Applied Microbiology and Biotechnology

, Volume 101, Issue 10, pp 4299–4314 | Cite as

Structural dynamics of microbial communities in polycyclic aromatic hydrocarbon-contaminated tropical estuarine sediments undergoing simulated aerobic biotreatment

  • Chioma C. ObiEmail author
  • Sunday A. Adebusoye
  • Olukayode O. Amund
  • Esther O. Ugoji
  • Mathew O. Ilori
  • Curtis J. Hedman
  • William J. Hickey
Environmental biotechnology


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.


Polycyclic 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.

Ethical approval

No animals or human subjects were used in these studies.

Supplementary material

253_2017_8151_MOESM1_ESM.pdf (184 kb)
ESM 1 (PDF 184 kb)


  1. 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
  2. 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
  3. Burgess RM, Berry WJ, Mount DR, Di Toro DM (2013) Mechanistic sediment quality guidelines based on contaminant bioavailability: equilibrium partitioning sediment benchmarks. Environ Toxicol Chem 32:102–114CrossRefPubMedGoogle Scholar
  4. 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
  5. 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
  6. 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
  7. Chen BW, Huang JY, Yuan K, Lin L, Wang XW, Yang LH, Luan TG (2016) Direct evidences on bacterial growth pattern regulating pyrene degradation pathway and genotypic dioxygenase expresssion. Marine Poll Bull 105:73–80. doi: 10.1016/j.marpolbul.2016.02.054 CrossRefGoogle Scholar
  8. 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
  9. Clarke KR, Somerfield PJ, Gorley RN (2008) Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Marine Biol Ecol 366:56–69. doi: 10.1016/j.jembe.2008.07.009 CrossRefGoogle Scholar
  10. 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
  11. 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
  12. 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
  13. 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
  14. Doyle E, Muckian L, Hickey AM, Clipson N (2008) Microbial PAH degradation. In: Laskin AI, Sariaslani S, Gadd GM (eds) Advances in applied microbiology, vol 65, pp 27–66. doi: 10.1016/s0065-2164(08)00602-3 Google Scholar
  15. 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
  16. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi: 10.1093/nar/gkh340
  17. EPA (2005) Contaminated sediment remediation guidance for hazardous waste sites. National service center for environmental publications (NSCEP), Washington DCGoogle Scholar
  18. Fernandez-Luqueno F, Valenzuela-Encinas C, Marsch R, Martinez-Suarez C, Vazquez-Nunez E, Dendooven L (2011) Microbial communities to mitigate contamination of PAHs in soil-possibilities and challenges: a review. Environ Sci Pollut Res 18:12–30. doi: 10.1007/s11356-010-0371-6 CrossRefGoogle Scholar
  19. Flocco CG, Gomes NCM, Mac Cormack W, Smalla K (2009) Occurrence and diversity of naphthalene dioxygenase genes in soil microbial communities from the maritime Antarctic. Environ Microbiol 11:700–714. doi: 10.1111/j.1462-2920.2008.01858.x CrossRefPubMedGoogle Scholar
  20. 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
  21. 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
  22. 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
  23. Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243CrossRefPubMedGoogle Scholar
  24. Harvey RG (1997) Polycyclic aromatic hydrocarbons. Wiley-VCH, New York, NYGoogle Scholar
  25. 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
  26. Jiang H, Lei R, Ding S-W, Zhu S (2014) Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 15:182. doi: 10.1186/1471-2105-15-182 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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
  28. Johnston CG, Johnston GP (2012) Bioremediation of polycyclic aromatic hydrocarbons. In: Arora R (ed) Microbial biotechnology: energy and environment. CABI, Wallingford, Oxfordshire, England, pp 279–296CrossRefGoogle Scholar
  29. Magoˇc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963CrossRefGoogle Scholar
  30. Matturro B, Presta E, Rossetti S (2016) Reductive dechlorination of tetrachloroethene in marine sediments: biodiversity and dehalorespiring capabilities of the indigenous microbes. Sci Total Environ 545:445–452. doi: 10.1016/j.scitotenv.2015.12.098 CrossRefPubMedGoogle Scholar
  31. McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ (2007) Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ Microbiol 9:165–176. doi: 10.1111/j.1462-2920.2006.01125.x CrossRefPubMedGoogle Scholar
  32. Moghadam MS, Ebrahimipour G, Abtahi B, Ghassempour A, Hashtroudi MS (2014) Biodegradation of polycyclic aromatic hydrocarbons by a bacterial consortium enriched from mangrove sediments. J Environ Health Sci Eng 12:114–125. doi: 10.1186/s40201-014-0114-6 CrossRefGoogle Scholar
  33. 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
  34. 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
  35. Niepceron M, Portet-Koltalo F, Merlin C, Motelay-Massei A, Barray S, Bodilis J (2010) Both Cycloclasticus spp. and Pseudomonas spp. as PAH-degrading bacteria in the seine estuary (France). FEMS Microbiol Ecol 71:137–147. doi: 10.1111/j.1574-6941.2009.00788.x CrossRefPubMedGoogle Scholar
  36. 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
  37. Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao QH (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955. doi: 10.1111/j.1574-6976.2008.00127.x CrossRefPubMedGoogle Scholar
  38. Richardson RE (2013) Genomic insights into organohalide respiration. Curr Opin Biotechnol 24:498–505. doi: 10.1016/j.copbio.2013.02.014 CrossRefPubMedGoogle Scholar
  39. 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
  40. 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
  41. Seo J-S, Keum Y-S, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Publ Health 6:278–309. doi: 10.3390/ijerph6010278 CrossRefGoogle Scholar
  42. 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
  43. Vacca DJ, Bleam WF, Hickey WJ (2005) Isolation of soil bacteria adapted to degrade humic acid-sorbed phenanthrene. Appl Environ Microbiol 71:3797–3805. doi: 10.1128/aem.71.7.3797-3805.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 67:503–549. doi: 10.1128/mmbr.67.4.503-549.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Vila J, Tauler M, Grifoll M (2015) Bacterial PAH degradation in marine and terrestrial habitats. Curr Opin Biotechnol 33:95–102. doi: 10.1016/j.copbio.2015.01.006 CrossRefPubMedGoogle Scholar
  46. Wang BJ, Lai QL, Cui ZS, Tan TF, Shao ZZ (2008) A pyrene-degrading consortium from deep-sea sediment of the West Pacific and its key member Cycloclasticus sp P1. Environ Microbiol 10:1948–1963. doi: 10.1111/j.1462-2920.2008.01611.x CrossRefPubMedGoogle Scholar
  47. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi: 10.1128/aem.00062-07 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Wickle W (2000) Polycyclic aromatic hydrocarbons (PAHs) in soil—A review. J Plant Nutr Soil Sci 163:229–248Google Scholar
  49. 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
  50. Wu P, Wang YS, Sun FL, Wu ML, Peng YL (2014) Bacterial polycyclic aromatic hydrocarbon ring-hydroxylating dioxygenases in the sediments from the Pearl River estuary, China. Appl Microbiol Biotechnol 98:875–884. doi: 10.1007/s00253-013-4854-5 CrossRefPubMedGoogle Scholar
  51. 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
  52. 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
  53. Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18:257–266. doi: 10.1016/j.copbio.2007.04.006 CrossRefPubMedGoogle Scholar
  54. 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
  55. Zhou HW, Guo CL, Wong YS, Tam NFY (2006) Genetic diversity of dioxygenase genes in polycyclic aromatic hydrocarbon-degrading bacteria isolated from mangrove sediments. FEMS Microbiol Lett 262:148–157. doi: 10.1111/j.1574-6968.2006.00379.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Chioma C. Obi
    • 1
    • 2
    Email author
  • Sunday A. Adebusoye
    • 1
  • Olukayode O. Amund
    • 1
  • Esther O. Ugoji
    • 1
  • Mathew O. Ilori
    • 1
  • Curtis J. Hedman
    • 3
  • William J. Hickey
    • 2
  1. 1.Department of MicrobiologyUniversity of LagosLagosNigeria
  2. 2.O.N. Allen Laboratory for Soil Microbiology, Department of Soil ScienceUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.Wisconsin State Laboratory of HygieneMadisonUSA

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