Comparative analysis of bacterial community-metagenomics in coastal Gulf of Mexico sediment microcosms following exposure to Macondo oil (MC252)

Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology

Volumn 106, Issue 5, 2014, Pages 993-1009

  Koo, Hyunmin ^a   Mojib, Nazia ^a,b   Thacker, Robert W ^a   Bej, Asim K ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

Biodegradative genes; Bioinformatics; Hydrocarbonoclastic bacteria; Oil spill; PCR; Pyrosequencing; Qiime

Indexed keywords

BACTERIAL DNA; BACTERIAL RNA; MACONDO OIL; OIL; RIBOSOME RNA; UNCLASSIFIED DRUG; POLYCYCLIC AROMATIC HYDROCARBON; RIBOSOME DNA; RNA 16S;

AMPLICON; ARTICLE; BACTERIAL GENE; BACTERIUM CULTURE; BACTERIUM DETECTION; BACTERIUM IDENTIFICATION; BACTEROIDETES; BIODEGRADATION; CONTROLLED STUDY; DYADOBACTER; EXIGUOBACTERIUM; FIRMICUTES; GENE AMPLIFICATION; GULF OF MEXICO; HALOMONAS; METAGENOMICS; MICROBIAL COMMUNITY; MICROCOSM; MOLLICUTES; NONHUMAN; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; PROTEOBACTERIA; PSEUDOALTEROMONAS; PYROSEQUENCING; SEDIMENT; SPECIES COMPARISON; SPECIES COMPOSITION; SPECIES DIFFERENCE; SPECIES DIVERSITY; SPECIES DOMINANCE; BIOTA; BIOTRANSFORMATION; CHEMISTRY; CLUSTER ANALYSIS; DNA SEQUENCE; DRUG EFFECTS; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY;

BACTERIA (MICROORGANISMS);

BIOTA; BIOTRANSFORMATION; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; GEOLOGIC SEDIMENTS; GULF OF MEXICO; METABOLIC NETWORKS AND PATHWAYS; METAGENOMICS; MOLECULAR SEQUENCE DATA; OILS; PHYLOGENY; POLYCYCLIC HYDROCARBONS, AROMATIC; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84910011209     PISSN: 00036072     EISSN: 15729699     Source Type: Journal    
DOI: 10.1007/s10482-014-0268-3     Document Type: Article

References (74)

1. Acosta-Martinez V, Dowd S, Sun Y, Allen V (2008) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40(11):2762–2770
2. Armougom F, Raoult D (2009) Exploring microbial diversity using 16S rRNA high-throughput methods. J Comput Sci Syst Biol 2(1):74–92
3. Atlas RM, Hazen TC (2011) Oil biodegradation and bioremediation: a tale of the two worst spills in U.S. history. Environ Sci Technol 45(16):6709–6715
4. Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JG, Sideman JG, Struhl K (1987) Short protocols in molecular biology: a compendium of methods from current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y. Greene Pub
5. Azam F, Fenchel T, Field JG, Gray J, Meyer-Reil L, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263
6. Baelum J, Borglin S, Chakraborty R, Fortney JL, Lamendella R, Mason OU, Auer M, Zemla M, Bill M, Conrad ME, Malfatti SA, Tringe SG, Holman HY, Hazen TC, Jansson JK (2012) Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill. Environ Microbiol 14(9):2405–2416
7. Beazley MJ, Martinez RJ, Rajan S, Powell J, Piceno YM, Tom LM, Andersen GL, Hazen TC, Van Nostrand JD, Zhou J, Mortazavi B, Sobecky PA (2012) Microbial community analysis of a coastal salt marsh affected by the Deepwater Horizon oil spill. PloSone 7(7):e41305–e41317
8. Brakstad OG, Bonaunet K (2006) Biodegradation of petroleum hydrocarbons in seawater at low temperatures (0–5 °C) and bacterial communities associated with degradation. Biodegradation 17(1):71–82
9. Brakstad OG, Lodeng AG (2005) Microbial diversity during biodegradation of crude oil in seawater from the North Sea. Microb Ecol 49(1):94–103
10. Campagna C, Short FT, Polidoro BA, McManus R, Collette BB, Pilcher NJ, Mitcheson YS, Stuart SN, Carpenter KE (2011) Gulf of Mexico oil blowout increases risks to globally threatened species. Bioscience 61(5):393–397
11. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26(2):266–267
12. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena 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 (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336
13. Chakraborty R, Borglin SE, Dubinsky EA, Andersen GL, Hazen TC (2012) Microbial response to the MC-252 Oil and Corexit 9500 in the Gulf of Mexico. Front Microbiol 3:357–362
14. Cho SH, Oh KH (2012) Removal of crude oil by microbial consortium isolated from oil-spilled area in the Korean Western coast. Bull Environ Contam Toxicol 89(3):680–685
15. D’Ippolito S, de Castro RE, Herrera Seitz K (2011) Chemotactic responses to gas oil of Halomonas spp. strains isolated from saline environments in Argentina. Rev Argent Microbiol 43(2):107–110
16. Deppe U, Richnow HH, Michaelis W, Antranikian G (2005) Degradation of crude oil by an arctic microbial consortium. Extremophiles 9(6):461–470
17. dos Santos HF, Cury JC, do Carmo, FL, dos Santos 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(3):e16943–e16951
18. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8(1):125–132
19. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461
20. Edlund A, Jansson JK (2008) Use of bromodeoxyuridine immunocapture to identify psychrotolerant phenanthrene-degrading bacteria in phenanthrene-enriched polluted Baltic Sea sediments. FEMS Microbiol Ecol 65(3):513–525
21. Evans FF, Rosado AS, Sebastián GV, Casella R, Machado PL, Holmström C, Kjelleberg S, Elsas JD, Seldin L (2004) Impact of oil contamination and biostimulation on the diversity of indigenous bacterial communities in soil microcosms. FEMS Microbiol Ecol 49(2):295–305
22. Fenchel T (1988) Marine plankton food chains. Annu Rev Ecol Syst 19:19–38
23. Fenchel T (2008) The microbial loop–25 years later. J Exp Mar bio Ecol 366(1):99–103
24. Freeman M, Gidiere S, Samuels M (2010) The Oil Spill’s Impact on Gulf Coast Oysters. Environmental Law Reporter: News & Analysis 40(11):11097
25. Gotelli NJ, Colwell RK (2011) Estimating species richness. Biological diversity: frontiers in measurement and assessment: 39–54
26. Hasegawa R, Toyama K, Miyanaga K, Tanji Y (2014) Identification of crude-oil components and microorganisms that cause souring under anaerobic conditions. Appl Microbiol Biotechnol 98(4):1853–1861
27. Hazen TC, Dubinsky EA, DeSantis TZ, Andersen GL, Piceno YM, Singh N, Jansson JK, Probst A, Borglin SE, Fortney JL, Stringfellow WT, Bill M, Conrad ME, Tom LM, Chavarria KL, Alusi TR, Lamendella R, Joyner DC, Spier C, Baelum J, Auer M, Zemla ML, Chakraborty R, Sonnenthal EL, D’Haeseleer P, Holman HY, Osman S, Lu Z, Van Nostrand JD, Deng Y, Zhou J, Mason OU (2010) Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330(6001):204–208
28. Head IM, Jones DM, Röling WF (2006) Marine microorganisms make a meal of oil. Nat Rev Microgiol 4(3):173–182
29. Hedlund BP, Geiselbrecht AD, Bair TJ, Staley JT (1999) Polycyclic aromatic hydrocarbon degradation by a new marine bacterium, Neptunomonas naphthovorans gen. nov., sp. nov. Appl Environ Microbiol 65(1):251–259
30. Hernandez-Raquet G, Budzinski H, Caumette P, Dabert P, Le Menach K, Muyzer G, Duran R (2006) Molecular diversity studies of bacterial communities of oil polluted microbial mats from the Etang de Berre (France). FEMS Microbiol Ecol 58(3):550–562
31. Hicken CE, Linbo TL, Baldwin DH, Willis ML, Myers MS, Holland L, Larsen M, Stekoll MS, Rice SD, Collier TK (2011) Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish. Proc Natl Acad Sci 108(17):7086–7090
32. Huang JP, Swain AK, Thacker RW, Ravindra R, Andersen DT, Bej AK (2013) Bacterial diversity of the rock-water interface in an East Antarctic freshwater ecosystem, Lake Tawani (P)†. Aquat Biosyst 9(1):4–14
33. Hughes JB, Hellmann JJ (2005) The application of rarefaction techniques to molecular inventories of microbial diversity. Methods Enzymol 397:292–308
34. Jimenez N, Vinas M, Bayona JM, Albaiges J, Solanas AM (2007) The Prestige oil spill: bacterial community dynamics during a field biostimulation assay. Appl Microbiol Biotechnol 77(4):935–945
35. Kimes NE, Callaghan AV, Aktas DF, Smith WL, Sunner J, Golding B, Drozdowska M, Hazen TC, Suflita JM, Morris PJ (2013) Metagenomic analysis and metabolite profiling of deep–sea sediments from the Gulf of Mexico following the Deepwater Horizon oil spill. Front Microbiol 4(50):eCollection 2013. doi:10.3389/fmicb.2013.00050
36. Koo H, Mojib N, Huang JP, Donahoe RJ, Bej AK Bacterial community shift in the coastal Gulf of Mexico salt-marsh sediment microcosm in vitro following exposure to the Mississippi Canyon Block 252 oil (MC252) 3 Biotech: 1–14
37. 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(22):7962–7974
38. Kryachko Y, Dong X, Sensen CW, Voordouw G (2012) Compositions of microbial communities associated with oil and water in a mesothermic oil field. Antonie Van Leeuwenhoek 101(3):493–506
39. Kvenvolden K, Cooper C (2003) Natural seepage of crude oil into the marine environment. Geo-Mar Lett 23(3–4):140–146
40. Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82(20):6955–6959
41. Li H, Zhang Y, Li DS, Xu H, Chen GX, Zhang CG (2009) Comparisons of different hypervariable regions of rrs genes for fingerprinting of microbial communities in paddy soils. Soil Biol Biochem 41(5):954–968
42. Liang JB, Chen YQ, Lan CY, Tam NFY, Zan QJ, Huang LN (2007) Recovery of novel bacterial diversity from mangrove sediment. Mar Biol 150(5):739–747
43. Liu Z, DeSantis TZ, Andersen GL, Knight R (2008) Accurate taxonomy assignments from 16S rRNA sequences produced by highly parallel pyrosequencers. Nucleic Acids Res 36(18):e120–e131
44. Liu Z, Liu J (2013) Evaluating bacterial community structures in oil collected from the sea surface and sediment in the northern Gulf of Mexico after the Deepwater Horizon oil spill. Microbiology Open 2(3):492–504
45. Lozupone C, Hamady M, Knight R (2006) UniFrac–an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7(1):371–385
46. Martinez-Murcia AJ, Anton AI, Rodriguez-Valera F (1999) Patterns of sequence variation in two regions of the 16S rRNA multigene family of Escherichia coli. Int J Syst Bacteriol 49:601–610
47. Mason OU, Hazen TC, Borglin S, Chain PS, Dubinsky EA, Fortney JL, Han J, Holman HY, Hultman J, Lamendella R, Mackelprang R, Malfatti S, Tom LM, Tringe SG, Woyke T, Zhou J, Rubin EM, Jansson JK (2012) Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill. ISME J 6(9):1715–1727
48. McKew BA, Coulon F, Yakimov MM, Denaro R, Genovese M, Smith CJ, Osborn AM, Timmis KN, McGenity TJ (2007) Efficacy of intervention strategies for bioremediation of crude oil in marine systems and effects on indigenous hydrocarbonoclastic bacteria. Environ Microbiol 9(6):1562–1571
49. 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(6):2858–2868
50. Mendelssohn IA, Andersen GL, Baltz DM, Caffey RH, Carman KR, Fleeger JW, Joye SB, Lin Q, Maltby E, Overton EB (2012) Oil impacts on coastal wetlands: implications for the Mississippi River Delta ecosystem after the Deepwater Horizon oil spill. Bioscience 62(6):562–574
51. Mohanty G, Mukherji S (2008) Enhancement of NAPL bioavailability by induction of cell-surface hydrophobicity in Exiguobacterium aurantiacum and Burkholderia cepacia. J Biotechnol 7(3):295–306
52. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59(3):695–700
53. Panicker G, Mojib N, Aislabie J, Bej AK (2010) Detection, expression and quantitation of the biodegradative genes in Antarctic microorganisms using PCR. Antonie Van Leeuwenhoek 97(3):275–287
54. Pope PB, Mackenzie AK, Gregor I, Smith W, Sundset MA, McHardy AC, Morrison M, Eijsink VG (2012) Metagenomics of the svalbard reindeer rumen microbiome reveals abundance of polysaccharide utilization loci. PloSone 7(6):e38571–e38580
55. Ritchie KB, Keller BD (2008) A scientific forum on the Gulf of Mexico: The Islands in the Stream Concept. Marine Sanctuaries Conservation Series NMSP-08-04. US Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Sanctuary Program, Silver Spring, MD, p.105
56. Roling WF, Milner MG, Jones DM, Lee K, Daniel F, Swannell RJ, Head IM (2002) Robust hydrocarbon degradation and dynamics of bacterial communities during nutrient-enhanced oil spill bioremediation. Appl Environ Microbiol 68(11):5537–5548
57. Ryerson TB, Aikin KC, Angevine WM, Atlas EL, Blake DR, Brock CA, Fehsenfeld FC, Gao RS, de Gouw JA, Fahey DW, Holloway JS, Lack DA, Lueb RA, Meinardi S, Middlebrook AM, Murphy DM, Neuman JA, Nowak JB, Parrish DD, Peischl J, Perring AE, Pollack IB, Ravishankara AR, Roberts JM, Schwarz JP, Spackman JR, Stark H, Warneke C, Watts LA (2011) Atmospheric emissions from the Deepwater Horizon spill constrain air-water partitioning, hydrocarbon fate, and leak rate. Geophys Res Lett 38(7):L07803–L07808
58. Ryerson TB, Camilli R, Kessler JD, Kujawinski EB, Reddy CM, Valentine DL, Atlas E, Blake DR, de Gouw J, Meinardi S (2012) Chemical data quantify Deepwater Horizon hydrocarbon flow rate and environmental distribution. Proc Natl Acad Sci U S A. 109(50):20246–20253
59. Satyanarayana T, Johri BN, Prakash A (2012) Microorganisms in environmental management. Springer, Microbes and Environment
60. Shannon CE, Weaver W, Blahut RE, Hajek B (1964) The mathematical theory of communication. University of Illinois press, Urbana
61. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504
62. Simpson EH (1949) Measurement of diversity. Nature 163(4148):688
63. Smith DM, Snow DE, Rees E, Zischkau AM, Hanson JD, Wolcott RD, Sun Y, White J, Kumar S, Dowd SE (2010) Evaluation of the bacterial diversity of pressure ulcers using bTEFAP pyrosequencing. BMC Med Genom 3:41–54
64. Sundarakrishnan B, Pushpanathan M, Jayashree S, Rajendhran J, Sakthivel N, Jayachandran S, Gunasekaran P (2012) Assessment of microbial richness in pelagic sediment of Andaman sea by bacterial tag encoded FLX titanium amplicon pyrosequencing (bTEFAP). Indian J Microbiol 52(4):544–550
65. Teramoto M, Ohuchi M, Hatmanti A, Darmayati Y, Widyastuti Y, Harayama S, Fukunaga Y (2011) Oleibacter marinus gen. nov., sp. nov., a bacterium that degrades petroleum aliphatic hydrocarbons in a tropical marine environment. Int J Syst Evol Microbiol 61:375–380
66. Vila J, Maria Nieto J, 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(2):349–362
67. Volkman JK, Revill AT (2002) Oil pollution and microbial regulation. In: Sabljic A (ed) Environmental and Ecological Chemistry, vol II, UNESCO-EoLSS, Paris, France, pp 1–9
68. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007a) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267
69. Wang YN, Cai H, Chi CQ, Lu AH, Lin XG, Jiang ZF, Wu XL (2007b) Halomonas shengliensis sp. nov., a moderately halophilic, denitrifying, crude-oil-utilizing bacterium. Int J Syst Evol Microbiol 57 (Pt 6):1222–1226
70. Wang LY, Gao CX, Mbadinga SM, Zhou L, Liu JF, Gu JD, Mu BZ (2011) Characterization of an alkane-degrading methanogenic enrichment culture from production water of an oil reservoir after 274 days of incubation. Int Biodeter Biodegr 65(3):444–450
71. Whitehead A, Dubansky B, Bodinier C, Garcia TI, Miles S, Pilley C, Raghunathan V, Roach JL, Walker N, Walter RB (2012) Genomic and physiological footprint of the Deepwater Horizon oil spill on resident marsh fishes. Proc Natl Acad Sci U S A. 109(50):20298–20302
72. Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18(3):257–266
73. Yanez-Arancibia A, Day JW (2004) The Gulf of Mexico: towards an integration of coastal management with large marine ecosystem management. Ocean Coast Manage 47(11–12):537–563
74. Zhang DC, Liu HC, Xin YH, Zhou YG, Schinner F, Margesin R (2010) Dyadobacter psychrophilus sp nov., a psychrophilic bacterium isolated from soil. Int J Syst Evol Microbiol 60:1640–1643