich M (2001) Molecular analyses of methyl-coenzyme M reductase α-subunit (mcrA) genes in rice field soil and enrichment cultures reveal the methanogenic phenotype of a novel archaeal lineage. Environ Microbiol 3(3):194–204

    Article  CAS  PubMed  Google Scholar 

  59. Thauer RK (1998) 140th Ordinary Meeting of the Society for General Microbiology, 31 March 1998: biochemistry of methanogenesis: a tribute to Marjory Stephenson. Microbiology 144(9):2377–2406

    Article  CAS  PubMed  Google Scholar 

  60. Tholen A, Pester M, Brune A (2007) Simultaneous methanogenesis and oxygen reduction by Methanobrevibacter cuticularis at low oxygen fluxes. FEMS Microbiol Ecol 62(3):303–312

    Article  CAS  PubMed  Google Scholar 

  61. Hirasawa JS, Sarti A, del Aguila NKS, Varesche MBA (2008) Application of molecular techniques to evaluate the methanogenic archaea and anaerobic bacteria in the presence of oxygen with different COD:Sulfate ratios in a UASB reactor. Anaerobe 14(4):209–218

    Article  CAS  PubMed  Google Scholar 

  62. Harris JM (1993) The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis. Microb Ecol 25(3):195–231

    Article  CAS  PubMed  Google Scholar 

  63. Wilde SB, Plante CJ (2002) Spatial heterogeneity of bacterial assemblages in marine sediments: the influence of deposit feeding by Balanoglossus aurantiacus. Estuarine Coastal Shelf Sci 55(1):97–107

    Article  Google Scholar 

  64. Lucas FS, Bertru G, Höfle MG (2003) Characterization of free-living and attached bacteria in sediments colonized by Hediste diversicolor. Aquat Microb Ecol 32(2):165–174

    Article  Google Scholar 

  65. Ficker M, Krastel K, Orlicky S, Edwards E (1999) Molecular characterization of a toluene-degrading methanogenic consortium. Appl Environ Microbiol 65(12):5576–5585

    PubMed Central  CAS  PubMed  Google Scholar 

  66. Zengler K, Richnow HH, Rossello-Mora R, Michaelis W, Widdel F (1999) Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401(6750):266–269

    Article  CAS  PubMed  Google Scholar 

  67. Kimes NE, Callaghan AV, Aktas DF, Smith WL, Sunner J, Golding BT, Drozdowska M, Hazen TC, Suflita JM, Morris PJ (2013) Metagenomic analysis and metabolite profiling of deep-sea sediments from the Gulf of Mexico following the Deepwater Horizon oil spill. Front Microbiol 4:50. doi:10.3389/fmicb.2013.00050

    PubMed Central  PubMed  Google Scholar 

  68. Watanabe K, Kodama Y, Hamamura N, Kaku N (2002) Diversity, abundance, and activity of archaeal populations in oil-contaminated groundwater accumulated at the bottom of an underground crude oil storage cavity. Appl Environ Microbiol 68(8):3899–3907

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Kasai Y, Takahata Y, Hoaki T, Watanabe K (2005) Physiological and molecular characterization of a microbial community established in unsaturated, petroleum-contaminated soil. Environ Microbiol 7(6):806–818

    Article  CAS  PubMed  Google Scholar 

  70. Yoshida N, Yagi K, Sato D, Watanabe N, Kuroishi T, Nishimoto K, Yanagida A, Katsuragi T, Kanagawa T, Kurane R, Tani Y (2005) Bacterial communities in petroleum oil in stockpiles. J Biosci Bioeng 99(2):143–149

    Article  CAS  PubMed  Google Scholar 

  71. Jones DM, Head IM, Gray ND, Adams JJ, Rowan AK, Aitken CM, Bennett B, Huang H, Brown A, Bowler BFJ, Oldenburg T, Erdmann M, Larter SR (2008) Crude-oil biodegradation via methanogenesis in subsurface petroleum reservoirs. Nature 451(7175):176–180

    Article  CAS  PubMed  Google Scholar 

  72. Siddique T, Penner T, Semple K, Foght JM (2011) Anaerobic biodegradation of longer-chain n-alkanes coupled to methane production in oil sands tailings. Environ Sci Technol 45(13):5892–5899

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by ANR (DHYVA project 06-SEST-009). We thank all the partners of the DHYVA project for their useful discussions.

Author information

Authors and Affiliations

  1. Equipe Environnement et Microbiologie, IPREM - UMR CNRS 5254, Université de Pau et des Pays de l’Adour, BP 1155, 64013, Pau Cedex, France

    Magalie Stauffert, Robert Duran, Claire Gassie & Cristiana Cravo-Laureau

Authors
  1. Magalie Stauffert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert Duran
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claire Gassie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cristiana Cravo-Laureau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert Duran.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stauffert, M., Duran, R., Gassie, C. et al. Response of Archaeal Communities to Oil Spill in Bioturbated Mudflat Sediments. Microb Ecol 67, 108–119 (2014). https://doi.org/10.1007/s00248-013-0288-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0288-y

Keywords

Search

Navigation