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

  • Chan Zhang
  • Wei-Jia ZhangEmail author
  • Qunjian Yin
  • Xuegong Li
  • Xiaoqing Qi
  • Long-Fei Wu


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.


deep-sea bacteria high hydrostatic pressure (HHP) trimethylamine N-oxide (TMAO) community structure 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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): 1 216–226, CrossRefGoogle Scholar
  2. Barrett, E L, Kwan, H S. 1985. Bacterial reduction of trimethylamine oxide. Annual Review of Microbiology, 39: 131–149, CrossRefGoogle Scholar
  3. 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, Scholar
  4. Boden, R. 2012. Emended description of the genus Methylophaga Janvier et al. 1985. International Journal of Systematic and Evolutionary Microbiology, 62 (7). 1644–1646, Scholar
  5. 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, Scholar
  6. 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, Scholar
  7. 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, Scholar
  8. 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, Scholar
  9. 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, Scholar
  10. 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): 5 814–823, Scholar
  11. 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): 6 298–305, Scholar
  12. 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, Scholar
  13. 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, Scholar
  14. 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, Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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, Scholar
  17. 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 o. 11, 000 meters. Applied and Environmental Microbiology, 64 (4): 1 510–1 513.Google Scholar
  18. 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): 6 220–229, Scholar
  19. 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): 2 096–101, Scholar
  20. 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.Google Scholar
  21. 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, Scholar
  22. 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): 3 378–387, Scholar
  23. 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, Scholar
  24. Lidbury, I, Murrell, J C, Chen, Y. 2014. Trimethylamine N-oxide Proceedings of the National Academy of Sciences of the United States of America, 111 (7): 2 710–715, Scholar
  25. 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: 050, Scholar
  26. Marietou, A, Bartlett, D H. 2014. Effects of high hydrostatic pressure on coastal bacterial community abundance and diversity. Applied and Environmental Microbiology, 80 (19): 5 992–003, Scholar
  27. 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, Scholar
  28. Montzka, S A, Dlugokencky, E J, Butler, J H. 2011. Non-CO2 greenhouse gases and climate change. Nature, 476 (7358): 43–50, Scholar
  29. 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): 3 668–675, Scholar
  30. Oger, P M, Jebbar, M. 2010. The many ways of coping with pressure. Research in Microbiology, 161 (10): 799–809, Scholar
  31. 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, Scholar
  32. 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, Scholar
  33. 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, Scholar
  34. 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, Scholar
  35. Raymond, J A, Plopper, G E. 2002. A bacterial TMAO transporter. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology, 133 (1): 29–34, Scholar
  36. 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, Scholar
  37. 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, Scholar
  38. 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, Scholar
  39. 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, Scholar
  40. 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): 1 459–461, Scholar
  41. 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): 2 216–222, Scholar
  42. 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, Scholar
  43. 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, Scholar
  44. 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): 1 214–222, Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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): 4 461–465, Scholar
  47. 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): 5 212–215, Scholar
  48. 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. Scholar
  49. 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): 1 613–617, Scholar
  50. 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, Scholar
  51. 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). 1192–1202, Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Chan Zhang
    • 1
    • 2
    • 3
    • 4
  • Wei-Jia Zhang
    • 1
    • 3
    • 4
    Email author
  • Qunjian Yin
    • 1
    • 2
    • 3
    • 4
  • Xuegong Li
    • 1
    • 3
    • 4
  • Xiaoqing Qi
    • 1
    • 3
    • 4
  • Long-Fei Wu
    • 3
    • 4
    • 5
  1. 1.Laboratory of Deep Sea Microbial Cell Biology, Institute of Deep-sea Science and EngineeringChinese Academy of SciencesSanyaChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.International Associated Laboratory of Evolution and Development of Magnetotactic Multicellular OrganismsCNRS-MarseilleMarseilleFrance
  4. 4.CAS-SanyaSanyaChina
  5. 5.Aix Marseille Univ, CNRS, LCBMarseilleFrance

Personalised recommendations