Genomic and physiological analysis reveals versatile metabolic capacity of deep-sea Photobacterium phosphoreum ANT-2200

Abstract

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.

High Hydrostatic Pressure Inducible Trimethylamine N-Oxide Reductase Improves the Pressure Tolerance of Piezosensitive Bacteria Vibrio fluvialis

“…The response regulator TorR binds at the TTCATA motif in the promoter regions of tor gene clusters and activates the gene expression only when phosphorylated by TorS ( Simon et al, 1995 ; Ansaldi et al, 2000 ; Bordi et al, 2004 ). HHP enhanced torA gene expression and TMAO reductase activity have only been previously reported in P. profundum SS9 and P. phosphoeum ANT-2200 ( Vezzi et al, 2005 ; Le Bihan et al, 2013 ; Zhang et al, 2016 ). Here, we extend the same phenotype to Vibrio , which is another genus of Vibrionaceae.…”

“…Photobacterium profundum piezophilic strain SS9 and piezophilic luminous bacterium P. phosphoreum ANT-2200 were isolated from 2,500 and 2,200 m depth, respectively ( Nogi et al, 1998 ; Al Ali et al, 2010 ; Martini et al, 2013 ). They both encode multiple TMAO reductases in the genome, and expression of one of these genes in each strain is up-regulated under the HHP condition ( Campanaro et al, 2005 ; Vezzi et al, 2005 ; Li et al, 2013 ; Zhang et al, 2016 ). Such HHP inducible TMAO reductase has never been reported in other species.…”

“…Such HHP inducible TMAO reductase has never been reported in other species. It is speculated that the TMAO reductase might be constantly synthesized in the deep-sea piezosphere and thus facilitate quick reaction to TMAO released from fish and other deep-sea animals ( Zhang et al, 2016 ). However, direct evidence supporting that TMAO respiration could be favorable for bacteria to live under HHP is lacking.…”

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

“…Both expression of TMAO reductase and kinetics of TMAO reduction are increased under HHP condition, which eventually result in improved pressure tolerance in deep-sea bacteria V. fluvialis QY27 when TMAO is presented (Yin et al, 2018). Pressure inducible TMAO reductase has been reported in several deepsea bacteria (Vezzi et al, 2005;Le Bihan et al, 2013;Zhang et al, 2014Zhang et al, , 2016, it is plausible to deduce that TMAO improved pressure tolerance may be present in other strains as well. However, none of the 32 strains analyzed in this study exhibited improved pressure tolerance at 30 MPa when supplemented with TMAO, indicating the remarkable phenomenon might be a species-specific feature of Vibrio fluvialis.…”

“…However, highly accumulated TMAO (up to 386±18 mmol/kg) has been observed in the muscle tissue of deep-sea animals, where it functions as an osmolyte and protects the proteins from multiple stresses including low temperature, high concentration of urea and HHP (Yancey et al, 1982(Yancey et al, , 2001(Yancey et al, , 2014Gillett et al, 1997;Saad-Nehme et al, 2001;Zou et al, 2002;He et al, 2009;Petrov et al, 2012). It is speculated that TMAO released from deep-sea animals may create a microenvironment with instant high concentration of TMAO and provides bacteria nearby precious nutrient for growth (Zhang et al, 2016).…”