The TorRS two component system regulates expression of TMAO reductase in response to high hydrostatic pressure in Vibrio fluvialis

Na Liu; Ting Jiang; Wen-Peng Cui; Xiao-Qing Qi; Xue-Gong Li; Yuan Lu; Long-Fei Wu; Wei-Jia Zhang

doi:10.3389/fmicb.2023.1291578

The TorRS two component system regulates expression of TMAO reductase in response to high hydrostatic pressure in Vibrio fluvialis

Front Microbiol. 2023 Nov 7:14:1291578. doi: 10.3389/fmicb.2023.1291578. eCollection 2023.

Authors

Na Liu^#^{1

2}, Ting Jiang^#^{1

2}, Wen-Peng Cui^{1

2}, Xiao-Qing Qi^{1

3

4}, Xue-Gong Li^{1

3

4}, Yuan Lu⁵, Long-Fei Wu^{4

6}, Wei-Jia Zhang^{1

3

4}

Affiliations

¹ Laboratory of Deep-Sea Microbial Cell Biology, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya, China.
² University of Chinese Academy of Sciences, Beijing, China.
³ Institution of Deep-sea Life Sciences, IDSSE-BGI, Sanya, China.
⁴ International Associated Laboratory of Evolution and Development of Magnetotactic Multicellular Organisms, CAS, Sanya, China.
⁵ College of Information Science & Engineering, Ocean University of China, Qingdao, China.
⁶ Aix Marseille University, CNRS, LCB, Marseille, France.

^# Contributed equally.

Abstract

High hydrostatic pressure (HHP) regulated gene expression is one of the most commonly adopted strategies for microbial adaptation to the deep-sea environments. Previously we showed that the HHP-inducible trimethylamine N-oxide (TMAO) reductase improves the pressure tolerance of deep-sea strain Vibrio fluvialis QY27. Here, we investigated the molecular mechanism of HHP-responsive regulation of TMAO reductase TorA. By constructing torR and torS deletion mutants, we demonstrated that the two-component regulator TorR and sensor TorS are responsible for the HHP-responsive regulation of torA. Unlike known HHP-responsive regulatory system, the abundance of torR and torS was not affected by HHP. Complementation of the ΔtorS mutant with TorS altered at conserved phosphorylation sites revealed that the three sites were indispensable for substrate-induced regulation, but only the histidine located in the alternative transmitter domain was involved in pressure-responsive regulation. Taken together, we demonstrated that the induction of TMAO reductase by HHP is mediated through the TorRS system and proposed a bifurcation of signal transduction in pressure-responsive regulation from the substrate-induction. This work provides novel knowledge of the pressure regulated gene expression and will promote the understanding of the microbial adaptation to the deep-sea HHP environment.

Keywords: TMAO reduction; TorRS; adaptation; deep-sea; high hydrostatic pressure; two-component system.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by grant NSFC91751108, 42076127 and 42176121 from the National Natural Science Foundation of China, grant ZDKJ2021028 and ZDKJ2019011 and from the Key Research and Development Program of Hainan Province, grant XDA19060403 from the Strategic Priority Research Program of the Chinese Academy of Sciences. The support provided by Chinese Academy of Sciences during a visit of W-JZ to University of California, San Diego is acknowledged.