Structural dynamics of microbial communities in polycyclic aromatic hydrocarbon-contaminated tropical estuarine sediments undergoing simulated aerobic biotreatment
- 616 Downloads
Coastal sediments contaminated by polycyclic aromatic hydrocarbons (PAHs) can be candidates for remediation via an approach like land farming. Land farming converts naturally anaerobic sediments to aerobic environments, and the response of microbial communities, in terms of community structure alterations and corresponding effects on biodegradative activities, is unknown. A key goal of this study was to determine if different sediments exhibited common patterns in microbial community responses that might serve as indicators of PAH biodegradation. Sediments from three stations in the Lagos Lagoon (Nigeria) were used in microcosms, which were spiked with a mixture of four PAH, then examined for PAH biodegradation and for shifts in microbial community structure by analysis of diversity in PAH degradation genes and Illumina sequencing of 16S rRNA genes. PAH biodegradation was similar in all sediments, yet each exhibited unique microbiological responses and there were no microbial indicators of PAH bioremediation common to all sediments.
KeywordsPolycyclic aromatic hydrocarbons Bioremediation Bacteria Sediment Illumina Lagos Lagoon
These studies were supported by graduate fellowships from the University of Lagos (to CCO) and by an endowment from the O.N. Allen Professorship in Soil Microbiology (to WJH). Processing of Illumina data through the QIIME pipeline was done by the University of Wisconsin-Madison, Bioinformatics Resource Center.
Compliance with ethical standards
This study was funded by an endowment from the O.N. Allen Professorship of Soil Science, University of Wisconsin, Madison, Wisconsin (to WJH).
Conflict of interest
The authors declare that they have no conflict of interest.
No animals or human subjects were used in these studies.
- Bordenave S, Goni-urriza M, Vilette C, Blanchard S, Caumette P, Duran R (2008) Diversity of ring-hydroxylating dioxygenases in pristine and oil contaminated microbial mats at genomic and transcriptomic levels. Environ Microbiol 10:3201–3211. doi: 10.1111/j.1462-2920.2008.01707.x CrossRefPubMedGoogle Scholar
- Bouchez-Naitali M, Blanchet D, Haeseler F, Vandecasteele JP (2008) Biodegradation of polycyclic aromatic hydrocarbons (PAHs). In: Vandecasteele JP (ed) Petroleum microbiology: concepts, environmental implications, industrial applications, Editions Technip, vol 1. Paris, France, pp 342–411Google Scholar
- Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello KE, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi: 10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
- Cebron A, Louvel B, Faure P, France-Lanord C, Chen Y, Murrell JC, Leyval C (2011) Root exudates modify bacterial diversity of phenanthrene degraders in PAH-polluted soil but not phenanthrene degradation rates. Environ Microbiol 13:722–736. doi: 10.1111/j.1462-2920.2010.02376.x CrossRefPubMedGoogle Scholar
- Cebron A, Norini MP, 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. J Microbiol Methods 73:148–159. doi: 10.1016/j.mimet.2008.01.009 CrossRefPubMedGoogle Scholar
- Chung WK, King GM (2001) Isolation, characterization, and polyaromatic hydrocarbon degradation potential of aerobic bacteria from marine macrofaunal burrow sediments and description of Lutibacterium anuloederans gen. Nov., sp nov., and Cycloclasticus spirillensus sp nov. Appl Environ Microbiol 67:5585–5592. doi: 10.1128/aem.67.12.5585-5592.2001 CrossRefPubMedPubMedCentralGoogle Scholar
- Cui ZS, Xu GS, Gao W, Li Q, Yang BJ, Yang GP, Zheng L (2014) Isolation and characterization of Cycloclasticus strains from Yellow Sea sediments and biodegradation of pyrene and fluoranthene by their syntrophic association with Marinobacter strains. Int Biodeterior Biodegradation 91:45–51. doi: 10.1016/j.ibiod.2014.03.005 CrossRefGoogle Scholar
- de Gannes V, Eudoxie G, Bekele I, Hickey WJ (2015) Relations of microbiome characteristics to edaphic properties of tropical soils from Trinidad. Front Microbiol:6. doi: 10.3389/fmicb.2015.01045
- Ding GC, Heuer H, Zühlke S, Spiteller M, Pronk GJ, Heister K, Kögel-Knabner I, Smalla K (2010) Soil type-dependent responses to phenanthrene as revealed by determining the diversity and abundance of polycyclic aromatic hydrocarbon ring-hydroxylating dioxygenase genes by using a novel PCR detection system. Appl Environ Microbiol 76:4765–4771. doi: 10.1128/aem.00047-10 CrossRefPubMedPubMedCentralGoogle Scholar
- dos Santos HF, Cury JC, Carmo FV, dosSantos AL, Tiedje J, van Elsas JD, Rosado AS, Peixoto RS (2011) Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution. PLoS One:6. doi: 10.1371/journal.pone.0016943
- Dubinsky EA, Conrad ME, Chakraborty R, Bill M, Borglin SE, Hollibaugh JT, Mason OU, Piceno YM, Reid FC, Stringfellow WT, Tom LM, Hazen TC, Andersen GL (2013) Succession of hydrocarbon-degrading bacteria in the aftermath of the Deepwater Horizon oil spill in the Gulf of Mexico. Environ Sci Technol 47:10860–10867. doi: 10.1021/es401676y
- Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi: 10.1093/nar/gkh340
- EPA (2005) Contaminated sediment remediation guidance for hazardous waste sites. National service center for environmental publications (NSCEP), Washington DCGoogle Scholar
- Fuentes S, Ding GC, Cardenas F, Smalla K, Seeger M (2015) Assessing environmental drivers of microbial communities in estuarine soils of the Aconcagua River in Central Chile. FEMS Microbiol Ecol 91. doi: 10.1093/femsec/fiv110
- Geiselbrecht AD, Hedlund BP, Tichi MA, Staley JT (1998) Isolation of marine polycyclic aromatic hydrocarbon (PAH)-degrading Cycloclasticus strains from the Gulf of Mexico and comparison of their PAH degradation ability with that of Puget sound Cycloclasticus strains. Appl Environ Microbiol 64:4703–4710PubMedPubMedCentralGoogle Scholar
- Gomes NCM, Borges LR, Paranhos R, Pinto FN, Krogerrecklenfort E, Mendonca-Hagler LCS, Smalla K (2007) Diversity of ndo genes in mangrove sediments exposed to different sources of polycyclic aromatic hydrocarbon pollution. Appl Environ Microbiol 73:7392–7399. doi: 10.1128/aem.01099-07 CrossRefPubMedPubMedCentralGoogle Scholar
- Harvey RG (1997) Polycyclic aromatic hydrocarbons. Wiley-VCH, New York, NYGoogle Scholar
- Jain PK (2014) Microbial biodegradation of polycyclic aromatic hydrocarbons In: Harzevili FD and Chen H (eds). CRC Press, Boca Raton, FL. p 331–350 doi: 10.1201/b17587-16
- Jiang L, Song M, Luo C, Zhang D, Zhang G (2015) Novel phenanthrene-degrading bacteria identified by DNA-stable isotope probing. PLoS One:10. doi: 10.1371/journal.pone.0130846
- Muangchinda C, Chavanich S, Viyakarn V, Watanabe K, Imura S, Vangnai AS, Pinyakong O (2015) Abundance and diversity of functional genes involved in the degradation of aromatic hydrocarbons in Antarctic soils and sediments around Syowa Station. Environ Sci Pollut Res 22:4725–4735. doi: 10.1007/s11356-014-3721-y CrossRefGoogle Scholar
- Muckian L, Grant R, Doyle E, Clipson N (2007) Bacterial community structure in soils contaminated by polycyclic aromatic hydrocarbons. Chemosphere 68(8):1535–1541Google Scholar
- Obi CC, Adebusoye SA, Ugoji EO, Ilori MO, Amund OO, Hickey WJ (2016) Microbial communities in sediments of Lagos lagoon, Nigeria: elucidation of community structure and potential impacts of contamination by municipal and industrial wastes. Front Microbiol 7:1213. doi: 10.3389/fmicb.2016.01213 CrossRefPubMedPubMedCentralGoogle Scholar
- Sauret C, Tedetti M, Guigue C, Dumas C, Lami R, Pujo-Pay M, Conan P, Goutx M, Ghiglione JF (2016) Influence of PAHs among other coastal environmental variables on total and PAH-degrading bacterial communities. Environ Sci Pollut Res 23:4242–4256. doi: 10.1007/s11356-015-4768-0 CrossRefGoogle 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, Van Horn 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. doi: 10.1128/aem.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi: 10.1093/molbev/msr121
- Wickle W (2000) Polycyclic aromatic hydrocarbons (PAHs) in soil—A review. J Plant Nutr Soil Sci 163:229–248Google Scholar
- Wilson MS, Herrick JB, Jeon CO, Hinman DE, Madsen EL (2003) Horizontal transfer of phnAc dioxygenase genes within one of two phenotypically and genotypically distinctive naphthalene-degrading guilds from adjacent soil environments. Appl Environ Microbiol 69:2172–2181. doi: 10.1128/aem.69.4.2172-2181.2003 CrossRefPubMedPubMedCentralGoogle Scholar
- Xia XH, Xia N, Lai Y, Dong J, Zhao P, Zhu B, Li Z, Ye W, Yuan Y, Huang J (2015) Response of PAH-degrading genes to PAH bioavailability in the overlying water, suspended sediment, and deposited sediment of the Yangtze River. Chemosphere 128:236–244. doi: 10.1016/j.chemosphere.2015.02.011 CrossRefPubMedGoogle Scholar
- Yakimov MM, Denaro R, Genovese M, Cappello S, D'Auria G, Chernikova TN, Timmis KN, Golyshin PN, Giuliano L (2005) Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons. Environ Microbiol 7:1426–1441. doi: 10.1111/j.1462-2920.2005.00829.x CrossRefPubMedGoogle Scholar
- Zhang J, Lin XG, Liu WW, Yin R (2012) Response of soil microbial community to the bioremediation of soil contaminated with PAHs. Huan Jing Ke Xue 33:2825–2831Google Scholar