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The deep-sea bacterium, Photobacterium profundum SS9, has been adopted as a model organism to understand the molecular basis of cold-adapted high-pressure-loving (piezophilic) growth. Despite growing optimally at 28 MPa (15 degrees C), P. profundum SS9 can grow over a wide range of pressures and temperatures. The ability to grow at atmospheric pressure has enabled a limited set of genetic tools to be developed, which has provided genetic insights into the mechanism of piezophilic growth in P. profundum SS9. This review focuses on how genetic studies have uncovered the importance of processes affecting the DNA and the bacterial cell envelope in the piezophilic growth of P. profundum SS9. In addition, a method was developed to assess quantitative piezophilic colony growth of P. profundum SS9 on solid agar. Future studies, using this methodology, could provide novel insights into the molecular basis of piezophilic, surface-attached growth.

Motility is a critical function needed for nutrient acquisition, biofilm formation, and the avoidance of harmful chemicals and predators. Flagellar motility is one of the most pressure-sensitive cellular processes in mesophilic bacteria; therefore, it is ecologically relevant to determine how deep-sea microbes have adapted their motility systems for functionality at depth. In this study, the motility of the deep-sea piezophilic bacterium Photobacterium profundum SS9 was investigated and compared with that of the related shallow-water piezosensitive strain Photobacterium profundum 3TCK, as well as that of the well-studied piezosensitive bacterium Escherichia coli. The SS9 genome contains two flagellar gene clusters: a polar flagellum gene cluster (PF) and a putative lateral flagellum gene cluster (LF). In-frame deletions were constructed in the two flagellin genes located within the PF cluster (flaA and flaC), the one flagellin gene located within the LF cluster (flaB), a component of a putative sodium-driven flagellar motor (motA2), and a component of a putative proton-driven flagellar motor (motA1). SS9 PF flaA, flaC, and motA2 mutants were defective in motility under all conditions tested. In contrast, the flaB and motA1 mutants were defective only under conditions of high pressure and high viscosity. flaB and motA1 gene expression was strongly induced by elevated pressure plus increased viscosity. Direct swimming velocity measurements were obtained using a high-pressure microscopic chamber, where increases in pressure resulted in a striking decrease in swimming velocity for E. coli and a gradual reduction for 3TCK which proceeded up to 120 MPa, while SS9 increased swimming velocity at 30 MPa and maintained motility up to a maximum pressure of 150 MPa. Our results indicate that P. profundum SS9 possesses two distinct flagellar systems, both of which have acquired dramatic adaptations for optimal functionality under high-pressure conditions.

In the ocean's most extreme depths, pressures of 70 to 110 megapascals prevent the growth of all but the most hyperpiezophilic (pressure-loving) organisms. The physiological adaptations required for growth under these conditions are considered to be substantial. Efforts to determine specific adaptations permitting growth at extreme pressures have thus far focused on relatively few gamma-proteobacteria, in part due to the technical difficulties of obtaining piezophilic bacteria in pure culture. Here, we present the molecular phylogenies of several new piezophiles of widely differing geographic origins. Included are results from an analysis of the first deep-trench bacterial isolates recovered from the southern hemisphere (9.9-km depth) and of the first gram-positive piezophilic strains. These new data allowed both phylogenetic and structural 16S rRNA comparisons among deep-ocean trench piezophiles and closely related strains not adapted to high pressure. Our results suggest that (i) the Circumpolar Deep Water acts as repository for hyperpiezophiles and drives their dissemination to deep trenches in the Pacific Ocean and (ii) the occurrence of elongated helices in the 16S rRNA genes increases with the extent of adaptation to growth at elevated pressure. These helix changes are believed to improve ribosome function under deep-sea conditions.

Deep-sea life requires adaptation to high pressure, an extreme yet common condition given that oceans cover 70% of Earth's surface and have an average depth of 3800 meters. Survival at such depths requires specific adaptation but, compared with other extreme conditions, high pressure has received little attention. Recently, Photobacterium profundum strain SS9 has been adopted as a model for piezophily. Here we report its genome sequence (6.4 megabase pairs) and transcriptome analysis. The results provide a first glimpse into the molecular basis for life in the largest portion of the biosphere, revealing high metabolic versatility.