Dynamics and distribution of bacterial and archaeal communities in oil-contaminated temperate coastal mudflat mesocosms

Environmental Science and Pollution Research

Volumn 22, Issue 20, 2015, Pages 15230-15247

  Sanni, Gbemisola O ^a   Coulon, Frédéric ^b   McGenity, Terry J ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b CRANFIELD UNIVERSITY   (United Kingdom)

Author keywords

454 Pyrosequencing; Archaeal communities; Biodegradation; Hydrocarbon degrading bacteria; Mudflats; Oil pollution; T RFLP

Indexed keywords

BACTERIUM; BIODEGRADATION; BIOFILM; COASTAL SEDIMENT; DIATOM; FINE GRAINED SEDIMENT; GENETIC ANALYSIS; MESOCOSM; MICROBIAL COMMUNITY; MUDFLAT; OIL POLLUTION; PETROLEUM HYDROCARBON;

ALCANIVORAX; ARCHAEA; BACILLARIOPHYTA; BACTERIA (MICROORGANISMS); CHROMATIALES; CYCLOCLASTICUS; ROSEOBACTER; THALASSOLITUUS;

ARCHAEAL RNA; BACTERIAL RNA; HYDROCARBON; PETROLEUM; RNA 16S; WATER POLLUTANT;

ARCHAEON; BACTERIUM; BIOFILM; BIOREMEDIATION; DIATOM; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; OIL SPILL; SEDIMENT; WATER POLLUTANT;

ARCHAEA; BACTERIA; BIODEGRADATION, ENVIRONMENTAL; BIOFILMS; DIATOMS; GEOLOGIC SEDIMENTS; HYDROCARBONS; PETROLEUM; PETROLEUM POLLUTION; RNA, ARCHAEAL; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; WATER POLLUTANTS, CHEMICAL;

EID: 84945152141     PISSN: 09441344     EISSN: 16147499     Source Type: Journal    
DOI: 10.1007/s11356-015-4313-1     Document Type: Article

References (79)

1. Abed RMM (2010) Interaction between cyanobacteria and aerobic heterotrophic bacteria in the degradation of hydrocarbons. Int Biodeter Biodegr 64:58–64
2. Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684
3. An D, Brown D, Chatterjee I, Dong X, Ramos-Padron E, Wilson S, Bordenave S, Caffrey SM, Gieg LM, Sensen CW, Voordouw G (2013) Microbial community and potential functional gene diversity involved in anaerobic hydrocarbon degradation and methanogenesis in an oil sands tailings pond. Genome 56:612–618
4. Anderson MS, Hall RA, Griffin M (1980) Microbial metabolism of alicyclic hydrocarbons: cyclohexane catabolism by a pure strain of Pseudomonas sp. J Gen Microbiol 120:89–94
5. Berardesco G, Dyhrman S, Gallagher E, Shiaris MP (1998) Spatial and temporal variation of phenanthrene-degrading bacteria in intertidal sediments. Appl Environ Microbiol 64:2560–2565
6. Bernhard AE, Landry ZC, Blevins A, de la Torré JR, Giblin AE et al (2010) Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl Environ Microbiol 76:1285–1289
7. 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 73:6089–6097
8. Brakstad OG, Lodeng AG (2005) Microbial diversity during biodegradation of crude oil in seawater from the North Sea. Microb Ecol 49:94–103
9. Capello S, Yakimov MM (2010) Alcanivorax. In: Timmis KN, McGenity TJ, van der Meer JR, de Lorenzo V (eds) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 1738–1748
10. Chronopoulou P-M, Sanni GO, Silas-Olu DI, Van der Meer JR, Timmis KN, Brussaard CPD, McGenity TJ (2014) Generalist hydrocarbon-degrading bacterial communities in the oil-polluted water column of the North Sea. Microb Biotechnol. doi:10.1111/1751-791512176
11. Chronoupolou P-M, Fahy A, Coulon F, Paissé S, Goñi-Urriza MS, Peperzak L, Acuña-Alvarez L, McKew BA, Lawson T, Timmis KN, Duran R, Underwood GJC, McGenity TJ (2013) Impact of a simulated oil spill on benthic phototrophs and nitrogen-fixing bacteria. Environ Microbiol 15:241–252
12. Coulon F, McKew BA, Osborn AM, McGenity TJ, Timmis KN (2007) Effects of temperature and biostimulation on oil-degrading microbial communities in temperate estuarine waters. Environ Microbiol 9:177–186
13. Coulon F, Chronopoulou P, Fahy A, Païssé S, Goñi-Urriza M, Peperzak L, Acuña-Alvarez L, McKew BA, Brussaard CPD, Underwood GJC, Van der Meer JR, Timmis KN, Duran R, McGenity TJ (2012) Central role of dynamic tidal biofilms dominated by aerobic hydrocarbonoclastic bacteria and diatoms in the biodegradation of hydrocarbons in coastal mudflats. Appl Environ Microbiol 78:3638–3648
14. Cui Z, Lai Q, Dong C, Shao Z (2008) Biodiversity of polycyclic aromatic hydrocarbon-degrading bacteria from deep sea sediments of the Middle Atlantic Ridge. Environ Microbiol 10:2138–2149
15. Deppe U, Richnow HH, Michaelis W, Antranikian G (2005) Degradation of crude oil by an arctic microbial consortium. Extremophiles 9:461–470
16. Dyksterhouse SE, Gray JP, Herwig RP, Lara JC, Staley JT (1995) Cycloclasticus pugetii gen nov, sp nov, an aromatic hydrocarbon-degrading bacterium from marine sediments. Int J Syst Evol Microbiol 45:116–123
17. Fahy A, McGenity TJ, Timmis KN, Ball AS (2006) Heterogeneous aerobic benzene-degrading communities in oxygen-depleted groundwaters. FEMS Microbiol Ecol 58:260–270
18. Felsenstein J (2009) PHYLIP (Phytogeny Inference Package) version 3.69. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
19. Fish SA, Shepherd TJ, McGenity TJ, Grant WD (2002) Recovery of 16S ribosomal RNA gene fragments from ancient halite. Nature 417:432–436
20. Fleeger JW, Carman KR, Nisbet RM (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317:207–233
21. Foster KR, Bell T (2012) Competition, not cooperation, dominates interactions among culturable microbial species. Curr Biol 22:1845–1850
22. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9–17
23. Harwati TU, Kasai Y, Kodama Y, Susilaningsih D, Watanabe K (2007) Characterization of diverse hydrocarbon-degrading bacteria isolated from Indonesian seawater. Microbes Environ 22:412–415
24. Head IM, Jones DM, Rőling WF (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4:173–182
25. Hug LA, Castelle CJ, Wrighton KC, Thomas BC, Sharon I, Frischkorn KR, Williams KH, Tringe SG, Banfield JF (2013) Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome 1:22–38
26. Kasai Y, Kishira H, Sasaki T, Syutsubo K, Watanabe K, Harayama S (2002a) Predominant growth of Alcanivorax strains in oil-contaminated and nutrient-supplemented sea water. Environ Microbiol 4:141–147
27. Kasai Y, Kishira H, Harayama S (2002b) Bacteria belonging to the genus Cycloclasticus play a primary role in the degradation of aromatic hydrocarbons released in a marine environment. Appl Environ Microbiol 68:5625–5633
28. Kodama Y, Stiknowati LI, Ueki A, Ueki K, Watanabe K (2008) Thalassospira tepidiphila sp nov, a polycyclic aromatic hydrocarbon-degrading bacterium isolated from seawater. Int J Syst Evol Microbiol 58:711–715
29. 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 77:7962–7974
30. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175
31. Lanfranconi MP, Bosch R, Nogales B (2010) Short-term changes in the composition of active marine bacterial assemblages in response to diesel oil pollution. Microb Biotechnol 3:607–621
32. Li M, Cao H, Hong Y, Gu JD (2011) Spatial distribution and abundances of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) in mangrove sediments. Appl Microbiol Biotechnol 89:1243–1254
33. Li Q, Wang F, Chen Z, Yin X, Xiao X (2012) Stratified active archaeal communities in the sediments of Jiulong River estuary China. Front Microbiol 3:311–314
34. Li J, Nedwell DB, Beddow J, Dumbrell AJ, McKew BA, Thorpe EL, Whitby C (2014) amoA gene abundances and nitrification potential rates suggest that benthic ammonia-oxidizing bacteria (AOB) not archaea (AOA) dominate N cycling in the Colne estuary, UK. Appl Environ Microbiol. doi:10.1128/AEM.02654-14
35. 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 2:492–504
36. Liu R, Zhang Y, Ding R, Li D, Gao Y, Yang M (2009) Comparison of archaeal and bacterial community structures in heavily oil-contaminated and pristine soils. J Biosci Bioeng 108:400–407
37. Lloyd K, Schreiber GL, Petersen DG, Kjeldsen KU, Lever MA, Steen AD, Stepanauskas R, Richter M, Kleindienst S, Lenk S, Schramm A, Jørgensen BB (2013) Predominant archaea in marine sediments degrade detrital proteins. Nature 496:215–220
38. Lopez GR, Levinton JS (1978) The availability of microorganisms attached to sediment particles as food for Hydrobia ventrosa Montagu (Gastropoda: Prosobranchia). Oecologia 32:263–275
39. Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Dymock D, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799
40. McGenity TJ (2014) Hydrocarbon biodegradation in intertidal wetland sediments. Curr Opin Biotechnol 27:46–54
41. McGenity TJ, Folwell BD, McKew BA, Sanni GO (2012) Marine crude-oil biodegradation: a central role for interspecies interactions. Aquat Biosyst 8:10–28
42. McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ (2007a) Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ Microbiol 9:165–176
43. McKew BA, Coulon F, Yakimov MM, Denaro R, Genovese M, Smith CJ, Osborn AM, Timmis KN, McGenity TJ (2007b) Efficacy of intervention strategies for bioremediation of crude oil in marine systems and effects on indigenous hydrocarbonoclastic Bacteria. Environ Microbiol 9:1562–1571
44. McKew BA, Taylor JD, McGenity TJ, Underwood GJC (2011) Resistance and resilience of benthic biofilm communities from a temperate saltmarsh to desiccation and rewetting. ISME J 5:30–41
45. Meng J, Xu J, Qin D, He Y, Xiao X, Wang F (2014) Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses. ISME J 8:650–659
46. Michel J, Owens EH, Zengel S, Graham A, Nixon Z, Allard T, Holton W, Reimer PD, Lamarche A, White M, Rutherford N, Childs C, Mauseth G, Challenger G, Taylor E (2013) Extent and degree of shoreline oiling: Deepwater Horizon oil spill, Gulf of Mexico. USA PLoS ONE 8:e65087
47. Miralles G, Nerini D, Mante C, Acquaviva M, Doumenq P, Michotey V, Nazaret S, Bertrand JC, Cuny P (2007) Effects of spilled oil on bacterial communities of Mediterranean coastal anoxic sediments chronically subjected to oil hydrocarbon contamination. Microb Ecol 54:646–661
48. Mortazavi B, Horel A, Beazley MJ, Sobecky PA (2013) Intrinsic rates of petroleum hydrocarbon biodegradation in Gulf of Mexico intertidal sandy sediments and its enhancement by organic substrates. J Hazard Mater 244–245:537–544
49. Munson MA, Nedwell DB, Embley TM (1997) Phylogenetic diversity of Archaea in sediment samples from a coastal salt marsh. Appl Environ Microbiol 63:4729–4733
50. 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
51. Nogales B, Aguilo-Ferretjans MM, Martin-Cardona C, Lalucat J, Bosch R (2007) Bacterial diversity, composition and dynamics in and around recreational coastal areas. Environ Microbiol 9:1913–1929
52. Païssé S, Goni-Urriza M, Coulon F, Duran R (2010) How a bacterial community originating from a contaminated coastal sediment responds to an oil input. Microb Ecol 60:394–405
53. 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 59:342–355
54. Prince RC (2010) Eukaryotic hydrocarbon degraders. In: Timmis KN, McGenity TJ, van der Meer JR, de Lorenzo V (eds) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 2066–2076
55. Prince RC, Lessard RR, Clark JR (2003) Bioremediation of marine oil spills. Oil Gas Sci Technol 58:463–468
56. Purdy KJ, Cresswell-Maynard TD, Nedwell DB, McGenity TJ, Grant WD, Timmis KN, Embley TM (2004) Isolation of haloarchaea that grow at low salinities. Environ Microbiol 6:591–595
57. Reddy CM, Eglinton TI, Hounshell A, White HK, Xu L, Gaines RB, Frysinger GS (2002) The West Falmouth oil spill after thirty years: the persistence of petroleum hydrocarbons in marsh sediments. Environ Sci Technol 36:4754–4760
58. Rőling WF, De Brito Couto IR, Swannell RP, Head IM (2004) Response of archaeal communities in beach sediments to spilled oil and bioremediation. Appl Environ Microbiol 70:2614–2620
59. Scott NM, Hess M, Bouskill NJ, Mason OU, Jansson JK, Gilbert JA (2014) The microbial nitrogen cycling potential is impacted by polyaromatic hydrocarbon pollution of marine sediments. Front Microbiol 5:108–115
60. Sekiguchi Y, Yamada T, Hanada S, Ohashi A, Harada H, Kamagata Y (2003) Anaerolinea thermophila gen nov, sp nov and Caldilinea aerophila gen nov, sp nov, novel filamentous thermophiles that represent a previously uncultured lineage of the domain Bacteria at the subphylum level. Int J Syst Evol Microbiol 53:1843–1851
61. Seyler LM, McGuinness LM, Kerkhof LJ (2014) Crenarchaeal heterotrophy in salt marsh sediments. ISME J 8:1534–1543
62. Sherry A, Gray ND, Ditchfield AK, Aitken CM, Jones DM, Röling WFM, Hallmann C, Larter SR, Bowler BFJ, Head IM (2013) Anaerobic biodegradation of crude oil under sulphate-reducing conditions leads to only modest enrichment of recognized sulphate-reducing taxa. Int Biodeter Biodegr 81:105–113
63. Smith CJ, Danilowicz BS, Clear AK, Costello FJ, Wilson B, Meijer WG (2005) T-Align, a web-based tool for comparison of multiple terminal restriction fragment length polymorphism profiles. FEMS Microbiol Ecol 54:375–380
64. Stauffert M, Cravo-Laureau C, Jézéquel R, Barantal S, Cuny P, Gilbert F, Cagnon C, Militon C, Amouroux D, Mahdaoui F, Bouyssiere B, Stora G, Merlin FX, Duran R (2013) Impact of oil on bacterial community structure in bioturbated sediments. PLoS ONE 8:e65347
65. Stauffert M, Duran R, Gassie C, Cravo-Laureau C (2014) Response of archaeal communities to oil spill in bioturbated mudflat sediments. Microb Ecol 67:108–119
66. Sutton NB, Maphosa F, Morillo JA, Abu Al-Soud W, Langenhoff AA, Grotenhuis T, Rijnaarts HH, Smidt H (2013) Impact of long-term diesel contamination on soil microbial community structure. Appl Environ Microbiol 79:619–630
67. Taketani RG, Franco NO, Rosado AS, Van Elsas JD (2010) Microbial community response to a simulated hydrocarbon spill in mangrove sediments. J Microbiol 48:7–15
68. Teira E, Lekunberri I, Gasol JM, Nieto-Cid M, Alvarez-Salgado XA, Figueiras FG (2007) Dynamics of the hydrocarbon-degrading Cycloclasticus bacteria during mesocosm-simulated oil spills. Environ Microbiol 9:2551–2562
69. 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
70. 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
71. Teramoto M, Queck SY, Ohnishi K (2013) Specialized hydrocarbonoclastic bacteria prevailing in seawater around a port in the Strait of Malacca. PLoS ONE 8:e66594
72. Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Gurvan M (2011) Environmental and gut Bacteroidetes: the food connection. Front Microbiol 2:93–108
73. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
74. Thornton DCO, Dong LF, Underwood GJC, Nedwell DB (2002) Factors affecting microphytobenthic biomass, species composition and production in the Colne Estuary (UK). Aquat Microb Ecol 27:285–300
75. Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 67:503–549
76. Winderl C, Anneser B, Griebler C, Meckenstock RU, Lueders T (2008) Depth-resolved quantification of anaerobic toluene degraders and aquifer microbial community patterns in distinct redox zones of a tar oil contaminant plume. Appl Environ Microbiol 74:792–801
77. 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
78. Yamada T, Sekiguchi Y, Hanada S, Imachi H, Ohashi A, Harada H, Kamagata Y (2006) Anaerolinea thermolimosa sp nov, Levilinea saccharolytica gen nov, sp nov and Leptolinea tardivitalis gen nov, sp nov, novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov and Caldilineae classis nov in the bacterial phylum Chloroflexi. Int J Syst Evol Microbiol 56:1331–1340
79. Yang S, Wen X, Zhao L, Shi Y, Jin H (2014) Crude oil treatment leads to shift of bacterial communities in soils from the deep active layer and upper permafrost along the China-Russia Crude Oil Pipeline route. PLoS ONE 9:e96552