Skip to main content
SpringerLink
Log in

Microbial community response to a simulated hydrocarbon spill in mangrove sediments

  • Articles
  • Published:
The Journal of Microbiology Aims and scope Submit manuscript

Abstract

In this study, we examined the hypothesis that the microbial communities in mangrove sediments with different chemical and historical characteristics respond differently to the disturbance of a hydrocarbon spill. Two different mangrove sediments were sampled, one close to an oil refinery that had suffered a recent oil spill and another that had not been in contact with oil. Based on the sampled sediment, two sets of mesocosms were built, and oil was added to one of them. They were subjected to mimicked mangrove conditions and monitored for 75 days. Archaeal and bacterial communities were evaluated through PCRDGGE. Both communities showed the emergence of small numbers of novel bands in response to oil pollution. 16S rRNA gene clone libraries were constructed from both mesocosms before the addition of oil and at day 75 after oil addition. LIBSHUFF analysis showed that both mangrove-based mesocosms contained similar communities at the start of the experiment and that they were different from the initial one, as well as from each other, after 75 days. These results hint at a role of environmental history that is not obvious from community diversity indicators, but is apparent from the response to the applied stress.

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

Similar content being viewed by others

References

  • Al-Sayed, H.A., E.H. Ghanem, and K.M. Saleh. 2005. Bacterial community and some physico-chemical characteristics in a subtropical mangrove environment in Bahrain. Mar. Pollut. Bull. 50, 147–155.

    Article  CAS  PubMed  Google Scholar 

  • Asami, H., M. Aida, and K. Watanabe. 2005. Accelerated sulfur cycle in coastal marine sediment beneath areas of intensive shellfish aquaculture. Appl. Environ. Microbiol. 71, 2925–2933.

    Article  CAS  PubMed  Google Scholar 

  • Bano, N., S. Ruffin, B. Ransom, and J.T. Hollibaugh. 2004. Phylogenetic composition of arctic ocean archaeal assemblages and comparison with antarctic assemblages. Appl. Environ. Microbiol. 70, 781–789.

    Article  CAS  PubMed  Google Scholar 

  • Brito, E.M., R. Guyoneaud, M. Goni-Urriza, A. Ranchou-Peyruse, A. Verbaere, M.A.C. Crapez, J.C.A. Wasserman, and R. Duran. 2006. Characterization of hydrocarbonoclastic bacterial communities from mangrove sediments in Guanabara bay, Brazil. Res. Microbiol. 157, 752–762.

    Article  CAS  PubMed  Google Scholar 

  • Buckley, D.H., V. Huangyutitham, T.A. Nelson, A. Rumberger, and J.E. Thies. 2006. Diversity of planctomycetes in soil in relation to soil history and environmental heterogeneity. Appl. Environ. Microbiol. 72, 4522–4531.

    Article  CAS  PubMed  Google Scholar 

  • Clarke, K.R. 1993. Nonparametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117–143.

    Article  Google Scholar 

  • Da Silva, M.L.B., R.L. Johnson, and P.J.J. Alvarez. 2007. Microbial characterization of groundwater undergoing treatment with a permeable reactive iron barrier. Environ. Eng. Sci. 24, 1122–1127.

    Article  Google Scholar 

  • DeSantis, T.Z., P. Hugenholtz, N. Larsen, M. Rojas, E.L. Brodie, K. Keller, T. Huber, D. Dalevi, P. Hu, and G.L. Andersen. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069–5072.

    Article  CAS  PubMed  Google Scholar 

  • Diaz, E. 2004. Bacterial degradation of aromatic pollutants: A paradigm of metabolic versatility. Int. Microbiol. 7, 173–180.

    CAS  PubMed  Google Scholar 

  • Duke, N.C., J.O. Meynecke, S. Dittmann, A.M. Ellison, K. Anger, U. Berger, S. Cannicci, K. Diele, K.C. Ewel, C.D. Field, N. Koedam, S.Y. Lee, C. Marchand, I. Nordhaus, and F. Dahdouh-Guebas. 2007. A world without mangroves? Science 317, 41–42.

    Article  CAS  PubMed  Google Scholar 

  • Edwards, U., T. Rogall, H. Blocker, M. Emde, and E.C. Bottger. 1989. Isolation and direct complete nucleotide determination of entire genes — characterization of a gene coding for 16S-ribosomal RNA. Nucleic Acids Res. 17, 7843–7853.

    Article  CAS  PubMed  Google Scholar 

  • El-Tarabily, K.A. 2002. Total microbial activity and microbial composition of a mangrove sediment are reduced by oil pollution at a site in the Arabian gulf. Can. J. Microbiol. 48, 176–182.

    Article  CAS  PubMed  Google Scholar 

  • Fierer, N. and R.B. Jackson. 2006. The diversity and biogeography of soil bacterial communities. PNAS 103, 626–631.

    Article  CAS  PubMed  Google Scholar 

  • Foti, M., D.Y. Sorokin, B. Lomans, M. Mussman, E.E. Zacharova, N.V. Pimenov, J.G. Kuenen, and G. Muyzer. 2007. Diversity, activity, and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl. Environ. Microbiol. 73, 2093–2100.

    Article  CAS  PubMed  Google Scholar 

  • Gomes, N.C.M., L.R. Borges, R. Paranhos, F.N. Pinto, E. Krogerrecklenfort, L.C.S. Mendonca-Hagler, and K. Smalla. 2007. Diversity of ndo genes in mangrove sediments exposed to different sources of polycyclic aromatic hydrocarbon pollution. Appl. Environ. Microbiol. 73, 7392–7399.

    Article  CAS  PubMed  Google Scholar 

  • Gomes, N.C., L.R. Borges, R. Paranhos, F.N. Pinto, L.C.S. Mendonca-Hagler, and K. Smalla. 2008. Exploring the diversity of bacterial communities in sediments of urban mangrove forests. FEMS Microbiol. Ecol. 66, 96–109.

    Article  CAS  Google Scholar 

  • Gonzalez-Acosta, B., Y. Bashan, N.Y. Hernandez-Saavedra, F. Ascencio, and G. De la Cruz-Aguero. 2006. Seasonal seawater temperature as the major determinant for populations of culturable bacteria in the sediments of an intact mangrove in an arid region. FEMS Microbiol. Ecol. 55, 311–321.

    Article  CAS  PubMed  Google Scholar 

  • Hall, T.A. 1999. Bioedit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/nt. Nucleic Acids Symposium Series 41, 95–98.

    CAS  Google Scholar 

  • Hamamura, N., S.H. Olson, D.M. Ward, and W.P. Inskeep. 2006. Microbial population dynamics associated with crude-oil biodegradation in diverse soils. Appl. Environ. Microbiol. 72, 6316–6324.

    Article  CAS  PubMed  Google Scholar 

  • Heuer, H. and K. Smalla. 1997. Evaluation of community-level catabolic profiling using Biolog GN microplates to study microbial community changes in potato phyllosphere. J. Microbiol. Methods 30, 49–61.

    Article  CAS  Google Scholar 

  • Holguin, G., M.A. Guzman, and Y. Bashan. 1992. 2 new nitrogenfixing bacteria from the rhizosphere of mangrove trees-their isolation, identification and in vitro interaction with rhizosphere Staphylococcus sp. FEMS Microbiol. Ecol. 101, 207–216.

    Article  CAS  Google Scholar 

  • Holguin, G., P. Vazquez, and Y. Bashan. 2001. The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: An overview. Biol. Fertil. Soils 33, 265–278.

    Article  CAS  Google Scholar 

  • Holmboe, N., E. Kristensen, and F.O. Andersen. 2001. Anoxic decomposition in sediments from a tropical mangrove forest and the temperate Wadden sea: Implications of N and P addition experiments. Estuar Coast Shelf Sci. 53, 125–140.

    Article  CAS  Google Scholar 

  • Hugenholtz, P. and N.R. Pace. 1996. Identifying microbial diversity in the natural environment: A molecular phylogenetic approach. Trends Biotechnol. 14, 190–197.

    Article  CAS  PubMed  Google Scholar 

  • Iwamoto, T., K. Tani, K. Nakamura, Y. Suzuki, M. Kitagawa, M. Eguchi, and M. Nasu. 2000. Monitoring impact of in situ biostimulation treatment on groundwater bacterial community by DGGE. FEMS Microbiol. Ecol. 32, 129–141.

    Article  CAS  PubMed  Google Scholar 

  • Jennerjahn, T.C. and V. Ittekkot. 2002. Relevance of mangroves for the production and deposition of organic matter along tropical continental margins. Naturwissenschaften 89, 23–30.

    Article  CAS  PubMed  Google Scholar 

  • Johnsen, A.R. and U. Karlson. 2005. PAH degradation capacity of soil microbial communities — does it depend on PAH exposure? Microb. Ecol. 50, 488–495.

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen, B.B. 1982. Mineralization of organic-matter in the sea bed — the role of sulfate reduction. Nature 296, 643–645.

    Article  Google Scholar 

  • Jukes, T.H. and C.R. Cantor. 1969. Evolution of protein molecules, pp. 21–132. In H.N. Munro (ed.), Mammalian protein metabolism, Academic Press, New York, N.Y., USA.

    Google Scholar 

  • Kjeldsen, K.U., A. Loy, T.F. Jakobsen, T.R. Thomsen, M. Wagner, and K. Ingvorsen. 2007. Diversity of sulfate-reducing bacteria from an extreme hypersaline sediment, Great Salt Lake (Utah). FEMS Microbiol. Ecol. 60, 287–298.

    Article  CAS  PubMed  Google Scholar 

  • Klepac-Ceraj, V., M. Bahr, B.C. Crump, A.P. Teske, J.E. Hobbie, and M.F. Polz. 2004. High overall diversity and dominance of microdiverse relationships in salt marsh sulphate-reducing bacteria. Environ. Microbiol. 6, 686–698.

    Article  CAS  PubMed  Google Scholar 

  • Kniemeyer, O., F. Musat, S.M. Sievert, K. Knittel, H. Wilkes, M. Blumenberg, W. Michaelis, A. Classen, C. Bolm, S.B. Joye, and F. Widdel. 2007. Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449, 898–901.

    Article  CAS  PubMed  Google Scholar 

  • Kondo, R., K.J. Purdy, S.D.Q. Silva, and D.B. Nedwell. 2007. Spatial dynamics of sulphate-reducing bacterial compositions in sediment along a salinity gradient in a UK estuary. Microb. Environ. 22, 11–19.

    Article  Google Scholar 

  • Labbe, D., R. Margesin, F. Schinner, L.G. Whyte, and C.W. Greer. 2007. Comparative phylogenetic analysis of microbial communities in pristine and hydrocarbon-contaminated alpine soils. FEMS Microbiol. Ecol. 59, 466–475.

    Article  CAS  PubMed  Google Scholar 

  • Lane, D.J. 1991. 16S/23S rRNA sequencing, pp. 115–175. In E. Stackebrandt and M. Goodfellow (eds.), Nucleic acid techniques in bacterial systematics. Wiley, New York, N.Y., USA.

    Google Scholar 

  • Lewis, R.R.I. 1983. Impact of oil spills on mangrove forests, pp. 171–183. In H.J. Teas (ed.), Tasks for vegetation science vol. 8 (biology and ecology of mangroves), Dr. W. Junk Publishers, The Hague, The Netherlands.

    Google Scholar 

  • Liang, J.B., Y.Q. Chen, C.Y. Lan, N.F.Y. Tam, Q.J. Zan, and L.N. Huang. 2007. Recovery of novel bacterial diversity from mangrove sediment. Mar. Biol. 150, 739–747.

    Article  Google Scholar 

  • Ma, Y.F., J.F. Wu, S.Y. Wang, C.Y. Jang, Y. Zhang, S.W. Qi, L. Liu, G.P. Zhao, and S.J. Liu. 2007. Nucleotide sequence of plasmid pCNB1 from Comamonas strain CNB-1 reveals novel genetic organization and evolution for 4-chloronitrobenzene degradation. Appl. Environ. Microbiol. 73, 4477–4483.

    Article  CAS  PubMed  Google Scholar 

  • Margesin, R., D. Labbe, F. Schinner, C.W. Greer, and L.G. Whyte. 2003. Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine alpine soils. Appl. Environ. Microbiol. 69, 3085–3092.

    Article  CAS  PubMed  Google Scholar 

  • Marri, P.R., W. Hao, and G.B. Golding. 2007. The role of laterally transferred genes in adaptive evolution. BMC Evol. Biol. 7(Suppl 1), S8.

    Article  PubMed  Google Scholar 

  • Miletto, M., P.L.E. Bodelier, and H.J. Laanbroek. 2007. Improved PCR-DGGE for high resolution diversity screening of complex sulfate-reducing prokaryotic communities in soils and sediments. J. Microbiol. Methods 70, 103–111.

    Article  CAS  PubMed  Google Scholar 

  • Miralles, G., V. Grossi, M. Acquaviva, R. Duran, J.C. Bertrand, and P. Cuny. 2007a. Alkane biodegradation and dynamics of phylogenetic subgroups of sulfate-reducing bacteria in an anoxic coastal marine sediment artificially contaminated with oil. Chemosphere 68, 1327–1334.

    Article  CAS  PubMed  Google Scholar 

  • Miralles, G., D. Nerini, C. Mante, M. Acquaviva, P. Doumenq, V. Michotey, S. Nazaret, J.C. Bertrand, and P. Cuny. 2007b. Effects of spilled oil on bacterial communities of mediterranean coastal anoxic sediments chronically subjected to oil hydrocarbon contamination. Microb. Ecol. 54, 646–661.

    Article  CAS  PubMed  Google Scholar 

  • Mussmann, M., K. Ishii, R. Rabus, and R. Amann. 2005. Diversity and vertical distribution of cultured and uncultured deltaproteobacteria in an intertidal mud flat of the Wadden sea. Environ. Microbiol. 7, 405–418.

    Article  PubMed  Google Scholar 

  • Muyzer, G., E.C. Dewaal, and A.G. Uitterlinden. 1993. Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genescoding for 16S ribosomal-RNA. Appl. Environ. Microbiol. 59, 695–700.

    CAS  PubMed  Google Scholar 

  • Muyzer, G. and A.J.M. Stams. 2008. The ecology and biotechnology of sulphate-reducing bacteria. Nat. Rev. Microbiol. 6, 441–454.

    CAS  PubMed  Google Scholar 

  • Oline, D.K. 2006. Phylogenetic comparisons of bacterial communities from serpentine and nonserpentine soils. Appl. Environ. Microbiol. 72, 6965–6971.

    Article  CAS  PubMed  Google Scholar 

  • Olivera, N.L., J.L. Esteves, and M.G. Commendatore. 1997. Alkane biodegradation by a microbial community from contaminated sediments in Patagonia, Argentina. Int. Biodeterior. Biodegrad. 40, 75–79.

    Article  CAS  Google Scholar 

  • Osborn, A.M., E.R.B. Moore, and K.N. Timmis. 2000. An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ. Microbiol. 2, 39–50.

    Article  CAS  PubMed  Google Scholar 

  • Perez-Jimenez, J.R. and L.J. Kerkhof. 2005. Phylogeography of sulfate-reducing bacteria among disturbed sediments, disclosed by analysis of the dissimilatory sulfite reductase genes (dsrAB). Appl. Environ. Microbiol. 71, 1004–1011.

    Article  CAS  PubMed  Google Scholar 

  • Polymenakou, P.N., A. Tselepides, E.G. Stephanou, and S. Bertilsson. 2006. Carbon speciation and composition of natural microbial communities in polluted and pristine sediments of the eastern Mediterranean sea. Mar. Pollut. Bull. 52, 1396–1405.

    Article  CAS  PubMed  Google Scholar 

  • Rees, G.N. and B.K.C. Patel. 2001. Desulforegula conservatrix gen. nov., sp. nov., a long-chain fatty acid-oxidizing, sulfate-reducing bacterium isolated from sediments of a freshwater lake. Int. J. Syst. Evol. Microbiol. 51, 1911–1916.

    CAS  PubMed  Google Scholar 

  • Salles, J.F., J.D. van Elsas, and J.A. van Veen. 2006 Effect of agricultural management regime on Burkholderia community structure in soil. Microb. Ecol. 52, 267–279.

    Article  CAS  PubMed  Google Scholar 

  • Salles, J.F., J.A. van Veen, and J.D. van Elsas. 2004. Multivariate analyses of Burkholderia species in soil: Effect of crop and land use history. Appl. Environ. Microbiol. 70, 4012–4020.

    Article  CAS  PubMed  Google Scholar 

  • Sambrook, J. and D.W. Russell. 2001. Molecular cloning: A laboratory manual (third edition). Cold Spring Harbor Laboratory Press, New York, N.Y., USA.

    Google Scholar 

  • Schloss, P.D. and J. Handelsman. 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71, 1501–1506.

    Article  CAS  PubMed  Google Scholar 

  • Singleton, D.R., M.A. Furlong, S.L. Rathbun, and W.B. Whitman. 2001. Quantitative comparisons of 16S rDNA sequence libraries from environmental samples. Appl. Environ. Microbiol. 67, 4373–4376.

    Article  Google Scholar 

  • Sousa, O.V., A. Macrae, F.G.R. Menezes, N.C.M. Gomes, R. Vieira, and L.C.S. Mendonca-Hagler. 2006. The impact of shrimp farming effluent on bacterial communities in mangrove waters, Ceara, Brazil. Mar. Pollut. Bull. 52, 1725–1734.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, D., A. Ueki, A. Amaishi, and K. Ueki. 2007a. Desulfopila aestuarii gen. nov., sp. nov., a Gram-negative, rod-like, sulfate reducing bacterium isolated from an estuarine sediment in Japan. Int. J. Syst. Evol. Microbiol. 57, 520–526.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, D., A. Ueki, A. Amaishi, and K. Ueki. 2007b. Diversity of substrate utilization and growth characteristics of sulfate-reducing bacteria isolated from estuarine sediment in Japan. J. Gen. Appl. Microbiol. 53, 119–132.

    Article  CAS  PubMed  Google Scholar 

  • Taketani, R.G., H.F. dos Santos, J.D. van Elsas, and A.S. Rosado. 2009. Characterisation of the effect of a simulated hydrocarbon spill on diazotrophs in mangrove sediment mesocosm. Antonie van Leeuwenhoek 96, 343–354.

    Article  PubMed  Google Scholar 

  • Thompson, J.D., T.J. Gibson, F. Plewniak, F. Jeanmougin, and D.G. Higgins. 1997. The Clustal-X Windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882.

    Article  CAS  PubMed  Google Scholar 

  • Wieder, R.K. and G.E. Lang. 1982. A critique of the analytical methods used examining decomposition data obtained from litter bags. Ecology 63, 1636–1642.

    Article  Google Scholar 

  • Wilms, R., B. Kopke, H. Sass, T.S. Chang, H. Cypionka, and B. Engelen. 2006. Deep biosphere-related bacteria within the subsurface of tidal flat sediments. Environ. Microbiol. 8, 709–719.

    Article  CAS  PubMed  Google Scholar 

  • Yamada, T., H. Imachi, A. Ohashi, H. Harada, S. Hanada, Y. Kamagata, and Y. Sekiguchi. 2007. Bellilinea caldifistulae gen. nov., sp. nov. and Longilinea arvoryzae gen. nov., sp. nov., strictly anaerobic, filamentous bacteria of the phylum chloroflexi isolated from methanogenic propionate-degrading consortia. Int. J. Syst. Evol. Microbiol. 57, 2299–2306.

    Article  CAS  PubMed  Google Scholar 

  • Yamada, T., Y. Sekiguchi, S. Hanada, H. Imachi, A. Ohashi, H. Harada, and Y. Kamagata. 2006. Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes anaerolineae classis nov and caldilineae classis nov in the bacterial phylum chloroflexi. Int. J. Syst. Evol. Microbiol. 56, 1331–1340.

    Article  CAS  PubMed  Google Scholar 

  • Yan, B., K. Hong, and Z.N. Yu. 2006. Archaeal communities in mangrove soil characterized by 16S rRNA gene clones. J. Microbiol. 44, 566–571.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratório de Ecologia Microbiana Molecular, Instituto de Microbiologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil

    Rodrigo Gouvêa Taketani, Natália Oliveira Franco & Alexandre Soares Rosado

  2. Microbial Ecology Department, Center for Ecological and Evolutionary Studies, University of Groningen, Groningen, 9750RA, The Netherlands

    Rodrigo Gouvêa Taketani & Jan Dirk van Elsas

Authors
  1. Rodrigo Gouvêa Taketani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Natália Oliveira Franco
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexandre Soares Rosado
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jan Dirk van Elsas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rodrigo Gouvêa Taketani.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Taketani, R.G., Franco, N.O., Rosado, A.S. et al. Microbial community response to a simulated hydrocarbon spill in mangrove sediments. J Microbiol. 48, 7–15 (2010). https://doi.org/10.1007/s12275-009-0147-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-009-0147-1

Keywords

Search

Navigation