Bacterial communities fluctuate in abundance and diversity under simulated oil-contaminated seawater conditions
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摘要
Marine bacteria have recently been identified as a potent solution for petroleum hydrocarbon degradation in response to hazardous oceanic oil spills. In this study, a mesocosm experiment simulating a petroleum spill event was performed to investigate changes in the abundance, structure, and productivity of bacterial communities in response to oil pollution. Cultured heterotrophic bacteria and total bacteria showed a consistent trend involving an immediate decrease in abundance, followed by a slight increase, and a steady low-level thereafter. However, the changing trend of bacterial productivity based on bacterial biomass and bacterial volume showed the opposite trend. In addition, the density of oil-degrading bacteria increased initially, then subsequently declined. The change in the bacterial community structure at day 0 and day 28 were also analyzed by amplified ribosomal DNA restriction analysis(ARDRA), which indicated that the species diversity of the bacterial community changed greatly after oil pollution. Alphaproteobacteria(40.98%)replaced Epsilonproteobacteria(51.10%) as the most abundant class, and Gammaproteobacteria(38.80%)became the second most dominant class in the whole bacterial community. The bacterial communities in oil-contaminated seawater(32 genera) became much more complex than those found in the natural seawater sample(16 genera). The proportion of petroleum-degrading bacteria in the oil-contaminated seawater also increased. In this study, culture-dependent and culture-independent approaches were combined to elucidate changes in both bacterial productivity and community structure. These findings will contribute to a better understanding of the role that bacteria play in material cycling and degradation in response to oil pollution.
Marine bacteria have recently been identified as a potent solution for petroleum hydrocarbon degradation in response to hazardous oceanic oil spills. In this study, a mesocosm experiment simulating a petroleum spill event was performed to investigate changes in the abundance, structure, and productivity of bacterial communities in response to oil pollution. Cultured heterotrophic bacteria and total bacteria showed a consistent trend involving an immediate decrease in abundance, followed by a slight increase, and a steady low-level thereafter. However, the changing trend of bacterial productivity based on bacterial biomass and bacterial volume showed the opposite trend. In addition, the density of oil-degrading bacteria increased initially, then subsequently declined. The change in the bacterial community structure at day 0 and day 28 were also analyzed by amplified ribosomal DNA restriction analysis(ARDRA), which indicated that the species diversity of the bacterial community changed greatly after oil pollution. Alphaproteobacteria(40.98%)replaced Epsilonproteobacteria(51.10%) as the most abundant class, and Gammaproteobacteria(38.80%)became the second most dominant class in the whole bacterial community. The bacterial communities in oil-contaminated seawater(32 genera) became much more complex than those found in the natural seawater sample(16 genera). The proportion of petroleum-degrading bacteria in the oil-contaminated seawater also increased. In this study, culture-dependent and culture-independent approaches were combined to elucidate changes in both bacterial productivity and community structure. These findings will contribute to a better understanding of the role that bacteria play in material cycling and degradation in response to oil pollution.
Marine bacteria have recently been identified as a potent solution for petroleum hydrocarbon degradation in response to hazardous oceanic oil spills. In this study, a mesocosm experiment simulating a petroleum spill event was performed to investigate changes in the abundance, structure, and productivity of bacterial communities in response to oil pollution. Cultured heterotrophic bacteria and total bacteria showed a consistent trend involving an immediate decrease in abundance, followed by a slight increase, and a steady low-level thereafter. However, the changing trend of bacterial productivity based on bacterial biomass and bacterial volume showed the opposite trend. In addition, the density of oil-degrading bacteria increased initially, then subsequently declined. The change in the bacterial community structure at day 0 and day 28 were also analyzed by amplified ribosomal DNA restriction analysis(ARDRA), which indicated that the species diversity of the bacterial community changed greatly after oil pollution. Alphaproteobacteria(40.98%)replaced Epsilonproteobacteria(51.10%) as the most abundant class, and Gammaproteobacteria(38.80%)became the second most dominant class in the whole bacterial community. The bacterial communities in oil-contaminated seawater(32 genera) became much more complex than those found in the natural seawater sample(16 genera). The proportion of petroleum-degrading bacteria in the oil-contaminated seawater also increased. In this study, culture-dependent and culture-independent approaches were combined to elucidate changes in both bacterial productivity and community structure. These findings will contribute to a better understanding of the role that bacteria play in material cycling and degradation in response to oil pollution.
引文
Acosta-González A,Martirani-von Abercron S M,Rosselló-Móra R,Wittich R M,Marqués S.2015.The ef fect of oil spills on the bacterial diversity and catabolic function in coastal sediments:a case study on the Prestige oil spill.Environmental Science and Pollution Research,22(20):15 200-15 214.
Amann R I,Ludwig W,Schleifer K H.1995.Phylogenetic identification and in situ detection of individual microbial cells without cultivation.Microbiological Reviews,59(1):143-169.
Atlas R M.1981.Microbial degradation of petroleum hydrocarbons:an environmental perspective.Microbiological Reviews,45(1):180-209.
Atlas R M.1991.Microbial hydrocarbon degradationbioremediation of oil spills.Journal of Chemical Technology and Biotechnology,52(2):149-156.
B?lum J S,Borglin S,Chakraborty R,Fortney J L,Lamendella R,Mason O U,Auer M,Zemla M,Bill M,Conrad M E,Malfatti S A,Tringe S G,Holman H Y,Hazen T C,Jansson J K.2012.Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill.Environmental Microbiology,14(9):2 405-2 416.
Bai J,Cui A L,Lv Y H.2007.The degradation capability of crude oil degrading strains and the impacting factors.Transactions of Oceanology and Limnology,(3):41-48.(in Chinese with English abstract)
Brakstad O G,L?deng A G G.2005.Microbial diversity during biodegradation of crude oil in seawater from the North Sea.Microbial Ecology,49(1):94-103.
Brambilla E,Hippe H,Hagelstein A,Tindall B J,Stackebrandt E.2001.16S rDNA diversity of cultured and uncultured prokaryotes of a mat sample from Lake Fryxell,McMurdo Dry Valleys,Antarctica.Extremophiles,5(1):23-33.
Brussaard C P D,Peperzak L,Witte Y,Huisman J.2010.An experimental oil spill at sea.In:Timmis K N ed.Handbook of Hydrocarbon and Lipid Microbiology.Springer,Berlin,Heidelberg.p.3 491-3 502.
Cappello S,Caruso G,Zampino D,Monticelli L S,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.Journal of Applied Microbiology,102(1):184-194.
Chronopoulou P,Sanni G O,Silas‐Olu D I,Meer J R,Timmis K N,Brussaard C P D,McGenity T J.2015.Generalist hydrocarbon‐degrading bacterial communities in the oil‐polluted water column of the North Sea.Microbial Biotechnology,8(3):434-447.
Collado L,Figueras M J.2011.Taxonomy,epidemiology,and clinical relevance of the genus Arcobacter.Clinical Microbiology Reviews,24(1):174-192.
de la Cueva S C,Rodríguez C H,Cruz N O S,Contreras J A R,Miranda J L.2016.Changes in bacterial populations during bioremediation of soil contaminated with petroleum hydrocarbons.Water,Air,&Soil Pollution,227:91.
Ding G C,Heuer H,Smalla K.2012.Dynamics of bacterial communities in two unpolluted soils after spiking with phenanthrene:soil type specific and common responders.Frontiers in Microbiology,3:290.
Dong C,Bai X,Sheng H,Jiao L,Zhou H,Shao Z.2015.Distribution of pahs and the pah-degrading bacteria in the deep-sea sediments of the high-latitude arctic ocean.Biogeosciences,12(7):2 163-2 177.
dos Santos H F,Cury J C,do Carmo F L,dos Santos A L,Tiedje J,van Elsas J D,Rosado A S,Peixoto R S.2011.Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing:bacterial proxies for oil pollution.P L o S One,6(3):e16943.
Elshahed M S,Senko J M,Najar F Z,Kenton S M,Roe B A,Dewers T A,Spear J R,Krumholz L R.2003.Bacterial diversity and sulfur cycling in a mesophilic sulfide-rich spring.Applied and Environmental Microbiology,69(9):5 609-5 621.
Fuhrman J A,Azam F.1980.Bacterioplankton secondary production estimates for coastal waters of British Columbia,Antarctica,and California.Applied and Environmental Microbiology,39(6):1 085-1 095.
Good I J.1953.The population frequencies of species and the estimation of population parameters.Biometrika,40(3-4):237-264.
Gutierrez T,Nichols P D,Whitman W B,Aitken M D.2012.Porticoccus hydrocarbonoclasticus sp.nov.,an aromatic hydrocarbon-degrading bacterium identified in laboratory cultures of marine phytoplankton.Applied and Environmental Microbiology,78(3):628-637.
Hassanshahian M,Yakimov M M,Denaro R,Genovese M,Cappello S.2014.Using real-time PCR to assess changes in the crude oil degrading microbial community in contaminated seawater mesocosms.International Biodeterioration&Biodegradation,93:241-248.
Jean J S,Lee M K,Wang S M,Chattopadhyay P,Maity J P.2008.Ef fects of inorganic nutrient levels on the biodegradation of benzene,toluene,and xylene(BTX)by Pseudomonas spp.in a laboratory porous media sand aquifer model.Bioresource Technology,99(16):7 807-7 815.
Jiang H C,Liu A Y,Ren L H,Song X K,Jiang X Y,Liu L J.2014.PCR-RFLP analysis of bacteria 16S rDNA in Laizhou Bay.Transactions of Oceanology and Limnology,(3):127-134.(in Chinese with English abstract)
Jiao S,Liu Z S,Lin Y B,Yang J,Chen W M,Wei G H.2016.Bacterial communities in oil contaminated soils:biogeography and co-occurrence patterns.Soil Biology and Biochemistry,98:64-73.
Kalyuzhnaya M G,Bowerman S,Lara J C,Lidstrom M E,Chistoserdova L.2006.Methylotenera mobilis gen.nov.,sp.nov.,an obligately methylamine-utilizing bacterium within the family Methylophilaceae.International Journal of Systematic and Evolutionary Microbiology,56(12):2 819-2 823.
Lebaron P,Servais P,Troussellier M,Courties C,Muyzer G,Bernard L,Sch?fer H,Pukall R,Stackebrandt E,Guindulain T,Vives-Rego J.2001.Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms:changes in abundances,activity and composition.FEMS Microbiology Ecology,34(3):255-266.
Li P P,Chen X C,Zhang Y R,Zhang X J,Mei G M,Guo Y M.2014.Purification and structural elucidation of exoploysaccharide from a new marine bacterium lentibacter algarum zxm100t.Chinese Journal of Biotechnology,30(3):455-463.(in Chinese with English abstract)
Li Y,Zhou H X,Liu J L,Zhang Y F,Chen J X,Zhang X H.2006.Distribution and identification of marine heterotrophic bacteria in dif ferent sea areas close to the shore of Qingdao.Periodical of Ocean University of China,36(6):965-970.(in Chinese with English abstract)
Liao J Q,Wang J,Jiang D L,Wang M C,Huang Y.2015.Longterm oil contamination causes similar changes in microbial communities of two distinct soils.Applied Microbiology and Biotechnology,99(23):10 299-10 310.
Liu Z F,Liu J Q.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.
LladóS,Gràcia E,Solanas A M,Vi?as M.2013.Fungal and bacterial microbial community assessment during bioremediation assays in an aged creosote-polluted soil.Soil Biology and Biochemistry,67:114-123.
Long S C,Aelion C M,Dobbins D C,Pfaender F K.1995.Acomparison of microbial community characteristics among petroleum-contaminated and uncontaminated subsurface soil samples.Microbial Ecology,30(3):297-307.
Maruyama A,Ishiwata H,Kitamura K,Sunamura M,Fujita T,Matsuo M,Hiqashihara T.2003.Dynamics of microbial populations and strong selection for Cycloclasticus pugetii following the Nakhodka oil spill.Microbial Ecology,46(4):442-453.
Mason O U,Scott N M,Gonzalez A,Robbinspianka A,B?lum J,Kimbrel J,Bouskill N J,Prestat E,Borglin S,Joyner DC,Fortney J L,Jurelevicius D,Stringfellow W T,AlvarezCohen L,Hazen T C,Knight R,Gilbert J A,Jansson J K.2014.Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill.The ISME Journal,8(7):1 464-1 475.
Meckenstock R U,Boll M,Mouttaki H,Koelschbach J S,Tarouco P C,Weyrauch P,Dong X Y,Himmelberg A M.2016.Anaerobic degradation of benzene and polycyclic aromatic hydrocarbons.Journal of Molecular Microbiology and Biotechnology,26(1-3):92-118.
Mishamandani S,Gutierrez T,Berry D,Aitken M D.2016.Response of the bacterial community associated with a cosmopolitan marine diatom to crude oil shows a preference for the biodegradation of aromatic hydrocarbons.Environmental Microbiology,18(6):1 817-1 833.
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Nishimura M,Yoshida A,Toyoda K,Yamada M,Nomura H,Wada M,Okamoto K,Shibata A,Takada H,Ohwada K.2006.Mesocosm experiment on the succession of microbial community in response to oil contamination to coastal seawater.La Mer,44(2):59-65.
Nogi Y,Yoshizumi M,Miyazaki M.2014.Thalassospira povalilytica sp.nov.,a polyvinyl-alcohol-degrading marine bacterium.International Journal of Systematic and Evolutionary Microbiology,64(4):1 149-1 153.
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Piehler M F,Maloney J S,Paerl H W.2002.Bacterioplanktonic abundance,productivity and petroleum hydrocarbon biodegradation in marinas and other coastal waters in North Carolina,USA.Marine Environmental Research,54(2):157-168.
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Ruan Y J,Deng Y L,Guo X S,Timmons M B,Lu H F,Han ZY,Ye Z Y,Shi M M,Zhu S M.2016.Simultaneous ammonia and nitrate removal in an airlift reactor using poly(butylene succinate)as carbon source and biofilm carrier.Bioresource Technology,216:1 004-1 013.
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Atlas R M.1981.Microbial degradation of petroleum hydrocarbons:an environmental perspective.Microbiological Reviews,45(1):180-209.
Atlas R M.1991.Microbial hydrocarbon degradationbioremediation of oil spills.Journal of Chemical Technology and Biotechnology,52(2):149-156.
B?lum J S,Borglin S,Chakraborty R,Fortney J L,Lamendella R,Mason O U,Auer M,Zemla M,Bill M,Conrad M E,Malfatti S A,Tringe S G,Holman H Y,Hazen T C,Jansson J K.2012.Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill.Environmental Microbiology,14(9):2 405-2 416.
Bai J,Cui A L,Lv Y H.2007.The degradation capability of crude oil degrading strains and the impacting factors.Transactions of Oceanology and Limnology,(3):41-48.(in Chinese with English abstract)
Brakstad O G,L?deng A G G.2005.Microbial diversity during biodegradation of crude oil in seawater from the North Sea.Microbial Ecology,49(1):94-103.
Brambilla E,Hippe H,Hagelstein A,Tindall B J,Stackebrandt E.2001.16S rDNA diversity of cultured and uncultured prokaryotes of a mat sample from Lake Fryxell,McMurdo Dry Valleys,Antarctica.Extremophiles,5(1):23-33.
Brussaard C P D,Peperzak L,Witte Y,Huisman J.2010.An experimental oil spill at sea.In:Timmis K N ed.Handbook of Hydrocarbon and Lipid Microbiology.Springer,Berlin,Heidelberg.p.3 491-3 502.
Cappello S,Caruso G,Zampino D,Monticelli L S,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.Journal of Applied Microbiology,102(1):184-194.
Chronopoulou P,Sanni G O,Silas‐Olu D I,Meer J R,Timmis K N,Brussaard C P D,McGenity T J.2015.Generalist hydrocarbon‐degrading bacterial communities in the oil‐polluted water column of the North Sea.Microbial Biotechnology,8(3):434-447.
Collado L,Figueras M J.2011.Taxonomy,epidemiology,and clinical relevance of the genus Arcobacter.Clinical Microbiology Reviews,24(1):174-192.
de la Cueva S C,Rodríguez C H,Cruz N O S,Contreras J A R,Miranda J L.2016.Changes in bacterial populations during bioremediation of soil contaminated with petroleum hydrocarbons.Water,Air,&Soil Pollution,227:91.
Ding G C,Heuer H,Smalla K.2012.Dynamics of bacterial communities in two unpolluted soils after spiking with phenanthrene:soil type specific and common responders.Frontiers in Microbiology,3:290.
Dong C,Bai X,Sheng H,Jiao L,Zhou H,Shao Z.2015.Distribution of pahs and the pah-degrading bacteria in the deep-sea sediments of the high-latitude arctic ocean.Biogeosciences,12(7):2 163-2 177.
dos Santos H F,Cury J C,do Carmo F L,dos Santos A L,Tiedje J,van Elsas J D,Rosado A S,Peixoto R S.2011.Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing:bacterial proxies for oil pollution.P L o S One,6(3):e16943.
Elshahed M S,Senko J M,Najar F Z,Kenton S M,Roe B A,Dewers T A,Spear J R,Krumholz L R.2003.Bacterial diversity and sulfur cycling in a mesophilic sulfide-rich spring.Applied and Environmental Microbiology,69(9):5 609-5 621.
Fuhrman J A,Azam F.1980.Bacterioplankton secondary production estimates for coastal waters of British Columbia,Antarctica,and California.Applied and Environmental Microbiology,39(6):1 085-1 095.
Good I J.1953.The population frequencies of species and the estimation of population parameters.Biometrika,40(3-4):237-264.
Gutierrez T,Nichols P D,Whitman W B,Aitken M D.2012.Porticoccus hydrocarbonoclasticus sp.nov.,an aromatic hydrocarbon-degrading bacterium identified in laboratory cultures of marine phytoplankton.Applied and Environmental Microbiology,78(3):628-637.
Hassanshahian M,Yakimov M M,Denaro R,Genovese M,Cappello S.2014.Using real-time PCR to assess changes in the crude oil degrading microbial community in contaminated seawater mesocosms.International Biodeterioration&Biodegradation,93:241-248.
Jean J S,Lee M K,Wang S M,Chattopadhyay P,Maity J P.2008.Ef fects of inorganic nutrient levels on the biodegradation of benzene,toluene,and xylene(BTX)by Pseudomonas spp.in a laboratory porous media sand aquifer model.Bioresource Technology,99(16):7 807-7 815.
Jiang H C,Liu A Y,Ren L H,Song X K,Jiang X Y,Liu L J.2014.PCR-RFLP analysis of bacteria 16S rDNA in Laizhou Bay.Transactions of Oceanology and Limnology,(3):127-134.(in Chinese with English abstract)
Jiao S,Liu Z S,Lin Y B,Yang J,Chen W M,Wei G H.2016.Bacterial communities in oil contaminated soils:biogeography and co-occurrence patterns.Soil Biology and Biochemistry,98:64-73.
Kalyuzhnaya M G,Bowerman S,Lara J C,Lidstrom M E,Chistoserdova L.2006.Methylotenera mobilis gen.nov.,sp.nov.,an obligately methylamine-utilizing bacterium within the family Methylophilaceae.International Journal of Systematic and Evolutionary Microbiology,56(12):2 819-2 823.
Lebaron P,Servais P,Troussellier M,Courties C,Muyzer G,Bernard L,Sch?fer H,Pukall R,Stackebrandt E,Guindulain T,Vives-Rego J.2001.Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms:changes in abundances,activity and composition.FEMS Microbiology Ecology,34(3):255-266.
Li P P,Chen X C,Zhang Y R,Zhang X J,Mei G M,Guo Y M.2014.Purification and structural elucidation of exoploysaccharide from a new marine bacterium lentibacter algarum zxm100t.Chinese Journal of Biotechnology,30(3):455-463.(in Chinese with English abstract)
Li Y,Zhou H X,Liu J L,Zhang Y F,Chen J X,Zhang X H.2006.Distribution and identification of marine heterotrophic bacteria in dif ferent sea areas close to the shore of Qingdao.Periodical of Ocean University of China,36(6):965-970.(in Chinese with English abstract)
Liao J Q,Wang J,Jiang D L,Wang M C,Huang Y.2015.Longterm oil contamination causes similar changes in microbial communities of two distinct soils.Applied Microbiology and Biotechnology,99(23):10 299-10 310.
Liu Z F,Liu J Q.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.
LladóS,Gràcia E,Solanas A M,Vi?as M.2013.Fungal and bacterial microbial community assessment during bioremediation assays in an aged creosote-polluted soil.Soil Biology and Biochemistry,67:114-123.
Long S C,Aelion C M,Dobbins D C,Pfaender F K.1995.Acomparison of microbial community characteristics among petroleum-contaminated and uncontaminated subsurface soil samples.Microbial Ecology,30(3):297-307.
Maruyama A,Ishiwata H,Kitamura K,Sunamura M,Fujita T,Matsuo M,Hiqashihara T.2003.Dynamics of microbial populations and strong selection for Cycloclasticus pugetii following the Nakhodka oil spill.Microbial Ecology,46(4):442-453.
Mason O U,Scott N M,Gonzalez A,Robbinspianka A,B?lum J,Kimbrel J,Bouskill N J,Prestat E,Borglin S,Joyner DC,Fortney J L,Jurelevicius D,Stringfellow W T,AlvarezCohen L,Hazen T C,Knight R,Gilbert J A,Jansson J K.2014.Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill.The ISME Journal,8(7):1 464-1 475.
Meckenstock R U,Boll M,Mouttaki H,Koelschbach J S,Tarouco P C,Weyrauch P,Dong X Y,Himmelberg A M.2016.Anaerobic degradation of benzene and polycyclic aromatic hydrocarbons.Journal of Molecular Microbiology and Biotechnology,26(1-3):92-118.
Mishamandani S,Gutierrez T,Berry D,Aitken M D.2016.Response of the bacterial community associated with a cosmopolitan marine diatom to crude oil shows a preference for the biodegradation of aromatic hydrocarbons.Environmental Microbiology,18(6):1 817-1 833.
Montagna P A,Bauer J E,Toal J,Hardin D,Spies R B.1987.Temporal variability and the relationship between benthic meiofaunal and microbial populations of a natural coastal petroleum seep.Journal of Marine Research,45(3):761-789.
Nishimura M,Yoshida A,Toyoda K,Yamada M,Nomura H,Wada M,Okamoto K,Shibata A,Takada H,Ohwada K.2006.Mesocosm experiment on the succession of microbial community in response to oil contamination to coastal seawater.La Mer,44(2):59-65.
Nogi Y,Yoshizumi M,Miyazaki M.2014.Thalassospira povalilytica sp.nov.,a polyvinyl-alcohol-degrading marine bacterium.International Journal of Systematic and Evolutionary Microbiology,64(4):1 149-1 153.
Osborn A M,Moore E R,Timmis K N.2000.An evaluation of terminal-restriction fragment length polymorphism(T-RFLP)analysis for the study of microbial community structure and dynamics.Environmental Microbiology,2(1):39-50.
Piehler M F,Maloney J S,Paerl H W.2002.Bacterioplanktonic abundance,productivity and petroleum hydrocarbon biodegradation in marinas and other coastal waters in North Carolina,USA.Marine Environmental Research,54(2):157-168.
Porter K G,Feig Y S.1980.The use of DAPI for identifying and counting aquatic microflora1.Limnology and Oceanography,25(5):943-948.
Prince R C,Gramain A,Mcgenity T J.2010.Prokaryotic hydrocarbon degraders.In:Timmis K N ed.Handbook of Hydrocarbon and Lipid Microbiology.Springer Berlin Heidelberg.
Prince R C.2015.Introduction:mesocosms and microcosms.In:McGenity T,Timmis K,Nogales B eds.Hydrocarbon and Lipid Microbiology Protocols.Springer Protocols Handbooks.Springer,Berlin,Heidelberg
R?ling W F M,Milner M G,Jones D M,Lee K,Daniel F,Swannell R J P,Head I M.2002.Robust hydrocarbon degradation and dynamics of bacterial communities during nutrient-enhanced oil spill bioremediation.Applied and Environmental Microbiology,68(11):5 537-5 548.
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