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.
Bacteria of the genus Photobacterium thrive worldwide in oceans and show substantial eco-physiological diversity including free-living, symbiotic and piezophilic life styles. Genomic characteristics underlying this variability across species are poorly understood. Here we carried out genomic and physiological analysis of Photobacterium phosphoreum strain ANT-2200, the first deep-sea luminous bacterium of which the genome has been sequenced. Using optical mapping we updated the genomic data and reassembled it into two chromosomes and a large plasmid. Genomic analysis revealed a versatile energy metabolic potential and physiological analysis confirmed its growth capacity by deriving energy from fermentation of glucose or maltose, by respiration with formate as electron donor and trimethlyamine N-oxide (TMAO), nitrate or fumarate as electron acceptors, or by chemo-organo-heterotrophic growth in rich media. Despite that it was isolated at a site with saturated dissolved oxygen, the ANT-2200 strain possesses four gene clusters coding for typical anaerobic enzymes, the TMAO reductases. Elevated hydrostatic pressure enhances the TMAO reductase activity, mainly due to the increase of isoenzyme TorA1. The high copy number of the TMAO reductase isoenzymes and pressure-enhanced activity might imply a strategy developed by bacteria to adapt to deep-sea habitats where the instant TMAO availability may increase with depth.
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