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Contribution of trimethylamine N-oxide on the growth and pressure tolerance of deep-sea bacteria

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Abstract

Trimethylamine N-oxide (TMAO) is widely dispersed in marine environments and plays an important role in the biogeochemical cycle of nitrogen. Diverse marine bacteria utilize TMAO as carbon and nitrogen sources or as electron acceptor in anaerobic respiration. Alteration of respiratory component according to the pressure is a common trait of deep-sea bacteria. Deep-sea bacteria from different genera harbor high hydrostatic pressure (HHP) inducible TMAO reductases that are assumed to be constitutively expressed in the deep-sea piezosphere and facilitating quick reaction to TMAO released from fish which is a potential nutrient for bacterial growth. However, whether deep-sea bacteria universally employ this strategy remains unknown. In this study, 237 bacterial strains affiliated to 23 genera of Proteobacteria, Bacteroidetes, Firmicutes and Actinobacteria were isolated from seawater, sediment or amphipods collected at different depths. The pressure tolerance and the utilization of TMAO were examined in 74 strains. The results demonstrated no apparent correlation between the depth where the bacteria inhabit and their pressure tolerance, regarding to our samples. Several deep-sea strains from the genera of Alteromonas, Halomonas, Marinobacter, Photobacterium, and Vibrio showed capacity of TMAO utilization, but none of the isolated Acinebacter, Bacillus, Brevundimonas, Muricauda, Novosphingobium, Rheinheimera, Sphingobium and Stenotrophomonas did, indicating the utilization of TMAO is a species-specific feature. Furthermore, we noticed that the ability of TMAO utilization varied among strains of the same species. TMAO has greater impact on the growth of deep-sea isolates of Vibrio neocaledonicus than shallow-water isolates. Taken together, the results describe for the first time the TMAO utilization in deep-sea bacterial strains, and expand our understanding of the physiological characteristic of marine bacteria.

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Acknowledgement

We thank Dr. HE Lisheng for sharing the South China Sea samples, Prof. Zhang Xiaohua for Vibrio fluvialis type strain ATCC33809.

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Authors and Affiliations

  1. Laboratory of Deep-sea Microbial Cell Biology, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya, 572000, China

    Qunjian Yin, Weijia Zhang, Xuegong Li, Lihong Zhou, Xiaoqing Qi & Chan Zhang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Qunjian Yin & Chan Zhang

  3. International Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, CNRS-Marseille/CAS-Beijing-Qingdao-Sanya, China

    Qunjian Yin, Weijia Zhang, Xuegong Li, Lihong Zhou, Xiaoqing Qi & Long-Fei Wu

  4. CAS Key Laboratory for Experimental Study under Deep-sea Extreme Conditions, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya, 572000, China

    Weijia Zhang, Xuegong Li, Lihong Zhou & Xiaoqing Qi

  5. AMU, LCB UMR 7283, CNRS-Marseille, 143402, France

    Long-Fei Wu

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  1. Qunjian Yin
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Correspondence to Weijia Zhang.

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Supported by the National Natural Science Foundation of China (Nos. 41506147, 91751108), the Strategic Priority Research Program of Chinese Academy of Sciences (No. XDB06010203), the Key Research and Development Program of Hainan Province (No. ZDYF2016211), the Natural Science Foundation of Hainan Province (No. 20163151), the Sanya City (No. 2016PT18), and a grant for LIA-MagMC from the Centre National de la Recherche Scientifique

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Yin, Q., Zhang, W., Li, X. et al. Contribution of trimethylamine N-oxide on the growth and pressure tolerance of deep-sea bacteria. J. Ocean. Limnol. 37, 210–222 (2019). https://doi.org/10.1007/s00343-019-7377-9

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