Cite this paper:
ZHANG Chan, ZHANG Wei-jia, YIN Qunjian, LI Xuegong, QI Xiaoqing, WU Long-fei. Distinct influence of trimethylamine N-oxide and high hydrostatic pressure on community structure and culturable deep-sea bacteria[J]. HaiyangYuHuZhao, 2020, 38(2): 364-377

Distinct influence of trimethylamine N-oxide and high hydrostatic pressure on community structure and culturable deep-sea bacteria

ZHANG Chan1,2,3, ZHANG Wei-jia1,3, YIN Qunjian1,2,3, LI Xuegong1,3, QI Xiaoqing1,3, WU Long-fei3,4
1 Laboratory of Deep Sea Microbial Cell Biology, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China;
3 International Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, CNRS-Marseille/CAS-Sanya, China;
4 Aix Marseille Univ, CNRS, LCB, Marseille F-13402, France
Trimethylamine N-oxide (TMAO) is one of the most important nutrients for bacteria in the deep-sea environment and is capable of improving pressure tolerance of certain bacterial strains. To assess the impact of TMAO on marine microorganisms, especially those dwelling in the deep-sea environment, we analyzed the bacterial community structure of deep-sea sediments after incubated under different conditions. Enrichments at 50 MPa and 0.1 MPa revealed that TMAO imposed a greater influence on bacterial diversity and community composition at atmospheric pressure condition than that under high hydrostatic pressure (HHP). We found that pressure was the primary factor that determines the bacterial community. Meanwhile, in total, 238 bacterial strains were isolated from the enrichments, including 112 strains affiliated to 16 genera of 4 phyla from the Yap Trench and 126 strains affiliated to 11 genera of 2 phyla from the Mariana Trench. Treatment of HHP reduced both abundance and diversity of isolates, while the presence of TMAO mainly affected the diversity of isolates obtained. In addition, certain genera were isolated only when TMAO was supplemented. Taken together, we demonstrated that pressure primarily defines the bacterial community and culturable bacterial isolates. Furthermore, we showed for the first time that TMAO had distinct influences on bacterial community depending on the pressure condition. The results enriched the understanding of the significance of TMAO in bacterial adaptation to the deep-sea environment.
Key words:    deep-sea bacteria|high hydrostatic pressure (HHP)|trimethylamine N-oxide (TMAO)|community structure   
Received: 2019-03-21   Revised: 2019-04-30
PDF (1762 KB) Free
Print this page
Add to favorites
Email this article to others
Articles by ZHANG Chan
Articles by ZHANG Wei-jia
Articles by YIN Qunjian
Articles by LI Xuegong
Articles by QI Xiaoqing
Articles by WU Long-fei
Aono E, Baba T, Ara T, Nishi T, Nakamichi T, Inamoto E, Toyonaga H, Hasegawa M, Takai Y, Okumura Y, Baba M, Tomita M, Kato C, Oshima T, Nakasone K, Mori H. 2010. Complete genome sequence and comparative analysis of Shewanella violacea, a psychrophilic and piezophilic bacterium from deep sea floor sediments. Molecular Biosystems, 6(7):1 216-1 226,
Barrett E L, Kwan H S. 1985. Bacterial reduction of trimethylamine oxide. Annual Review of Microbiology, 39:131-149,
Bartlett D H. 2002. Pressure effects on in vivo microbial processes. Biochimica et Biophysica Acta (BBA)-Protein Structure and Molecular Enzymology, 1595(1-2):367-381,
Boden R. 2012. Emended description of the genus Methylophaga Janvier et al. 1985. International Journal of Systematic and Evolutionary Microbiology, 62(7):1 644-1 646,
Campanaro S, Treu L, Valle G. 2008. Protein evolution in deep sea bacteria:an analysis of amino acids substitution rates.BMC Evolutionary Biology, 8:313,
Chikuma S, Kasahara R, Kato C, Tamegai H. 2007. Bacterial adaptation to high pressure:a respiratory system in the deep-sea bacterium Shewanella violacea DSS12. FEMS Microbiology Letters, 267(1):108-112,
Dinasquet J, Tiirola M, Azam F. 2018. Enrichment of bacterioplankton able to utilize one-carbon and methylated compounds in the coastal Pacific Ocean. Frontiers in Marine Science, 5:307,
Doronina N V, Darmaeva T D, Trotsenko Y A. 2003.Methylophaga alcalica sp. nov., a novel alkaliphilic and moderately halophilic, obligately methylotrophic bacterium from an East Mongolian saline soda lake.International Journal of Systematic and Evolutionary Microbiology, 53:223-229,
Dos Santos J P, Iobbi-Nivol C, Couillault C, Giordano G, Méjean V. 1998. Molecular analysis of the trimethylamine N-oxide (TMAO) reductase respiratory system from a Shewanella species. Journal of Molecular Biology, 284(2):421-433,
Dunn A K, Stabb E V. 2008. Genetic analysis of trimethylamine N-oxide reductases in the light organ symbiont Vibrio fischeri ES114. Journal of Bacteriology, 190(17):5 814-5 823,
Eloe E A, Lauro F M, Vogel R F, Bartlett D H. 2008. The deepsea bacterium Photobacterium profundum SS9 utilizes separate flagellar systems for swimming and swarming under high-pressure conditions. Applied and Environmental Microbiology, 74(20):6 298-6 305,
Follonier S, Escapa I F, Fonseca P M, Henes B, Panke S, Zinn M, Prieto M A. 2013. New insights on the reorganization of gene transcription in Pseudomonas putida KT2440 at elevated pressure. Microbial Cell Factories, 12:30,
Gaboyer F, Vandenabeele-Trambouze O, Cao J W, Ciobanu M C, Jebbar M, Le Romancer M, Alain K. 2014.Physiological features of Halomonas lionensis sp. nov., a novel bacterium isolated from a Mediterranean Sea sediment. Research in Microbiology, 165(7):490-500,
Gibb S W, Hatton A D. 2004. The occurrence and distribution of trimethylamine-N-oxide in Antarctic coastal waters.Marine Chemistry, 91(1-4):65-75,
Gillett M B, Suko J R, Santoso F O, Yancey P H. 1997.Elevated levels of trimethylamine oxide in muscles of deep-sea gadiform teleosts:a high-pressure adaptation? Journal of Experimental Zoology, 279(4):386-391,<386::Aid-Jez8>3.0.Co;2-K.
He H L, Chen X L, Zhang X Y, Sun C Y, Zou B C, Zhang Y Z. 2009. Novel use for the osmolyte trimethylamine N-oxide:retaining the psychrophilic characters of cold-adapted protease deseasin MCP-01 and simultaneously improving its thermostability. Marine Biotechnology, 11(6):710-716,
Kato C, Li L N, Nogi Y, Nakamura Y, Tamaoka J, Horikoshi K. 1998. Extremely barophilic bacteria isolated from the Mariana Trench, Challenger Deep, at a depth of 11, 000 meters. Applied and Environmental Microbiology, 64(4):1 510-1 513.
Kaye J Z, Baross J A. 2004. Synchronous effects of temperature, hydrostatic pressure, and salinity on growth, phospholipid profiles, and protein patterns of four Halomonas species isolated from deep-sea hydrothermal-vent and sea surface environments. Applied and Environmental Microbiology, 70(10):6 220-6 229,
Kim H G, Doronina N V, Trotsenko Y A, Kim S W. 2007.Methylophaga aminisulfidivorans sp. nov., a restricted facultatively methylotrophic marine bacterium. International Journal of Systematic and Evolutionary Microbiology, 57(9):2 096-2 101,
King G M. 1984. Metabolism of trimethylamine, choline, and glycine betaine by sulfate-reducing and methanogenic bacteria in marine sediments. Applied and Environmental Microbiology, 48(4):719-725.
Kusube M, Kyaw T S, Tanikawa K, Chastain R A, Hardy K M, Cameron J, Bartlett D H. 2017. Colwellia marinimaniae sp. nov., a hyperpiezophilic species isolated from an amphipod within the Challenger Deep, Mariana Trench. International Journal of Systematic and Evolutionary Microbiology, 67(4):824-831,
Li C Y, Chen X L, Shao X, Wei T D, Wang P, Xie B B, Qin Q L, Zhang X Y, Su H N, Song X Y, Shi M, Zhou B C, Zhang Y Z. 2015. Mechanistic insight into trimethylamine N-oxide recognition by the marine bacterium Ruegeria pomeroyi DSS-3. Journal of Bacteriology, 197(21):3 378-3 387,
Lidbury I D E A, Murrell J C, Chen Y. 2015. Trimethylamine and trimethylamine N-oxide are supplementary energy sources for a marine heterotrophic bacterium:implications for marine carbon and nitrogen cycling. ISME Journal, 9(3):760-769,
Lidbury I, Murrell J C, Chen Y. 2014. Trimethylamine N-oxide metabolism by abundant marine heterotrophic bacteria. Proceedings of the National Academy of Sciences of the United States of America, 111(7):2 710-2 715,
Marietou A, Chastain R, Beulig F, Scoma A, Hazen T C, Bartlett D H. 2018. The effect of hydrostatic pressure on enrichments of hydrocarbon degrading microbes from the Gulf of Mexico following the deepwater horizon oil spill.Frontiers in Microbiology, 9:1 050,
Marietou, A, Bartlett D H. 2014. Effects of high hydrostatic pressure on coastal bacterial community abundance and diversity. Applied and Environmental Microbiology, 80(19):5 992-6 003,
Marino D, Andrio E, Danchin E G J, Oger E, Gucciardo S, Lambert A, Puppo A, Pauly N. 2011. A Medicago truncatula NADPH oxidase is involved in symbiotic nodule functioning. New Phytologist, 189(2):580-592,
Montzka S A, Dlugokencky E J, Butler J H. 2011. Non-CO2 greenhouse gases and climate change. Nature, 476(7358):43-50,
Nogi Y, Abe M, Kawagucci S, Hirayama H. 2014. Psychrobium conchae gen. nov., sp. nov., a psychrophilic marine bacterium isolated from the iheya North hydrothermal field. International Journal of Systematic and Evolutionary Microbiology, 64(11):3 668-3 675,
Oger P M, Jebbar M. 2010. The many ways of coping with pressure. Research in Microbiology, 161(10):799-809,
Peoples L M, Donaldson S, Osuntokun O, Xia Q, Nelson A, Blanton J, Allen E E, Church M J, Bartlett D H. 2018.Vertically distinct microbial communities in the Mariana and Kermadec trenches. PLoS One, 13(4):e0195102,
Peoples L M, Grammatopoulou E, Pombrol M, Xu X X, Osuntokun O, Blanton J, Allen E E, Nunnally C C, Drazen J C, Mayor D J, Bartlett D H. 2019. Microbial community diversity within sediments from two geographically separated hadal trenches. Frontiers in Microbiology, 10:347,
Petrov E, Rohde P R, Cornell B, Martinac B. 2012. The protective effect of osmoprotectant TMAO on bacterial mechanosensitive channels of small conductance MscS/MscK under high hydrostatic pressure. Channels, 6(4):262-271,
Qin Q L, Li Y, Zhang Y J, Zhou Z M, Zhang W X, Chen X L, Zhang X Y, Zhou B C, Wang L, Zhang Y Z. 2011.Comparative genomics reveals a deep-sea sedimentadapted life style of Pseudoalteromonas sp. SM9913. The ISME Journal, 5(2):274-284,
Raymond J A, Plopper G E. 2002. A bacterial TMAO transporter. Comparative Biochemistry and Physiology B:Biochemistry and Molecular Biology, 133(1):29-34,
Saad-Nehme J, Silva J L, Meyer-Fernandes J R. 2001.Osmolytes protect mitochondrial F0F1-ATPase complex against pressure inactivation. Biochimica et Biophysica Acta (BBA)-Protein Structure and Molecular Enzymology, 1546(1):164-170,
Tamegai H, Li L N, Masui N, Kato C. 1997. A denitrifying bacterium from the deep sea at 11 000-m depth.Extremophiles, 1(4):207-211,
Tarn J, Peoples L M, Hardy K, Cameron J, Bartlett D H. 2016.Identification of free-living and particle-associated microbial communities present in hadal regions of the Mariana Trench. Frontiers in Microbiology, 7:665,
Tindall B J, Rosselló-Móra R, Busse H J, Ludwig W, Kämpfer P. 2010. Notes on the characterization of prokaryote strains for taxonomic purposes. International Journal of Systematic and Evolutionary Microbiology, 60(1):249-266,
Vezzi A, Campanaro S, D'Angelo M, Simonato F, Vitulo N, Lauro F M, Cestaro A, Malacrida G, Simionati B, Cannata N, Romualdi C, Bartlett D H, Valle G. 2005. Life at depth:Photobacterium profundum genome sequence and expression analysis. Science, 307(5714):1 459-1 461,
Villeneuve C, Martineau C, Mauffrey F, Villemur R. 2013.Methylophaga nitratireducenticrescens sp. nov.Methylophaga frappieri sp. nov., isolated from the biofilm of the methanol-fed denitrification system treating the seawater at the Montreal Biodome. International Journal of Systematic and Evolutionary Microbiology, 63(6):2 216-2 222,
Wang F P, Wang J B, Jian H H, Zhang B, Li S K, Wang F, Zeng X W, Gao L, Bartlett D H, Yu J, Hu S N, Xiao X. 2008.Environmental adaptation:Genomic analysis of the piezotolerant and psychrotolerant deep-sea iron reducing bacterium Shewanella piezotolerans WP3. Journal of Biotechnology, 3(4):e1937,
Wannicke N, Frindte K, Gust G, Liskow I, Wacker A, Meyer A, Grossart H P. 2015. Measuring bacterial activity and community composition at high hydrostatic pressure using a novel experimental approach:a pilot study. FEMS Microbiology Ecology, 91(5):fiv036,
Yancey P H, Clark M E, Hand S C, Bowlus R D, Somero G N. 1982. Living with water-stress-evolution of osmolyte systems. Science, 217(4566):1 214-1 222,
Yancey P H, Fyfe-Johnson A L, Kelly R H, Walker V P, Auñón M T. 2001. Trimethylamine oxide counteracts effects of hydrostatic pressure on proteins of deep-sea teleosts.Journal of Experimental Zoology, 289(3):172-176,<172::Aid-Jez3>3.0.Co;2-J.
Yancey P H, Gerringer M E, Drazen J C, Rowden A A, Jamieson A. 2014. Marine fish may be biochemically constrained from inhabiting the deepest ocean depths.Proceedings of the National Academy of Sciences of the United States of America, 111(12):4 461-4 465,
Yayanos A A, Dietz A S, Van Boxtel R. 1981. Obligately barophilic bacterium from the Mariana Trench.Proceedings of the National Academy of Sciences of the United States of America-Biological Sciences, 78(8):5 212-5 215,
Yin Q J, Zhang W J, Qi X Q, Zhang S D, Jiang T, Li X G, Chen Y, Santini C L, Zhou H, Chou I M, Wu L F. 2018. High hydrostatic pressure inducible trimethylamine N-oxide reductase improves the pressure tolerance of piezosensitive bacteria Vibrio fluvialis. Frontiers in Microbiology, 8:2646,
Yoon S H, Ha S M, Kwon S, Lim J, Kim Y, Seo H, Chun J. 2017. Introducing EzBioCloud:a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. International Journal of Systematic and Evolutionary Microbiology, 67(5):1 613-1 617,
Zhang S D, Santini C L, Zhang W J, Barbe V, Mangenot S, Guyomar C, Garel M, Chen H T, Li X G, Yin Q J, Zhao Y, Armengaud J, Gaillard J C, Martini S, Pradel N, Vidaud C, Alberto F, Médigue C, Tamburini C, Wu L F. 2016.Genomic and physiological analysis reveals versatile metabolic capacity of deep-sea Photobacterium phosphoreum ANT-2200. Extremophiles, 20(3):301-310,
Zou Q, Bennion B J, Daggett V, Murphy K P. 2002. The molecular mechanism of stabilization of proteins by TMAO and its ability to counteract the effects of urea.Journal of the American Chemical Society, 124(7):1 192-1 202,