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Impact of petroleum hydrocarbon contamination on the indigenous soil microbial community

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Abstract

Changes in the microbial community structure in agricultural soils and soils contaminated with hydrocarbons were evaluated using the culture-independent method of 16S rRNA gene sequence analysis. The bacterial composition was more diverse in the agricultural soil (AS) samples in terms of number of species and Shannon diversity index [6.6 vs. 1.94 for the hydrocarbon-contaminated soil (HCS)]. Twelve known bacterial groups were identified in the AS: Proteobacteria (41 % of bacterial community), Actinobacteria (34 %), Acidobacteria (5 %), Firmicutes (4 %), Chloroflexi (4 %), Bacteroidetes (3 %), Gemmatimonadetes, Planctomycetes, Verrucomicrobia, Armatimonadetes, Cyanobacteria, TM7 and Archaea (the latter 7 each accounting for 1–2%) . In comparison, the clonal library from the HCS samples included members from only five groups: Proteobacteria (85 %) and Bacteriodetes, Actinobacteria, Chloroflexi and Verrucomicrobia (the latter four collectively accounting for 15 %). The family Ectothiorhodospiraceae was the most dominant family within the Proteobacteria isolated from the HCS. These microbes are known to synthesize a number of biotechnologically useful products, such as polyhydroxyalkanoates and ectoines, and their dominance in the sampled area suggests the possibility of discovering better adapted novel genes of commercial importance, especially since the site had high alkaline and saline characteristics. Soils (arid, alpine and polar) which are nutrient and moisture limited are typically often dominated by Actinobacteria that are well adapted to low-resource environments and do not show major changes in community structure as a result of hydrocarbon contamination.

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References

  • Abou-Shanab RA, van Berkum P, Angle JS (2007) Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68:360–367

    Article  CAS  PubMed  Google Scholar 

  • Achtman M, Wagner M (2008) Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6:431–440. doi:10.1038/nrmicro1872

    CAS  PubMed  Google Scholar 

  • Buckley DH, Schmidt TM (2003) Diversity and dynamics of microbial communities in soils from agro-ecosystems. Environ Microbiol 5:441–452

    Article  PubMed  Google Scholar 

  • Felsenstein J (1989) PHYLIP—Phylogeny inference package (version 32). Cladistics 5:164–166

    Google Scholar 

  • Galinski EA, Herzog RM (1990) The role of trehalose as a substitute for nitrogen containing compatible solutes (Ectothiorhodospira halochloris). Arch Microbiol 153:607–613

    Article  CAS  Google Scholar 

  • Goodfellow M, Williams ST (1983) Ecology of actinomycetes. Annu Rev Microbiol 37:189–216

    Article  CAS  PubMed  Google Scholar 

  • Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–685

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hedlund BP, Gosink JJ, Staley JT (1997) Verrucomicrobia div. nov., a new division of the bacteria containing three new species of Prothecobacter. Ant v Leeuwenhoeck 72:29–38

  • Herschkovitz Y, Lerner A, Davidov Y, Okon Y, Jurkevitch E (2005) Azospirillum brasilense does not affect population structure of specific rhizobacterial communities of inoculated maize (Zea mays). Environ Microbiol 7:1847–1852

    Article  CAS  PubMed  Google Scholar 

  • Hetzer A, Daughney CJ, Morgan HW (2006) Cadmium ion biosorption by the thermophilic bacteria Geobacillus stearothermophilus and G. thermocatenulatus. Appl Environ Microbiol 72:4020–4027

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kalia VC, Chauhan A, Bhattacharyya G, Rashmi (2003) Genomic databases yield novel bioplastic producers. Nat Biotechnol 21:845–846

    Article  CAS  PubMed  Google Scholar 

  • Kapur M, Jain RK (2004) Microbial diversity: exploring the unexplored. WFCC Newsl 39:12–16

    Google Scholar 

  • Köberl M, Müller H, Ramadan EM, Berg G (2011) Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health. PLoS ONE 6(9):e24452. doi:10.1371/journal.pone.0024452

    Article  PubMed Central  PubMed  Google Scholar 

  • Kothe E, Dimkpa C, Haferburg G, Schmidt A, Schmidt A, Schütze E (2010) Streptomycetes heavy metal resistance: extracellular and intracellular mechanisms. In: Sherameti I, Varma A (eds) Soil heavy metals. Springer, Berlin, pp 225–235

    Chapter  Google Scholar 

  • Lal B, Khanna S (1996) Degradation of crude oil by Acinetobacter calcoaceticus and Alcaligenes odorans. J Appl Bacteriol 81:355–362

    CAS  PubMed  Google Scholar 

  • Lăzăroaie MM (2009) Investigation of saturated and aromatic hydrocarbon resistance mechanisms in Pseudomonas aeruginosa IBBML1 Cent Eur. J Biol 4:469–481

    Google Scholar 

  • Liang Y, Van Nostrand JD, Deng Y, He Z, Wu L, Zhang X, Li G, Zhou J (2011) Functional gene diversity of soil microbial communities from five oil-contaminated fields in China. ISME J 5:403–413

    Article  PubMed Central  PubMed  Google Scholar 

  • Marinari S, Mancinelli R, Campiglia E, Grego S (2006) Chemical and biological indicators of soil quality in organic and convewntional farming system in Central Italy. Ecol Indic 6:701–711

    Article  Google Scholar 

  • Mishra S, Jyoti J, Kuhad RC, Lal B (2001) Evaluation of inoculum addition to stimulate in situ bioremediation of oily-sludge-contaminated soil. Appl Environ Microbiol 67:675–1681

    Article  Google Scholar 

  • Nautiyal CS, Chauhan PS, Bhatia CR (2010) Changes in soil physico-chemical properties and microbial functional diversity due to 14 years of conversion of grassland to organic agriculture in semi-arid agroecosystem. Soil Tillage Res 109:55–60

    Article  Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 1 2nd edn. Agronomy Monogr No 9. American Society of Agronomy (ASA), Madison, pp 539–581

  • Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, VanHorn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sheik CS, Mitchell TW, Rizvi FZ, Rehman Y, Faisal M et al (2012) Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. PLoS ONE 7(6):e40059. doi:10.1371/journal.pone.0040059

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shi W, Becker J, Bischoff M, Turco RF, Konopka AE (2002) Association of microbial community composition and activity with lead, chromium, and hydrocarbon contamination. Appl Environ Microbiol 68:3859–3866

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Singh SP, Purohit MK, Raval VH, Pandey S, Akbari VG, Rawal CM (2010) Capturing the potential of haloalkaliphilic bacteria from the saline habitats through culture dependent and metagenomic approaches. In: Mendez-Vilas A (ed) Current research, technology and education topics in applied microbiology and microbial biotechnology. Formatex Research Center, Badajoz, pp 81–87

    Google Scholar 

  • Sorokin DY, Trotsenko YA, Doronina NV, Tourova TP, Galinski EA, Kolganova TV, Muyzer G (2007) Methylohalomonas lacus gen. nov., sp nov and Methylonatrum kenyense gen. nov., sp. nov., methylotrophic gamma proteobacteria from hypersaline lakes. Int J Syst Evol Microbiol 57:2762–2769

  • Steven B, Lionard M, Kuske CR, Vincent WF (2013) High bacterial diversity of biological soil crusts in water tracks over permafrost in the high arctic polar desert. PLoS ONE 8(8):e71489. doi:10.1371/journal.pone.0071489

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stoeck T, Kasper J, Bunge J, Leslin C, Ilyin V, Epstein S (2007) Protistan diversity in the arctic: a case of paleoclimate shaping modern biodiversity? PLoS ONE 2:e728. doi:10.1371/journal.pone.0000728

    Article  PubMed Central  PubMed  Google Scholar 

  • Stoffels M, Amann R, Ludwig W, Hekmat D, Schleifer KH (1998) Bacterial community dynamics during start-up of a trickle-bed bioreactor degrading aromatic compounds. Appl Environ Microbiol 64:930–939

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sutton NB, Maphosa F, Morillo JA, Abu Al-Soud W, Langenhoff AA, Grotenhuis T, Rijnaarts HH, Smidt H (2013) Impact of long-term diesel contamination on soil microbial community structure. Appl Environ Microbiol 79:619–630. doi:10.1128/AEM.02747-12. Epub 2012 Nov 9

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Torsvik V, Sørheim R, Goksøyr J (1996) Total bacterial diversity in soil and sediment communities. J Ind Microbiol Biotechnol 17:170–178

    Article  CAS  Google Scholar 

  • Tourova TP, Spiridonova EM, Berg IA, Slobodova NV, Boulygina ES, Sorokin DY (2007) Phylogeny and evolution of the family Ectothiorhodospiraceae based on comparison of 16S rRNA, cbbL and nifH gene sequences. Int J Syst Evol Microbiol 57:2387–2398

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Kolvek S, Goodwin S, Len RW (2004) Poly(hydroxyalkanoic acid) Biosynthesis in Ectothiorhodospira shaposhnikovii: characterization and reactivity of a Type III PHA synthase. Biomacromolecules 5:40–48

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the Department of Biotechnology, Government of India for funding of this research and the Council of Scientific and Industrial Research, New Delhi, for providing fellowship to Simrita Cheema.

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Authors and Affiliations

  1. Centre for Bioresources and Biotechnology, TERI University, Plot No.10, Institutional Area, Vasant Kunj, New Delhi, 110070, India

    Simrita Cheema

  2. Microbial Biotechnology Division, TERI, India Habitat Centre, Lodhi Road, New Delhi, 110003, India

    Simrita Cheema, Meeta Lavania & Banwari Lal

  3. Environmental and Industrial Biotechnology, TERI University, Darbari Seth Block, India Habitat Center, Lodhi Road, New Delhi, 110003, India

    Banwari Lal

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  1. Simrita Cheema
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  2. Meeta Lavania
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  3. Banwari Lal
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Correspondence to Banwari Lal.

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Cheema, S., Lavania, M. & Lal, B. Impact of petroleum hydrocarbon contamination on the indigenous soil microbial community. Ann Microbiol 65, 359–369 (2015). https://doi.org/10.1007/s13213-014-0868-1

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  • DOI: https://doi.org/10.1007/s13213-014-0868-1

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