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

Volumn 5, Issue 4, 2015, Pages 379-392

  Koo, Hyunmin ^a   Mojib, Nazia ^a,c   Huang, Jonathan P ^a   Donahoe, Rona J ^b   Bej, Asim K ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA   (United States)

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

Author keywords

Biodegradative genes; Bioinformatics; Metagenomics; Oil spill; PCR; Pyrosequencing; QIIME

Indexed keywords

ALKANE HYDROXYLASE; BACTERIAL DNA; BACTERIAL ENZYME; BIPHENYL DIOXYGENASE; CANYON BLOCK 252 OIL; CATECHOL 2,3 DIOXYGENASE; NAPHTHALENE DIOXYGENASE; OIL; RNA 16S; SEA WATER; TOLUENE DIOXYGENASE; UNCLASSIFIED DRUG;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL GENE; BACTEROIDETES; BETAPROTEOBACTERIA; COASTAL WATERS; CONTROLLED STUDY; DELTAPROTEOBACTERIA; EPSILONPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GEOGRAPHIC DISTRIBUTION; GULF OF MEXICO; IN VITRO STUDY; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DEGRADATION; MICROBIAL DIVERSITY; MICROCOSM; NONHUMAN; OIL SPILL; OPERATIONAL TAXONOMIC UNIT; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PYROSEQUENCING; RNA 16S GENE; SEDIMENT; SEQUENCE ANALYSIS; UNITED STATES; X RAY DIFFRACTION;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); CHROMATIALES; CLOSTRIDIALES; DELTAPROTEOBACTERIA; EPSILONPROTEOBACTERIA; FIRMICUTES; GAMMAPROTEOBACTERIA; METHYLOCOCCALES; MOLLICUTES; OCEANOSPIRILLALES; PSEUDOMONADALES; RHODOBACTERALES; SYNTROPHOBACTERALES;

EID: 85015548427     PISSN: 2190572X     EISSN: 21905738     Source Type: Journal    
DOI: 10.1007/s13205-014-0233-x     Document Type: Article

References (88)

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. American Water Works Association (AWWA) (2012) Standard Methods for the Examination of Water and Wastewater, vol 22ed. Washington: American Public Health Association (APHA) 22 ed:1360
3. Arreguin-Sanchez F, Zetina-Rejon M, Manickchand-Heileman S, Ramirez-Rodriguez M, Vidal L (2004) Simulated response to harvesting strategies in an exploited ecosystem in the southwestern Gulf of Mexico. Ecol Model 172(2–4):421–432
4. 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
5. 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. Wiley, New York
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. PLoS One 7(7):e41305
8. Bordenave S, Goni-Urriza MS, Caumette P, Duran R (2007) Effects of heavy fuel oil on the bacterial community structure of a pristine microbial mat. Appl Environ Microbiol 73(19):6089–6097
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. Camilli R, Reddy CM, Yoerger DR, Van Mooy BA, Jakuba MV, Kinsey JC, McIntyre CP, Sylva SP, Maloney JV (2010) Tracking hydrocarbon plume transport and biodegradation at Deepwater Horizon. Science 330(6001):201–204
11. Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4(6):458–468
12. 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
13. 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. Mat Methods 7(5):335–336
14. Cappello S, Caruso G, Zampino D, Monticelli LS, Maimone G, Denaro R, Tripodo B, Troussellier M, Yakimov M, Giuliano L (2007) Microbial community dynamics during assays of harbour oil spill bioremediation: a microscale simulation study. J Appl Microbiol 102(1):184–194
15. 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
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. Devereux R, Hines M, Stahl D (1996) S cycling: characterization of natural communities of sulfate-reducing bacteria by 165 rRNA sequence comparisons. Microb Ecol 32(3):283–292
18. 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
19. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008a) 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
20. Dowd SE, Sun Y, Secor PR, Rhoads DD, Wolcott BM, James GA, Wolcott RD (2008b) Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol 8:43
21. Drever JI (1973) The preparation of oriented glay mineral specimens for X-ray diffraction analysis by a filter-membrane peel technique. Am Miner 58:553–554
22. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461
23. Elshahed MS, Senko JM, Najar FZ, Kenton SM, Roe BA, Dewers TA, Spear JR, Krumholz LR (2003) Bacterial diversity and sulfur cycling in a mesophilic sulfide-rich spring. Appl Environ Microbiol 69(9):5609–5621
24. Engle VD (2011) Estimating the provision of ecosystem services by Gulf of Mexico coastal wetlands. Wetlands 31(1):179–193
25. Evans FF, Rosado AS, Sebastian GV, Casella R, Machado PL, Holmstrom 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
26. Glória Pereira M, Mudge SM, Latchford J (2002) Consequences of linseed oil spills in salt marsh sediments. Mar Pollut Bull 44(6):520–533
27. Grabowski A, Nercessian O, Fayolle F, Blanchet D, Jeanthon C (2005) Microbial diversity in production waters of a low-temperature biodegraded oil reservoir. FEMS Microbiol Ecol 54(3):427–443
28. Gupta RS (2006) Molecular signatures (unique proteins and conserved indels) that are specific for the epsilon proteobacteria (Campylobacterales). BMC Genom 7:167
29. 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
30. 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
31. Head IM, Jones DM, Röling WF (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4(3):173–182
32. 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
33. Hemalatha S, Veeramanikandan P (2011) Characterization of aromatic hydrocarbon rading bacteria from petroleum contaminated sites. J Environ Prot 2:243
34. 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
35. Herrmann S, Kleinsteuber S, Chatzinotas A, Kuppardt S, Lueders T, Richnow HH, Vogt C (2010) Functional characterization of an anaerobic benzene-degrading enrichment culture by DNA stable isotope probing. Environ Microbiol 12(2):401–411
36. Howarth RW (1984) The ecological significance of sulfur in the energy dynamics of salt marsh and coastal marine sediments. Biogeochemistry 1(1):5–27
37. Hubert CR, Oldenburg TB, Fustic M, Gray ND, Larter SR, Penn K, Rowan AK, Seshadri R, Sherry A, Swainsbury R, Voordouw G, Voordouw JK, Head IM (2012) Massive dominance of Epsilonproteobacteria in formation waters from a Canadian oil sands reservoir containing severely biodegraded oil. Environ Microbiol 14(2):387–404
38. Hughes JB, Hellmann JJ (2005) The application of rarefaction techniques to molecular inventories of microbial diversity. Methods Enzymol 397:292–308
39. Kim JN, Kim BS, Kim SJ, Cerniglia CE (2012) Effects of crude oil, dispersant, and oil dispersant mixtures on human fecal microbiota in an in vitro culture system. MBio 3(5):e00376-12
40. 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
41. Klepac-Ceraj V, Bahr M, Crump BC, Teske AP, Hobbie JE, Polz MF (2004) High overall diversity and dominance of microdiverse relationships in salt marsh sulphate-reducing bacteria. Environ Microbiol 6(7):686–698
42. Kok M, Oldenhuis R, Van Der Linden M, Raatjes P, Kingma J, van Lelyveld PH, Witholt B (1989) The Pseudomonas oleovorans alkane hydroxylase gene. Sequence and expression. J Biol Chem 264(10):5435–5441
43. 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
44. 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
45. Kurkela S, Lehvaslaiho H, Palva ET, Teeri TH (1988) Cloning, nucleotide sequence and characterization of genes encoding naphthalene dioxygenase of Pseudomonas putida strain NCIB9816. Gene 73(2):355–362
46. Kvenvolden KA, Cooper CK (2003) Natural seepage of crude oil into the marine environment. Geo-Mar Lett 23(3–4):140–146
47. 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
48. Laramee L, Lawrence JR, Greer CW (2000) Molecular analysis and development of 16S rRNA oligonucleotide probes to characterize a diclofop-methyl-degrading biofilm consortium. Can J Microbiol 46(2):133–142
49. 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
50. 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
51. 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. Microbiologyopen 2(3):492–504
52. 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
53. 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
54. Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73(5):1576–1585
55. 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
56. Mesarch MB, Nakatsu CH, Nies L (2000) Development of catechol 2,3-dioxygenase-specific primers for monitoring bioremediation by competitive quantitative PCR. Appl Environ Microbiol 66(2):678–683
57. Mitsch WJ, Gosselink JG (2000) The value of wetlands: importance of scale and landscape setting. Ecol Econ 35(1):25–33
58. 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
59. Nakai C, Kagamiyama H, Nozaki M, Nakazawa T, Inouye S, Ebina Y, Nakazawa A (1983) Complete nucleotide sequence of the metapyrocatechase gene on the TOI plasmid of Pseudomonas putida mt-2. J Biol Chem 258(5):2923–2928
60. National Health Environmental Effects Research Laboratory (US) Gulf Ecology Division (1999) The ecological condition of estuaries in the Gulf of Mexico, vol 98. US Environmental Protection Agency, Office of Research and Development, The Office, Gulf Breeze, Fla. vol 4
61. 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
62. Pavlova A, Papazova D (2003) Oil-spill identification by gas chromatography–mass spectrometry. J Chromatogr Sci 41(5):271–273
63. Phelps CD, Kerkhof LJ, Young LY (1998) Molecular characterization of a sulfate-reducing consortium which mineralizes benzene. FEMS Microbiol Ecol 27(3):269–279
64. Phillips CJ, Paul EA, Prosser JI (2000) Quantitative analysis of ammonia oxidising bacteria using competitive PCR. FEMS Microbiol Ecol 32(2):167–175
65. Pomeroy LR (1974) The ocean’s food web, a changing paradigm. Bioscience 24(9):499–504
66. 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. PloS One 7(6):e38571
67. Prabagaran SR, Manorama R, Delille D, Shivaji S (2007) Predominance of Roseobacter, Sulfitobacter, Glaciecola and Psychrobacter in seawater collected off Ushuaia, Argentina, Sub-Antarctica. FEMS Microbiol Ecol 59(2):342–355
68. Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26(7):1641–1650
69. Ratajczak A, Geissdorfer W, Hillen W (1998) Alkane hydroxylase from Acinetobacter sp. strain ADP1 is encoded by alkM and belongs to a new family of bacterial integral-membrane hydrocarbon hydroxylases. Appl Environ Microbiol 64(4):1175–1179
70. Redmond MC, Valentine DL (2012) Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill. Proc Natl Acad Sci USA 109(50):20292–20297
71. 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, pp 105
72. 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
73. Roling WF, Milner MG, Jones DM, Fratepietro F, Swannell RP, Daniel F, Head IM (2004) Bacterial community dynamics and hydrocarbon degradation during a field-scale evaluation of bioremediation on a mudflat beach contaminated with buried oil. Appl Environ Microbiol 70(5):2603–2613
74. Sette LD, Simioni KC, Vasconcellos SP, Dussan LJ, Neto EV, Oliveira VM (2007) Analysis of the composition of bacterial communities in oil reservoirs from a southern offshore Brazilian basin. Antonie Van Leeuwenhoek 91(3):253–266
75. Shannon CE, Weaver W, Blahut RE, Hajek B (1964) The mathematical theory of communication. University of Illinois press, Urbana
76. 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
77. Silliman BR, van de Koppel J, McCoy MW, Diller J, Kasozi GN, Earl K, Adams PN, Zimmerman AR (2012) Degradation and resilience in Louisiana salt marshes after the BP-Deepwater Horizon oil spill. Proc Natl Acad Sci USA 109(28):11234–11239
78. Simpson EH (1949) Measurement of diversity. Nature 163(4148):688
79. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103(32):12115–12120
80. 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
81. Teal JM (1986) The ecology of regularly flooded salt marshes of New England: a community profile. Biological Report, vol 85. Woods Hole Oceanographic Institution, USA
82. van Beilen JB, Wubbolts MG, Witholt B (1994) Genetics of alkane oxidation by Pseudomonas oleovorans. Biodegradation 5(3–4):161–174
83. van Beilen JB, Smits TH, Whyte LG, Schorcht S, Rothlisberger M, Plaggemeier T, Engesser KH, Witholt B (2002) Alkane hydroxylase homologues in gram-positive strains. Environ Microbiol 4(11):676–682
84. 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(16):5261–5267
85. Whyte LG, Hawari J, Zhou E, Bourbonniere L, Inniss WE, Greer CW (1998) Biodegradation of variable-chain-length alkanes at low temperatures by a psychrotrophic Rhodococcus sp. Appl Environ Microbiol 64(7):2578–2584
86. Wirsen CO, Sievert SM, Cavanaugh CM, Molyneaux SJ, Ahmad A, Taylor LT, DeLong EF, Taylor CD (2002) Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur. Appl Environ Microbiol 68(1):316–325
87. Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18(3):257–266
88. Yanez-Arancibia A, Day JW (2004) The Gulf of Mexico: towards an integration of coastal management with large marine ecosystem management. Ocean Coast Manag 47(11–12):537–563