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Background The deep ocean is characterized by low temperatures, high hydrostatic pressures, and low concentrations of organic matter. While these conditions likely select for distinct genomic characteristics within prokaryotes, the attributes facilitating adaptation to the deep ocean are relatively unexplored. In this study, we compared the genomes of seven strains within the genus Colwellia, including some of the most piezophilic microbes known, to identify genomic features that enable life in the deep sea. Results Significant differences were found to exist between piezophilic and non-piezophilic strains of Colwellia. Piezophilic Colwellia have a more basic and hydrophobic proteome. The piezophilic abyssal and hadal isolates have more genes involved in replication/recombination/repair, cell wall/membrane biogenesis, and cell motility. The characteristics of respiration, pilus generation, and membrane fluidity adjustment vary between the strains, with operons for a nuo dehydrogenase and a tad pilus only present in the piezophiles. In contrast, the piezosensitive members are unique in having the capacity for dissimilatory nitrite and TMAO reduction. A number of genes exist only within deep-sea adapted species, such as those encoding d-alanine-d-alanine ligase for peptidoglycan formation, alanine dehydrogenase for NADH/NAD+ homeostasis, and a SAM methyltransferase for tRNA modification. Many of these piezophile-specific genes are in variable regions of the genome near genomic islands, transposases, and toxin-antitoxin systems. Conclusions We identified a number of adaptations that may facilitate deep-sea radiation in members of the genus Colwellia, as well as in other piezophilic bacteria. An enrichment in more basic and hydrophobic amino acids could help piezophiles stabilize and limit water intrusion into proteins as a result of high pressure. Variations in genes associated with the membrane, including those involved in unsaturated fatty acid production and respiration, indicate that membrane-based adaptations are critical for coping with high pressure. The presence of many piezophile-specific genes near genomic islands highlights that adaptation to the deep ocean may be facilitated by horizontal gene transfer through transposases or other mobile elements. Some of these genes are amenable to further study in genetically tractable piezophilic and piezotolerant deep-sea microorganisms.

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The subduction of seamounts and ridge features at convergent plate boundaries plays an important role in the deformation of the overriding plate and influences geochemical cycling and associated biological processes. Active serpentinization of forearc mantle and serpentinite mud volcanism on the Mariana forearc (between the trench and active volcanic arc) provides windows on subduction processes.  Here, we present (1) the first observation of an extensive exposure of an undeformed Cretaceous seamount currently being subducted at the Mariana Trench inner slope; (2) vertical deformation of the forearc region related to subduction of Pacific Plate seamounts and thickened crust; (3) recovered Ocean Drilling Program and International Ocean Discovery Program cores of serpentinite mudflows that confirm exhumation of various Pacific Plate lithologies, including subducted reef limestone; (4) petrologic, geochemical and paleontological data from the cores that show that Pacific Plate seamount exhumation covers greater spatial and temporal extents; (5) the inference that microbial communities associated with serpentinite mud volcanism may also be exhumed from the subducted plate seafloor and/or seamounts; and (6) the implications for effects of these processes with regard to evolution of life. This article is part of a discussion meeting issue ‘Serpentine in the Earth system’.

Background 24The deep ocean is characterized by low temperatures, high hydrostatic pressures, and low 25 concentrations of organic matter. While these conditions likely select for distinct genomic 26 characteristics within prokaryotes, the attributes facilitating adaptation to the deep ocean are 27 relatively unexplored. In this study, we compared the genomes of seven strains within the genus 28Colwellia, including some of the most piezophilic microbes known, to identify genomic features 29 that enable life in the deep sea. 30 31 Results 32 Significant differences were found to exist between piezophilic and non-piezophilic strains of 33 Colwellia. Piezophilic Colwellia have a more basic and hydrophobic proteome. The piezophilic 34 abyssal and hadal isolates have more genes involved in replication/recombination/repair, cell 35 wall/membrane biogenesis, and cell motility. The characteristics of respiration, pilus generation, 36 and membrane fluidity adjustment vary between the strains, with operons for a nuo 37 dehydrogenase and a tad pilus only present in the piezophiles. In contrast, the piezosensitive 38 members are unique in having the capacity for dissimilatory nitrite and TMAO reduction. A 39 number of genes exist only within deep-sea adapted species, such as those encoding d-alanine-d-40 alanine ligase for peptidoglycan formation, alanine dehydrogenase for NADH/NAD + 41 homeostasis, and archaeal methyltransferase for tRNA modification. Many of these piezophile-42 specific genes are in variable regions of the genome near genomic islands, transposases, and 43 toxin-antitoxin systems. 44 45 Conclusions 46We identified a number of adaptations that may facilitate deep-sea radiation in members of the 47 genus Colwellia, as well as in other piezophilic bacteria. An enrichment in more basic and 48 hydrophobic amino acids could help piezophiles stabilize and limit water intrusion into proteins 49 as a result of high pressure. Variations in genes associated with the membrane, including those 50 involved in unsaturated fatty acid production and respiration, indicate that membrane-based 51 adaptations are critical for coping with high pressure. The presence of many piezophile-specific 52 genes near genomic islands highlights that adaptation to the deep ocean may be facilitated by 53 horizontal gene transfer through transposases or other mobile elements. Some of these genes are 54 amenable to further study in genetically tractable piezophilic and piezotolerant deep-sea 55 microorganisms.

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Physiological and gene expression studies of deep‐sea bacteria under pressure conditions similar to those experienced in their natural habitat are critical for understanding growth kinetics and metabolic adaptations to in situ conditions. The Campylobacterium (aka Epsilonproteobacterium) Nautilia sp. strain PV‐1 was isolated from hydrothermal fluids released from an active deep‐sea hydrothermal vent at 9° N on the East Pacific Rise. Strain PV‐1 is a piezophilic, moderately thermophilic, chemolithoautotrophic anaerobe that conserves energy by coupling the oxidation of hydrogen to the reduction of nitrate or elemental sulfur. Using a high‐pressure–high temperature continuous culture system, we established that strain PV‐1 has the shortest generation time of all known piezophilic bacteria and we investigated its protein expression pattern in response to different hydrostatic pressure regimes. Proteogenomic analyses of strain PV‐1 grown at 20 and 5 MPa showed that pressure adaptation is not restricted to stress response or homeoviscous adaptation but extends to enzymes involved in central metabolic pathways. Protein synthesis, motility, transport, and energy metabolism are all affected by pressure, although to different extents. In strain PV‐1, low‐pressure conditions induce the synthesis of phage‐related proteins and an overexpression of enzymes involved in carbon fixation.