Abstract
High hydrostatic pressure (HHP) exerts severe effects on cellular processes including impaired cell division, abolished motility and affected enzymatic activities. Transcriptomic and proteomic analyses showed that bacteria switch the expression of genes involved in multiple energy metabolism pathways to cope with HHP. We sought evidence of a changing bacterial metabolism by supplying appropriate substrates that might have beneficial effects on the bacterial lifestyle at elevated pressure. We isolated a piezosensitive marine bacterium Vibrio fluvialis strain QY27 from the South China Sea. When trimethylamine N-oxide (TMAO) was used as an electron acceptor for energy metabolism, QY27 exhibited a piezophilic-like phenotype with an optimal growth at 30 MPa. Raman spectrometry and biochemistry analyses revealed that both the efficiency of the TMAO metabolism and the activity of the TMAO reductase increased under high pressure conditions. Among the two genes coding for TMAO reductase catalytic subunits, the expression level and enzymatic activity of TorA was up-regulated by elevated pressure. Furthermore, a genetic interference assay with the CRISPR-dCas9 system demonstrated that TorA is essential for underpinning the improved pressure tolerance of QY27. We extended the study to Vibrio fluvialis type strain ATCC33809 and observed the same phenotype of TMAO-metabolism improved the pressure tolerance. These results provide compelling evidence for the determinant role of metabolism in the adaption of bacteria to the deep-sea ecosystems with HHP.
Highlights
Trimethylamine N-oxide (TMAO) is widely dispersed in marine environments and plays an important role in the biogeochemical cycle of nitrogen (Ge et al, 2011)
The respiratory chain of piezophile Shewanella violacea DSS12 consists of the bc1-complex and cytochrome c oxidase at 0.1 MPa, whereas cytochrome c-551 and quinol oxidase exhibited higher pressure tolerance is utilized at 60 MPa (Ohke et al, 2013)
Increasing evidence supports the bacterial anticipation of nutrient availability in the deep-sea to switch on the cognate energy metabolism pathway
Summary
Trimethylamine N-oxide (TMAO) is widely dispersed in marine environments and plays an important role in the biogeochemical cycle of nitrogen (Ge et al, 2011). TMAO can be produced through oxidation of TMA by a variety of marine bacteria, phytoplankton, invertebrates and fishes (Barrett and Kwan, 1985; Seibel and Walsh, 2002; McCrindle et al, 2005). It accumulates in the tissue of marine animals and serves to protect against osmotic stress, adverse effects of low temperature, high concentration of urea and HHP (Yancey et al, 1982; Saad-Nehme et al, 2001; Zou et al, 2002; He et al, 2009; Petrov et al, 2012). It can be catabolized by the SAR11 clade and marine Roseobacter clade (MRC) bacteria as a carbon and nitrogen source (Lidbury et al, 2014, 2015) or as an electron acceptor of anaerobic respiration in diverse species of marine bacteria and most species of Enterobacteriaceae (Barrett and Kwan, 1985; Dos Santos et al, 1998; Dunn and Stabb, 2008)
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