Complete genome sequence and comparative analysis of Shewanella violacea, a psychrophilic and piezophilic bacterium from deep sea floor sediments

Graduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma, Nara, Japan.
Molecular BioSystems (Impact Factor: 3.18). 07/2010; 6(7):1216-26. DOI: 10.1039/c000396d
Source: PubMed

ABSTRACT Remineralization of organic matter in deep-sea sediments is important in oceanic biogeochemical cycles, and bacteria play a major role in this process. Shewanella violacea DSS12 is a psychrophilic and piezophilic gamma-proteobacterium that was isolated from the surface layer of deep sea sediment at a depth of 5110 m. Here, we report the complete genome sequence of S. violacea and comparative analysis with the genome of S. oneidensis MR-1, isolated from sediments of a freshwater lake. Unlike S. oneidensis, this deep-sea Shewanella possesses very few terminal reductases for anaerobic respiration and no c-type cytochromes or outer membrane proteins involved in respiratory Fe(iii) reduction, which is characteristic of most Shewanella species. Instead, the S. violacea genome contains more terminal oxidases for aerobic respiration and a much greater number of putative secreted proteases and polysaccharases, in particular, for hydrolysis of collagen, cellulose and chitin, than are encoded in S. oneidensis. Transporters and assimilatory reductases for nitrate and nitrite, and nitric oxide-detoxifying mechanisms (flavohemoglobin and flavorubredoxin) are found in S. violacea. Comparative analysis of the S. violacea genome revealed the respiratory adaptation of this bacterium to aerobiosis, leading to predominantly aerobic oxidation of organic matter in surface sediments, as well as its ability to efficiently use diverse organic matter and to assimilate inorganic nitrogen as a survival strategy in the nutrient-poor deep-sea floor.

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    • "As a result of such microbial adaptation to low temperature, the rate and efficiency of organic carbon mineralization in the cold may be as high as in temperate and warm habitats (Kostka et al., 1999). However, bacteria that grow at temperatures extending into the mesophilic range and that do not show cold adaptations were also isolated from the cold deep seafloor (Rüger, 1989; Rüger and Tan, 1992; Finster and Bak, 1993; Chen et al., 2003; Aono et al., 2010). "
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    ABSTRACT: The temperature responses of sulfate-reducing microbial communities were used as community temperature characteristics for their in situ temperature adaptation, their origin, and dispersal in the deep sea. Sediments were collected from a suite of coastal, continental shelf, and slope sediments from the southwest and southeast Atlantic and permanently cold Arctic fjords from water depths ranging from the intertidal zone to 4327 m. In situ temperatures ranged from 8 °C on the shelf to -1 °C in the Arctic. Temperature characteristics of the active sulfate-reducing community were determined in short-term incubations with 35S-sulfate in a temperature gradient block spanning a temperature range from 0 to 40 °C. An optimum temperature (Topt) between 27 °C and 30 °C for the South Atlantic shelf sediments and for the intertidal flat sediment from Svalbard was indicative of a psychrotolerant/mesophilic sulfate-reducing community, whereas Topt ≤20 °C in South Atlantic slope and Arctic shelf sediments suggested a predominantly psychrophilic community. High sulfate reduction rates (20-50%) at in situ temperatures compared to those at Topt further support this interpretation and point to the importance of the ambient temperature regime for regulating the short-term temperature response of sulfate-reducing communities. A number of cold (<4 °C) continental slope sediments showed broad temperature optima reaching as high as 30 °C, suggesting the additional presence of apparently mesophilic sulfate-reducing bacteria. Since the temperature characteristics of these mesophiles do not fit with the permanently cold deep-sea environment, we suggest that these mesophilic microorganisms are of allochthonous origin and transported to this site. It is likely that they were deposited along with the mass-flow movement of warmer shelf-derived sediment. These data therefore suggest that temperature response profiles of bacterial carbon mineralization processes can be used as community temperature characteristics, and that mixing of bacterial communities originating from diverse locations carrying different temperature characteristics needs to be taken into account to explain temperature response profiles of bacterial carbon mineralization processes in sediments.
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    ABSTRACT: Shewanella violacea DSS12, a deep-sea bacterium, produces eicosapentaenoic acid (EPA) as a component of membrane phospholipids. Although various isolates from the deep sea, such as Photobacterium profundum SS9, Colwellia psychrerythraea 34H and various Shewanella strains, produce EPA- or docosahexaenoic acid-containing phospholipids, the physiological role of these polyunsaturated fatty acids remains unclear. In this article, we illustrate the physiological importance of EPA for high-pressure adaptation in strain DSS12 with the help of an EPA-deficient mutant (DSS12(pfaA)). DSS12(pfaA) showed significant growth retardation at 30 MPa, but not at 0.1 MPa. We also found that DSS12(pfaA) grown at 30 MPa forms filamentous cells. When an EPA-containing phospholipid (sn-1-oleoly-sn-2-eicosapentaenoyl phosphatidylethanolamine) was supplemented, the growth retardation and the morphological defect of DSS12(pfaA) were suppressed, indicating that the externally added EPA-containing phospholipid compensated for the loss of endogenous EPA. In contrast, the addition of an oleic acid-containing phospholipid (sn-1,2-dioleoyl phosphatidylethanolamine) did not affect the growth and the morphology of the cells. Immunofluorescent microscopic analysis with anti-FtsZ antibody revealed a number of Z-rings and separated nucleoids in DSS12(pfaA) grown at 30 MPa. These results demonstrate the physiological importance of EPA for the later step of Z-ring formation of S. violacea DSS12 under high-pressure conditions.
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