Distinctive Gene and Protein Characteristics of Extremely Piezophilic Colwellia

Abstract

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.

Comparative genomic analysis of obligately piezophilic Moritella yayanosii DB21MT-5 reveals bacterial adaptation to the Challenger Deep, Mariana Trench

“…Additionally, abundant genes involved in inorganic ion transport, heavy metal resistance and stress response are detected at the bottom of Yap Trench as well as the Puerto Rico Trench, suggesting a common characteristic of hadal micro-organisms [25,28]. Consistent with previous findings, it is recently confirmed experimentally that three obligate piezophiles from the genus of Colwellia exhibited higher resistance to copper compared to their pressure sensitive counterparts [26].…”

“…The presence of the nuo gene cluster enables the piezophilic Moritella strains to acquire electrons from NADH, while the non-piezophilic strains might rely on other forms of reductant for energy generation. The same trait has been observed in strains from the genus of Colwellia, in which the nuo genes are uniquely present in three hadal piezophiles [26]. It is speculated that the generation and consumption of NADH are effected by high pressures, and the additional nuo gene cluster may facilitate the energy generation and protect cells from reductive stress caused by the excess of NADH.…”

“…We identified one GI composing ten bacteriophage-related genes that are specific to the strain DB21MT-5, and 14 GIs containing obligate-specific genes with mobile genetic elements (MGEs) such as transposases, integrases and recombinases located adjacent. It should be noted that the presence of MGEs near genes specific to piezophilic strains has also been observed within the genus of Colwellia and Shewanella, and it has been proposed that the MGEs may enhance acquisition of genes and acclimation to HHP environment [26].…”

“…Physiological study of this distinctive group is obstructed by the stringent requirement in their isolation and cultivation. In an effort to illustrate their peculiar lifestyles and adaptation to the extreme HHP environments, a number of metagenomic and comparative genomic studies have been carried out [25][26][27]. Eloe et al reported an enrichment of genes related to signal transduction and polysaccharide degradation in the metagenomes from the Puerto Rico Trench compared to shallow water samples [28].…”

Genome sequence analysis of deep sea Aspergillus sydowii BOBA1 and effect of high pressure on biodegradation of spent engine oil

“…Furthermore, BOBA1 showed genes that could facilitate tolerance to high pressure (Supplementary Table S10 ). Numerous genes or gene clusters to cope with extreme living conditions such as genes for d -alanine- d -alanine ligase (2) involved in peptidoglycan formation, alanine dehydrogenase (3) for NADH/NAD + homeostasis and SAM domain containing protein (1) for tRNA modification were present in BOBA1 67 . The existence of cytochrome c (3) genes could provide more ability to cope with the high pressure environments 68 .…”