Skip to main content
Log in

Aliphatic Hydrocarbon Enhances Phenanthrene Degradation by Autochthonous Prokaryotic Communities from a Pristine Seawater

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The microbial diversity and functioning around oceanic islands is poorly described, despite its importance for ecosystem homeostasis. Here, we aimed to verify the occurrence of microbe-driven phenanthrene co-oxidation in the seawater surrounding the Trindade Island (Brazil). We also used Next-Generation Sequencing to evaluate the effects of aliphatic and polycyclic aromatic hydrocarbons (PAHs) on these microbial community assemblies. Microcosms containing seawater from the island enriched with either labelled (9-14C) or non-labelled phenanthrene together with hexadecane, weathered oil, fluoranthene or pyrene, and combinations of these compounds were incubated. Biodegradation of phenanthrene-9-14C was negatively affected in the presence of weathered oil and PAHs but increased in the presence of hexadecane. PAH contamination caused shifts in the seawater microbial community—from a highly diverse one dominated by Alphaproteobacteria to less diverse communities dominated by Gammaproteobacteria. Furthermore, the combination of PAHs exerted a compounded negative influence on the microbial community, reducing its diversity and thus functional capacity of the ecosystem. These results advance our understanding of bacterial community dynamics in response to contrasting qualities of hydrocarbon contamination. This understanding is fundamental in the application and monitoring of bioremediation strategies if accidents involving oil spillages occur near Trindade Island and similar ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol. 11:R106. https://doi.org/10.1186/gb-2010-11-10-r106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Atlas RM, Hazen TC (2011) Oil Biodegradation and bioremediation: a tale of the two worst spills in U.S. history. Environ Sci Technol 45:6709–6715. https://doi.org/10.1021/es2013227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bachoon DS, Araujo MM, Hodson RE (2001) Microbial community dynamics and evaluation of bioremediation strategies in oil-impacted salt marsh microcosms. J Ind Microbiol Biot 27:72–79. https://doi.org/10.1038/sj/jim/7000165

    Article  CAS  Google Scholar 

  4. Barros JAL (1959) Relatório prévio sobre a expedição João Alberto à Ilha da Trindade. Rio de Janeiro. 75 p

  5. Beazley MJ, Martinez RJ, Rajan S, et al. (2012) Microbial community analysis of a coastal salt marsh affected by the Deepwater Horizon oil spill. PLoS One 7:e41305. https://doi.org/10.1371/journal.pone.0041305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Belkin S, Stieber M, Tiehm A, Frimmel FH, Abeliovich A, Werner P, Ulitzur S (1994) Toxicity and genotoxicity enhancement during poly-cyclic aromatic hydrocarbon biodegradation. Environ. Toxicol. Water Qual. 9:303–309. https://doi.org/10.1002/tox.2530090409

    Article  CAS  Google Scholar 

  7. Birman I, Alexander M (1996) Effect of viscosity of nonaqueous-phase liquids (NAPLs) on biodegradation of NAPL constituents. Environ. Toxicol. Chem. 15:1683–1686. https://doi.org/10.1002/etc.5620151005

    CAS  Google Scholar 

  8. Bodour AA, Guerrero-Barajas C, Jiorle BV, et al. (2004) Structure and characterization of flavolipids, a novel class of biosurfactants produced by Flavobacterium sp. strain MTN11. Appl. Environ. Microbiol. 70:114–120. https://doi.org/10.1128/AEM.70.1.114-120.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Boehm PD, Page DS, Burns WA, et al. (2001) Resolving the origin of the petrogenic hydrocarbon background in Prince William Sound, Alaska. Environ Sci Technol 35:471–479. https://doi.org/10.1021/es001421j

    Article  CAS  PubMed  Google Scholar 

  10. Bouchez M, Blanchet D, Vandecasteele JP (1995a) Degradation of polycyclic aromatic hydrocarbons by purê strains and by defined strain associations: inhibition phenomena and cometabolism. Appl Microbiol Biot 43:156–164. https://doi.org/10.1007/s002530050385

    Article  CAS  Google Scholar 

  11. Bouchez M, Blanchet D, Vandecasteele JP (1995b) Substrate avaiability in phenanthrene biodegradation: transfer mechanism and influence on metabolism. Appl Microbiol Biotecnol 43:952–960. https://doi.org/10.1007/s002530050510

    Article  CAS  Google Scholar 

  12. Bouchez M, Rakatozafy H, Marchal R, et al. (1999) Diversity of bacterial strains degrading hexadecane in relation to the mode of substrate uptake. J. Appl. Microbiol. 86:421–428. https://doi.org/10.1046/j.1365-2672.1999.00678.x

    Article  Google Scholar 

  13. Campos EJD (2006) Equatorward translation of the Vitoria Eddy in a numerical simulation. Geophys. Res. Lett. 33:L22607. https://doi.org/10.1029/2006GL026997

    Article  Google Scholar 

  14. Caporaso JG, Kuczynski J, Stombaugh J, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Caporaso JG, Lauber CL, Walters WA, et al. (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. P Natl Acad Sci USA 108(1):4516–4522. https://doi.org/10.1073/pnas.1000080107

    Article  CAS  Google Scholar 

  16. Chakraborty R, Borglin SE, Dubinsky EA, et al. (2012) Microbial response to the MC-252 oil and corexit 9500 in the Gulf of Mexico. Front. Microbiol. 3:357. https://doi.org/10.3389/fmicb.2012.00357

    PubMed  PubMed Central  Google Scholar 

  17. Chao A (1984) Nonparametric estimation of the numbers of classes in a population. Scandinavian J. Statistics 11:265–270

    Google Scholar 

  18. Coulon F, McKew BA, Osborn AM, et al. (2007) Effects of temperature and biostimulation on oil-degrading microbial communities in temperate estuarine waters. Environ. Microbiol. 9:177–186. https://doi.org/10.1111/j.1462-2920.2006.01126.x

    Article  CAS  PubMed  Google Scholar 

  19. Cui Z, Lai Q, Dong C, et al. (2008) Biodiversity of polycyclic aromatic hydrocarbon-degrading bactéria from deep sea sediments of the Middle Atlantic Ridge. Environ. Microbiol. 10:2138–2149. https://doi.org/10.1111/j.1462-2920.2008.01637.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Delgado-Baquerizo M, Maestre FT, Reich PB, et al. (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7:10541. https://doi.org/10.1038/ncomms10541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Dubinsky EA, Conrad ME, Chakraborty R, et al. (2013) Succession of hydrocarbon-degrading bacteria in the aftermath of the deepwater horizon oil spill in the Gulf of Mexico. Environ Sci Technol Lett 47:10860–10867. https://doi.org/10.1021/es401676y

    Article  CAS  Google Scholar 

  22. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  23. Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3

    Article  Google Scholar 

  24. Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264. https://doi.org/10.1093/biomet/40.3-4.237

    Article  Google Scholar 

  25. Grigalunas TA, Anderson RC, Brown Jr GM, Congar R, Meade NF, Sorensen PE (1986) Estimating the cost of oil spills: lessons from the Amoco Cadiz incident. Mar. Resour. Econ. 2:239–263. https://doi.org/10.1086/mre.2.3.42628902

    Article  Google Scholar 

  26. Gutierrez T, Singleton DR, Aitken MD, et al. (2011) Stable isotope probing of an algal bloom to identify uncultivated members of the Rhodobacteraceae associated with low-molecular-weight polycyclic aromatic hydrocarbon degradation. Appl. Environ. Microbiol. 77:7856–7860. https://doi.org/10.1128/AEM.06200-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Gutierrez T, Green DH, Nichols PD, et al. (2013a) Polycyclovorans algicola gen. nov., sp. nov., an aromatic-hydrocarbon-degrading marine bacterium found associated with laboratory cultures of marine phytoplankton. Appl. Environ. Microbiol. 79:205–214. https://doi.org/10.1128/AEM.02833-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gutierrez T, Singleton DR, Berry D, et al. (2013b) Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation DNA-SIP. ISME J 7:2091–2104. https://doi.org/10.1038/ismej.2013.98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gutierrez T, Rhodes G, Mishamandani S, et al. (2014) Polycyclic aromatic hydrocarbon degradation of phytoplankton-associated Arenibacter spp. and description of Arenibacter algicola sp. nov., an aromatic hydrocarbon-degrading bacterium. Appl. Environ. Microbiol. 80:618–628. https://doi.org/10.1128/AEM.03104-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Haldar S, Chatterjee S, Sugimoto N, et al. (2011) Identification of Vibrio campbellii isolated from diseased farm-shrimps from south India and establishment of its pathogenic potential in an Artemia model. Microbiology 157:179–188. https://doi.org/10.1099/mic.0.041475-0

    Article  CAS  PubMed  Google Scholar 

  31. Hara A, Naik S, Syutsubo K, et al. (2004) Cloning and functional analysis of alkB genes in Alcanivorax borkumensis SK2. Environ. Microbiol. 6:191–197. https://doi.org/10.1046/j.1462-2920.2003.00550.x

    Article  CAS  PubMed  Google Scholar 

  32. Harayama S, Kasai Y, Hara A (2004) Microbial communities in oil-contaminated seawater. Curr. Opin. Biotechnol. 15:205–214. https://doi.org/10.1016/j.copbio.2004.04.002

    Article  CAS  PubMed  Google Scholar 

  33. Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J. Hazard. Mater. 169:1–15. https://doi.org/10.1016/j.jhazmat.2009.03.137

    Article  CAS  PubMed  Google Scholar 

  34. Head IM, Jones DM, Roling WFM (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4:173–182. https://doi.org/10.1038/nrmicro1348

    Article  CAS  PubMed  Google Scholar 

  35. Heipieper HJ, Weber FJ, Sikkema J, Keweloh H, de Bont JA (1994) Mechanisms of resistance of whole cells to toxic organic solvents. Trends Microbiol. 12:409–415. https://doi.org/10.1016/0167-7799(94)90029-9

    CAS  Google Scholar 

  36. Hemalatha S, Veeramanikandan P (2011) Characterization of aromatic hydrocarbon degrading bactéria from petroleum contaminated sites. J Environ Protect 2:243–254. https://doi.org/10.4236/jep.2011.23028

    Article  CAS  Google Scholar 

  37. Jin HM, Kim JM, Lee HJ, Madsen EL, Jeon CO (2015) Alteromonas as a key agent of polycyclic aromatic hydrocarbon biodegradation in crude oil-contaminates coastal sediment. Environ Sci Technol 46:7731–7740. https://doi.org/10.1021/es3018545

    Article  Google Scholar 

  38. Khan SA, Bibi N, Shrewani SK (2015) Isolation, screening and co-metabolism of policyclic aromatic hydrocarbons by soil bacteria. American-Eurasian J Agric & Environ Sci 15:800–812. https://doi.org/10.5829/idosi.aejaes.2015.15.5.93218

    CAS  Google Scholar 

  39. Kleindienst S, Paul JH, Joye SB (2015) Using dispersants after oil spills: impacts on the composition and activity of microbial communities. Nat Rev Microbiol 13:388–396. https://doi.org/10.1038/nrmicro3452

    Article  CAS  PubMed  Google Scholar 

  40. Kostka JE, Prakash O, Overholt WA, Green SJ, Freyer G, Canion A, Delgardio J, Norton N, Hazen TC, Huettel M (2011) Hydrocarbon-degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the Deepwater Horizon oil spill. Appl. Environ. Microbiol. 77:7962–3974. https://doi.org/10.1128/AEM.05402-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Liu C, Wang W, Wu Y, Zhou Z, Lai Q, Shao Z (2011) Multiple alkane hydroxylase systems in a marine alkane degrader, Alcanivorax dieselolei B-5. Environ. Microbiol. 13:1168–1178. https://doi.org/10.1111/j.1462-2920.2010.02416.x

    Article  CAS  PubMed  Google Scholar 

  42. Liu Z, Liu J (2013) Evaluating bacterial community structures in oil collected from the sea surfasse and sediment in the northern Gulf of Mexico after the Deepwater Horizon oil spill. Microbiol Open 2:492–504. https://doi.org/10.1002/mbo3.89

    Article  CAS  Google Scholar 

  43. Liu Z, Liu J, Zhu Q, Wu W (2012) The weathering of oil after the Deepwater Horizon oil spill: insights from the chemical composition of the oil from the sea surface, salt marshes and sediments. Environ. Res. Lett. 18:7(3). https://doi.org/10.1088/1748-9326/7/3/035302

    CAS  Google Scholar 

  44. Lozupone C, Knight R (2015) UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71:8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005

    Article  Google Scholar 

  45. McGenity TJ, Folwell BD, McKew BA, Sanni GO (2012) Marine crude-oil biodegradation: a central role for interspecies interactions. Aquat Biosyst 8:10. https://doi.org/10.1016/j.marpolbul.2014.09.021

    Article  PubMed  PubMed Central  Google Scholar 

  46. Mehdinia A, Aghadadashi V, Fumani NS (2015) Origin, distribution and toxicological potential of polycyclic aromatic hydrocarbons in surface sediments from the Bushehr Coast, the Persian Gulf. Mar. Pollut. Bull. 90:334–338. https://doi.org/10.1016/j.marpolbul.2014.09.021

    Article  CAS  PubMed  Google Scholar 

  47. Melcher RJ, Apitz SE, Hemmingsen BB (2002) Impact of irradiation and polycyclic aromatic hydrocarbon spiking on microbial populations in marine sediment for future aging and biodegradability studies. Appl. Environ. Microbiol. 68:2858–2868. https://doi.org/10.1128/AEM.68.6.2858-2868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Meyers PA, Ishiwatari R (1993) Lacustrine organic geochemistry—an overview of indicators of organic matter sources and diagenesis in lake sediments. Org. Geochem. 20:867–900. https://doi.org/10.1016/0146-6380(93)90100-P

    Article  CAS  Google Scholar 

  49. Mishamandani S, Gutierrez T, Aitken MD (2014) DNA-based stable isotope probing coupled with cultivation methods implicates Methylophaga in hydrocarbon degradation. Fronti Microbiol 5:76. https://doi.org/10.3389/fmicb.2014.00076

    Google Scholar 

  50. Morais D, Pylro V, Clark IM, Hirsch PR, Tótola MR (2016) Responses of microbial community from tropical pristine coastal soil to crude oil contamination. Peer J. https://doi.org/10.7717/peerj.1733

  51. Neff JM (1979) Polycyclic aromatic hydrocarbons in the aquatic environment. Sources, fates and biological effects. Applied Science Publishers, London. https://doi.org/10.1016/j.ejpe.2015.03.011

    Google Scholar 

  52. Pansiripat S, Pornsunthorntawee O, Rujiravanit R, Kitiyanan B, Somboonthanate P, Chavadej S (2010) Biosurfactant production by Pseudomonas aeruginosa SP4 using sequencing batch reactors: effect of oil-to-glucose ratio. Biochem. Eng. J. 49:185–191. https://doi.org/10.1016/j.bej.2009.12.011

    Article  CAS  Google Scholar 

  53. Peterson CH, Rice SD, Short JW, Esler D, Bodkin JL, Ballachey BE, Irons DB (2003) Long-term ecosystem response to the Exxon Valdez oil spill. Science 302:2082–2086. https://doi.org/10.1126/science.1084282

    Article  CAS  PubMed  Google Scholar 

  54. Pylro VS, Roesch LF, Ortega JM, do Amaral AM, Tótola MR, Hirsch PR, Rosado AS, Góes-Neto A, da Silva AL, Rosa CA, Morais DK (2014a) Brazilian microbiome project: revealing the unexplored microbial diversity—challenges and prospects. Microbial Ecol 67:237–241. https://doi.org/10.1007/s00248-013-0302-4

    Article  Google Scholar 

  55. Pylro VS, Roesch LF, Morais DK, Clark IM, Hirsch PR, Tótola MR (2014b) Data Analysis for 16S microbial profiling from different benchtop sequencing platforms. J Microbiol Meth 107:30–37. https://doi.org/10.1016/j.mimet.2014.08.018

    Article  CAS  Google Scholar 

  56. Pylro VS, Morais DK, de Oliveira FS, dos Santos FG, Lemos LN, Oliveira G, Roesch LF (2016) BMPOS: A flexible and user-friendly tool sets for microbiome studies. Microbial Ecol 72:443–447. https://doi.org/10.1007/s00248-016-0785-x

    Article  Google Scholar 

  57. Qiao M, Wang C, Huang S, Wang D, Wang Z (2006) Composition, sources, and potential toxicological significance of PAHs in the surface sediments of the Meiliang Bay, Taihu Lake, China. Environ. Int. 32:28–33. https://doi.org/10.1016/j.envint.2005.04.005

    Article  CAS  PubMed  Google Scholar 

  58. Redmond LC, Valentine DL (2011) Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill. Proc. Natl. Acad. Sci. 109:20292–20297. https://doi.org/10.1073/pnas.1108756108

    Article  PubMed  PubMed Central  Google Scholar 

  59. Richard JY, Vogel TM (1999) Characterization of a soil bacterial consortium capable of degrading diesel fuel. Int Biodeter Biodegr 44:93–100. https://doi.org/10.1016/S0964-8305(99)00062-1

    Article  CAS  Google Scholar 

  60. Robinson MD, McCarthy DJ, Smyth JK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616

    Article  CAS  PubMed  Google Scholar 

  61. Rodrigues EM, Tótola MR (2015b) Petroleum: from basic features to hydrocarbons bioremediation in oceans. OALib 2:1–17. https://doi.org/10.4236/oalib.1102136

    Article  Google Scholar 

  62. Rodrigues EM, Kalks KH, Fernandes PL, Tótola MR (2015) Bioremediation strategies of hydrocarbons and microbial diversity in the Trindade Island shoreline—Brazil. Mar. Pollut. Bull. 101:517–525. https://doi.org/10.1016/j.marpolbul.2015.10.063

    Article  CAS  PubMed  Google Scholar 

  63. Rodrigues EM, Kalks KHM, Tótola MR (2015a) Prospect, isolation, and characterization of microorganisms for potential use in cases of oil bioremediation along the coast of Trindade Island, Brazil. J. Environ. Manag. 156:15–22. https://doi.org/10.1016/j.jenvman.2015.03.016

    Article  CAS  Google Scholar 

  64. Samanta SK, Singh OV, Jain RK (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol. 20:243–248. https://doi.org/10.1016/S0167-7799(02)01943-1

    Article  CAS  PubMed  Google Scholar 

  65. Sandrin TR, Kight WB, Maier WJ, Maier RM (2006) Influence of a nonaqueous phase liquid (NAPL) on biodegradation of phenanthrene. Biodegradation 17:423–435. https://doi.org/10.1007/s10532-005-9013-y

    Article  CAS  PubMed  Google Scholar 

  66. Santisi S, Cappello S, Catalfamo M, Mancini G, Hassanshahian M, Genovese L, Giuliano L, Yakimov MM (2015) Biodegradation of crude oil by individual bacterial strains and a mixed bacterial consortium. Braz. J. Microbiol. 46:377–387. https://doi.org/10.1590/S1517-838246120131276

    Article  PubMed  PubMed Central  Google Scholar 

  67. Schweigert N, Zehnder AJB, Eggen RIL (2001) Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Environ. Microbiol. 3:81–91

    Article  CAS  PubMed  Google Scholar 

  68. Silliman JE, Meyers PA, Eadie BJ (1998) Perylene: an indicator of alteration processes or precursor materials? Org. Geochem. 29:1737–1744. https://doi.org/10.1016/S0146-6380(98)00056-4

    Article  CAS  Google Scholar 

  69. Smith CB, Johnson CN, King GM (2012) Assessment of polyaromatic hydrocarbon degradation by potentially pathogenic environmental Vibrio parahaemolyticus isolates from coastal Louisiana, USA. Mar. Pollut. Bull. 64:138–143. https://doi.org/10.1016/j.marpolbul.2011.10.007

    Article  CAS  PubMed  Google Scholar 

  70. Soares LC (1964) As Ilhas Oceanicas. In: Azevedo A (ed) Brasil, a terra e o homem, bases físicas. Companhia Editora Nacional, São Paulo, pp. 341–378

    Google Scholar 

  71. Stagars MH, Ruff SE, Amann R, Knittel K (2015) High diversity of anaerobic alkane-degrading microbial communities in marine seep sediments based on (1-methylalkyl) succinate synthase genes. Front. Microbiol. 6:1511. https://doi.org/10.3389/fmicb.2015.01511

    PubMed  Google Scholar 

  72. Sverdrup LE, Nielsen T, Krogh PH (2002) Soil ecotoxicity of polycyclic aromatic hydrocarbons in relation to soil sorption, lipophilicity, and water solubility. Environ Sci Technol 36:2429–2435. https://doi.org/10.1021/es010180s

    Article  CAS  PubMed  Google Scholar 

  73. Tapilatu YH, Grossi V, Acquaviva M, Militon C, Bertrand JC, Cuny P (2010) Isolation of hydrocarbon-degrading extremely halophilic archaea from an uncontaminated hypersaline pond (Camargue, France). Extremophiles 14:225–231. https://doi.org/10.1007/s00792-010-0301-z

    Article  CAS  PubMed  Google Scholar 

  74. Teramoto M, Suzuki M, Okazaki F, Hatmanti A, Harayama S (2009) Oceanobacter-related bacteria are important for the degradation of petroleum aliphatic hydrocarbons in the tropical marine environment. Microbiology 155:3362–3370. https://doi.org/10.1099/mic.0.030411-0

    Article  CAS  PubMed  Google Scholar 

  75. Thompson FL, Thompson CC, Hoste B, Vandemeulebroecke K, Gullian M, Swings J (2003) Vibrio fortis sp. nov. and Vibrio hepatarius sp. nov. isolated from aquatic animals and the marine environment. Int J Syst Evol Micr 53:1495–1501. https://doi.org/10.1099/ijs.0.02658-0

    Article  CAS  Google Scholar 

  76. Vila J, Nieto JM, Mertens J, Springael D, Grifoll M (2010) Microbial community structure of a heavy fuel oil-degrading marine consortium: linking microbial dynamics with polycyclic aromatic hydrocarbon utilization. FEMS Microbiol. Ecol. 73:349–362. https://doi.org/10.1111/j.1574-6941.2010.00902.x

    CAS  PubMed  Google Scholar 

  77. Vila J, Tauler M, Grifoll M (2015) Bacterial PAH degradation in marine and terrestrial habitats. Curr Opin Biotech 33:95–102. https://doi.org/10.1016/j.copbio.2015.01.006

    Article  CAS  PubMed  Google Scholar 

  78. Vinas M, Sabaté J, Espuny MJ, Solanas AM (2005) Bacterial community dynamics and polycyclic aromatic hydrocarbon degradation during bioremediation of heavily creosote-contaminated soil. Appl. Environ. Microbiol. 71:7008–7018. https://doi.org/10.1128/AEM.71.11.7008-7018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Wang Y, Feng N, Li Q, Ding J, Zhan Y, Chang Y (2012) Isolation and characterization of bacteria associated with a syndrome disease of sea urchin Strongylocentrotus intermedius in North China. Aquac. Res. 44:691–700. https://doi.org/10.1111/j.1365-2109.2011.03073.x

    Article  Google Scholar 

  80. Wu Y, Zhang J, Mi T, Li B (2001) Occurrence of n-alkanes and polycyclic aromatic hydrocarbons in the core sediments of the Yellow Sea. Mar. Chem. 76:1–15

    Article  CAS  Google Scholar 

  81. Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr. Opin. Biotechnol. 18:257–266. https://doi.org/10.1016/j.copbio.2007.04.006

    Article  CAS  PubMed  Google Scholar 

  82. Zhong Y, Luan T, Wang X, Lan C, Tam NF (2007) Influence of growth medium on cometabolic degradation of polycyclic aromatic hydrocarbons by Sphingomonas sp. strain PheB4. App Microb and Biotechnol 75(1):175–186. https://doi.org/10.1007/s00253-006-0789-4

    Article  CAS  Google Scholar 

  83. Zhu L, Yang X, Xue C, Chen Y, Qu L, Lu W (2012) Enhanced rhamnolipids production by Pseudomonas aeruginosa based on a pH stage-controlled fed-batch fermentation process. Bioresource Tech 117:208–213. https://doi.org/10.1016/j.biortech.2012.04.091

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank the Brazilian Navy, Captain Rodrigo Otoch Chaves and Captain Sidnei da Costa Abrantes for the logistic support while collecting samples. This work was supported by the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico/CNPq) which provided all approvals and permits (project grant number 405544/2012-0 and authorisation access to genetic resources process number 010645/2013-6), FAPEMIG and CAPES. VSP receives fellowship from FAPESP (Process 2016/02219-8). This work was supported by the Brazilian Microbiome Project (http://www.brmicrobiome.org) and the National Institute of Science and Technology: Microbiome (http://www.inct-microbiome.org).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Edmo Montes Rodrigues.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rodrigues, E.M., Morais, D.K., Pylro, V.S. et al. Aliphatic Hydrocarbon Enhances Phenanthrene Degradation by Autochthonous Prokaryotic Communities from a Pristine Seawater. Microb Ecol 75, 688–700 (2018). https://doi.org/10.1007/s00248-017-1078-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-1078-8

Keywords

Navigation