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Microbial diversity and hydrocarbon depletion in low and high diesel-polluted soil samples from Keller Peninsula, South Shetland Islands

Published online by Cambridge University Press:  08 December 2014

Juliano C. Cury
Affiliation:
Universidade Federal de São João Del-Rei, Sete Lagoas, Minas Gerais, Brazil Laboratório de Ecologia Microbiana Molecular, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Diogo A. Jurelevicius
Affiliation:
Laboratório de Genética Microbiana, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Helena D.M. Villela
Affiliation:
Laboratório de Ecologia Microbiana Molecular, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Hugo E. Jesus
Affiliation:
Laboratório de Ecologia Microbiana Molecular, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Raquel S. Peixoto
Affiliation:
Laboratório de Ecologia Microbiana Molecular, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Carlos E.G.R. Schaefer
Affiliation:
Departamento de Solos, Universidade Federal de Viçosa, Minas Gerais, Brazil
Marcia C. Bícego
Affiliation:
Instituto Oceanográfico, Universidade de São Paulo, São Paulo, Brazil
Lucy Seldin*
Affiliation:
Laboratório de Genética Microbiana, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Alexandre S. Rosado
Affiliation:
Laboratório de Ecologia Microbiana Molecular, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
*
*Corresponding author: [email protected]

Abstract

The bioremediation of Antarctic soils is a challenge due to the harsh conditions found in this environment. To characterize better the effect of total petroleum hydrocarbon (TPH) concentrations on bacterial, archaeal and microeukaryotic communities in low (LC) and high (HC) hydrocarbon-contaminated soil samples from the Maritime Antarctic clone libraries (small-subunit rRNA genes) were constructed. The results showed that a high concentration of hydrocarbons resulted in a decrease in bacterial and eukaryotic diversity; however, no effect of the TPH concentration was observed for the archaeal community. The HC soil samples demonstrated a high relative abundance of bacterial operational taxonomic units (OTUs) affiliated with unclassified group TM7 and eukaryotic OTUs affiliated with unclassified fungi from Pezizomycotina subphyla. Chemical analyses of the LC and HC soil samples revealed the presence of negligible amounts of nitrogen, thereby justifying the use of biostimulation to remediate these Antarctic soils. Microcosm experiments showed that the application of fertilizers led to an increase of up to 27.8% in the TPH degradation values. The data presented here constitute the first step towards developing the best method to deploy bioremediation in Antarctic soils and provide information to indicate an appropriate action plan for immediate use in the case of new accidents.

Type
Biological Sciences
Copyright
© Antarctic Science Ltd 2014 

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References

Aislabie, J., Ryburn, J. & Sarmah, A. 2008. Hexadecane mineralization activity in ornithogenic soil from Seabee Hook, Cape Hallett, Antarctica. Polar Biology, 31, 421428.Google Scholar
Aislabie, J. & Foght, J.M. 2010. Response of polar soil bacterial communities to fuel spills. In Bej, A.K., Aislabie, J. & Atlas, R.M., eds. Polar microbiology. The ecology, biodiversity and bioremediation potential of microorganisms in extremely cold environments. Boca Raton, FL: Taylor & Francis, 215230.Google Scholar
Alvarez, V.M., Marques, J.M., Korenblum, E. & Seldin, L. 2011. Comparative bioremediation of crude oil-amended tropical soil microcosms by natural attenuation, bioaugmentation, or bioenrichment. Applied and Environmental Soil Science, 2011, 101155/2011/156320.CrossRefGoogle Scholar
Ashelford, K.E., Chuzhanova, N.A., Fry, J.C., Jones, A.J. & Weightman, A.J. 2006. New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Applied and Environmental Microbiology, 72, 57345741.Google Scholar
Atlas, R.M. & Hazen, T.C. 2011. Oil biodegradation and bioremediation: a tale of the two worst spills in US history. Environmental Science & Technology, 45, 67096715.Google Scholar
Ball, A. & Truskewycz, A. 2013. Polyaromatic hydrocarbon exposure: an ecological impact ambiguity. Environmental Science and Pollution Research, 20, 43114326.Google Scholar
Bano, N., Ruffin, S., Ransom, B. & Hollibaugh, J.T. 2004. Phylogenetic composition of Arctic Ocean archaeal assemblages and comparison with Antarctic assemblages. Applied and Environmental Microbiology, 70, 781789.CrossRefGoogle ScholarPubMed
Bell, T.H., Yergeau, E., Martineau, C., Juck, D., Whyte, L.G. & Greer, C.W. 2011. Identification of nitrogen-incorporating bacteria in petroleum-contaminated arctic soils by using [15N]DNA-based stable isotope probing and pyrosequencing. Applied and Environmental Microbiology, 77, 41634171.Google Scholar
Bell, T.H., Yergeau, E., Maynard, C., Juck, D., Whyte, L.G. & Greer, C.W. 2013. Predictable bacterial composition and hydrocarbon degradation in Arctic soils following diesel and nutrient disturbance. ISME Journal, 7, 12001210.Google Scholar
Bell, T.H., Hassan, S.E., Lauron-Moreau, A., Al-Otaibi, F., Hijri, M., Yergeau, E. & St-Arnaud, M. 2014. Linkage between bacterial and fungal rhizosphere communities in hydrocarbon-contaminated soils is related to plant phylogeny. ISME Journal, 8, 331343.CrossRefGoogle ScholarPubMed
Bícego, M.C., Taniguchi, S., Yogui, G.T., Montone, R.C., Da Silva, D.A.M., Lourenço, R.A., Martins, C.C., Sasaki, S.T., Pellizari, V.H. & Weber, R.R. 2006. Assessment of contamination by polychlorinated biphenyls and aliphatic and aromatic hydrocarbons in sediments of the Santos and São Vicente Estuary System, São Paulo, Brazil. Marine Pollution Bulletin, 52, 18041816.CrossRefGoogle Scholar
Callaghan, A.V., Davidova, I.A., Savage-Ashlock, K., Parisi, V.A., Gieg, L.M., Suflita, J.M., Kukor, J.J. & Wawrik, B. 2010. Diversity of benzyl- and alkylsuccinate synthase genes in hydrocarbon-impacted environments and enrichment cultures. Environmental Science & Technology, 44, 72877294.CrossRefGoogle ScholarPubMed
Cébron, A., Norini, M.P., Beguiristain, T. & Leyval, C. 2008. Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHD alpha) genes from Gram positive and Gram negative bacteria in soil and sediment samples. Journal of Microbiological Methods, 73, 148159.Google Scholar
Chao, A. & Lee, S.M. 1992. Estimating the number of classes via sample coverage. Journal of the American Statistical Association, 87, 210217.Google Scholar
Chao, A. 1987. Estimating the population size for capture-recapture data with unequal catchability. Biometrics, 43, 783791.CrossRefGoogle ScholarPubMed
Chenier, M.R., Beaumier, D., Roy, R., Driscoll, B.T., Lawrence, J.R. & Greer, C.W. 2003. Impact of seasonal variations and nutrient inputs on cycling nitrogen and degradation of hexadecane by replicated river biofilms. Applied and Environmental Microbiology, 69, 51705177.CrossRefGoogle ScholarPubMed
Delille, D., Coulon, F. & Pelletier, E. 2004. Biostimulation of natural microbial assemblages in oil-amended vegetated and desert sub-Antarctic soils. Microbial Ecology, 47, 407415.Google Scholar
Ewing, B. & Green, P. 1998. Base-calling of automated sequencer traces using Phred. II. Error probabilities. Genome Research, 8, 186194.Google Scholar
Ferguson, S.H., Woinarski, A.Z., Snape, I., Morris, C.E. & Revill, A.T. 2004. A field trial of in situ chemical oxidation to remediate long-term diesel contaminated Antarctic soil. Cold Regions Science and Technology, 40, 4760.Google Scholar
Ferrari, B.C., Winsley, T.J., Bergquist, P.L. & van Dorst, J. 2012. Flow cytometry in environmental microbiology: a rapid approach for the isolation of single cells for advanced molecular biology analysis. Methods in Molecular Biology, 881, 326.Google Scholar
Ferrari, B.C., Zhang, C.D. & van Dorst, J. 2011. Recovering greater fungal diversity from pristine and diesel fuel contaminated sub-Antarctic soil through cultivation using both a high and a low nutrient media approach. Frontiers in Microbiology, 2, 10.3389/fmicb 2011.00217.CrossRefGoogle Scholar
Flocco, C.G., Gomes, N.C.M., MacCormack, W. & Smalla, K. 2009. Occurrence and diversity of naphthalene dioxygenase genes in soil microbial communities from the Maritime Antarctic. Environmental Microbiology, 11, 700714.Google Scholar
Good, I.J. & Toulmin, G. 1956. The number of new species, and the increase of population coverage, when a sample is increased. Biometrika, 43, 4563.Google Scholar
Hamamura, N., Olson, S.H., Ward, D.M. & Inskeep, W.P. 2006. Microbial population dynamics associated with crude-oil biodegradation in diverse soils. Applied and Environmental Microbiology, 72, 63166324.CrossRefGoogle ScholarPubMed
Hugenholtz, P., Tyson, G.W., Webb, R.I., Wagner, A.M. & Blackall, L.L. 2001. Investigation of candidate division TM7, a recently recognized major lineage of the domain Bacteria with no known pure-culture representatives. Applied and Environmental Microbiology, 67, 411419.Google Scholar
Jurelevicius, D., Alvarez, V.M., Peixoto, R., Rosado, A.S. & Seldin, L. 2012a. Bacterial polycyclic aromatic hydrocarbon ring-hydroxylating dioxygenases (PAH-RHD) encoding genes in different soils from King George Bay, Antarctic Peninsula. Applied Soil Ecology, 55, 10.1016/j.apsoil.2011.12.008.Google Scholar
Jurelevicius, D., Alvarez, V.M., Peixoto, R., Rosado, A.S. & Seldin, L. 2013. The use of a combination of alkB primers to better characterize the distribution of alkane-degrading bacteria. PLoS One, 8, 10.1371/journal.pone0066565.CrossRefGoogle ScholarPubMed
Jurelevicius, D., Cotta, S.R., Peixoto, R., Rosado, A.S. & Seldin, L. 2012b. Distribution of alkane-degrading bacteria communities in soils from King George Island, Maritime Antarctic. European Journal of Soil Biology, 51, 3744.Google Scholar
Kuntze, K., Shinoda, Y., Moutakki, H., McInerney, M.J., Vogt, C., Richnow, H.H. & Boll, M. 2008. 6-Oxocyclohex-1-ene-1-carbonyl-coenzyme A hydrolases from obligately anaerobic bacteria: characterization and identification of its gene as a functional marker for aromatic compounds degrading anaerobes. Environmental Microbiology, 10, 15471556.CrossRefGoogle ScholarPubMed
Maturin, L.J. & Peeler, J.T. 2001. Aerobic plate count. In Hammack, T., Feng, P., Jinneman, K., Regan, P.M., Kase, J., Orlandi P. & Burkhardt, W., eds. Bacteriological analytical manual. Arlington, TX: AOAC International, 301310.Google Scholar
Mills, H.J., Martinez, R.J., Story, S. & Sobecky, P.A. 2004. Identification of members of the metabolically active microbial populations associated with Beggiatoa species mat communities from Gulf of Mexico cold-seep sediments. Applied and Environmental Microbiology, 70, 54475458.Google Scholar
Moktali, V., Park, J., Fedorova-Abrams, N.D., Park, B., Choi, J., Lee, Y.H. & Kang, S. 2012. Systematic and searchable classification of cytochrome P450 proteins encoded by fungal and oomycete genomes. BMC Genomics, 13, 10 1186/1471-2164-13-525.Google Scholar
Moon-van der Staay, S.Y., de Wachter, R. & Vaulot, D. 2001. Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature, 409, 607610.Google Scholar
Panicker, G., Mojib, N., Aislabie, J. & Bej, A.K. 2010. Detection, expression and quantitation of the biodegradative genes in Antarctic microorganisms using PCR. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 97, 275287.Google Scholar
Powell, S.M., Bowman, J.P., Ferguson, S.H. & Snape, I. 2010. The importance of soil characteristics to the structure of alkane-degrading bacterial communities on sub-Antarctic Macquarie Island. Soil Biology & Biochemistry, 42, 20122021.Google Scholar
Sambrook, J. & Russell, D.W. 2001. In molecular cloning: a laboratory manual. New York, NY: Cold Spring Harbour Laboratory Press, 2344 pp.Google Scholar
Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., van Horn, D.J. & Weber, C.F. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 75377541.Google Scholar
Shannon, C.E. & Weaver, W. 1949. The mathematical theory of communication. Chicago, IL: University of Illinois Press, 144 pp.Google Scholar
Simas, F.N.B., Schaefer, C.E.G.R., Melo, V.F., Albuquerque-Filho, M.R., Michel, R.F.M., Pereira, V.V., Gomes, M.R.M. & da Costa, L.M. 2007. Ornithogenic cryosols from Maritime Antarctica: phosphatization as a soil forming process. Geoderma, 138, 191203.Google Scholar
Wang, Q., Garrity, G.M., Tiedje, J.M. & Cole, J.R. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73, 52615267.Google Scholar
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