Cite this paper:
LI Xiaohong, YOU Cai, QU Liang, ZHOU Bin, TANG Xuexi, XIAO Hui. Bacterial communities fluctuate in abundance and diversity under simulated oil-contaminated seawater conditions[J]. HaiyangYuHuZhao, 2019, 37(2): 615-627

Bacterial communities fluctuate in abundance and diversity under simulated oil-contaminated seawater conditions

LI Xiaohong1,2, YOU Cai3, QU Liang4, ZHOU Bin1,2, TANG Xuexi1,2, XIAO Hui1,2
1 College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China;
2 Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China;
3 Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
4 CNOOC Limited, Tianjin Branch, Tianjin 300459, China
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.
Key words:    petroleum pollution|bacterial community|bacterial growth|amplified ribosomal DNA restriction analysis (ARDRA)   
Received: 2018-03-03   Revised: 2018-05-11
PDF (720 KB) Free
Print this page
Add to favorites
Email this article to others
Articles by LI Xiaohong
Articles by YOU Cai
Articles by QU Liang
Articles by ZHOU Bin
Articles by TANG Xuexi
Articles by XIAO Hui
Acosta-González A, Martirani-von Abercron S M, Rosselló-Móra R, Wittich R M, Marqués S. 2015. The effect 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.
Bælum 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, Lødeng 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 oilpolluted 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. PLoS 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. Effects 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, Schäfer 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 different 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.
Lladó S, Gràcia E, Solanas A M, Viñas 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. A comparison 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, Bælum J, Kimbrel J, Bouskill N J, Prestat E, Borglin S, Joyner D C, 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 Röling 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.
Ruan Y J, Deng Y L, Guo X S, Timmons M B, Lu H F, Han Z Y, 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.
Scopa A, Salzano G, Scrano L, Bufo S A, Bonomo M G. 2006. Preliminary assessment of microbial community recovery after an accidental oil spill by molecular analysis.Fresenius Environmental Bulletin, 7(1):675-681.
Sun Y J, Lu S D, Zhao X H, Ding A Z, Wang L. 2017. Longterm oil pollution and in situ microbial response of groundwater in Northwest China. Archives of Environmental Contamination and Toxicology, 72(4):519-529.
Varjani S J, Srivastava V K. 2015. Green technology and sustainable development of environment. Renewable Research Journal, 3(1):244-249.
Viggor S, Juhanson J, Jõesaar M, Mitt M, Truu J, Vedler E, Heinaru A. 2013. Dynamic changes in the structure of microbial communities in Baltic Sea coastal seawater microcosms modified by crude oil, shale oil or diesel fuel.Microbiological Research, 168(7):415-427.
Wrenn B A, Venosa A D. 1996. Selective enumeration of aromatic and aliphatic hydrocarbon degrading bacteria by a most-probable-number procedure. Canadian Journal of Microbiology, 42(3):252-258.
Wu M L, Ye X Q, Chen K L, Li W, Yuan J, Jiang X. 2017. Bacterial community shift and hydrocarbon transformation during bioremediation of short-term petroleumcontaminated soil. Environmental Pollution, 223:657-664.
Xiao H, Zhang Y, Zhang Z, Zhu L, You C, Tang X X. 2009. A preliminary study on the bacterial diversity in surface sediments from the coastal water of Qingdao and Weihai in summer and winter. Periodical of Ocean University of China, 39(4):641-646. (in Chinese with English abstract)
Xu H S, Yang X S, Li Y. 1999. Diagnosis and Control of Bacterial Diseases in Penaeid Shrimp Hatcheries. China Ocean Press, Beijing, China. p.55-101. (in Chinese)
Yakimov M, Timmis K N, Golyshin P N. 2007. Obligate oildegrading marine bacteria. Current Opinion in Biotechnology, 18(3):257-266.
Zanaroli G, Di Toro S, Todaro D, Varese G C, Bertolotto A, Fava F. 2010.Characterization of two diesel fuel degrading microbial consortia enriched from a non acclimated, complex source of microorganisms. Microbial Cell Factories, 9:10.
Zhou H Y, Wang H, Huang Y, Fang T T. 2016. Characterization of pyrene degradation by halophilic Thalassospira sp.strain tsl5-1 isolated from the coastal soil of Yellow Sea, China. International Biodeterioration & Biodegradation, 107:62-69.
Zrafi-Nouira I, Guermazi S, Chouari R, Safi N M D, Pelletier E, Bakhrouf A, Saidane-Mosbahi D, Sghir A. 2009. Molecular diversity analysis and bacterial population dynamics of an adapted seawater microbiota during the degradation of Tunisian zarzatine oil. Biodegradation, 20(4):467-486.