Distinctive gene and protein characteristics of extremely piezophilic Colwellia

Abstract

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.

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

“…Five genes related to copper oxidation, sequestration and regulation and two cobalt transporter subunits are highly conserved and exclusively present in DB21MT-5 and two piezophilic strains. This is in agreement with previous reports that piezophilic Colwellia strains from the Mariana Trench are more resistant to copper than piezo-sensitive counterparts [26] and with the observation of abundant heavy metal resistance genes at the bottom of the Yap Trench [25]. Considering the enriched of trace metals, including Cu, Mn and Ni in surface sediment at hadal trenches [89, 90], and the discovery that HHP increases copper toxicity to Palaemon varians [91], micro-organisms inhabiting abyssopelagic and hadopelagic zones are more likely to experience heavy metal stress.…”

“…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 ].…”

“…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 [25–27]. Eloe et al .…”

Bacterial and Archaeal Communities in Polymetallic Nodules, Sediments, and Bottom Waters of the Abyssal Clarion-Clipperton Zone: Emerging Patterns and Future Monitoring Considerations

“…And like their shallow-water counterparts, deep-sea sponges host communities of bacteria and archaea that are distinct from those of the surrounding seawater, with deep-sea sponges particularly favorable habitats for members of the Nitrosopumilaceae (e.g., Steinert et al, 2020). Over the very long temporal duration of nodules (Ku and Broecker, 1969;Hein et al, 2020), attached macro-organisms would presumably episodically die; live vs. detrital epizoans would likely have different effects on microbes, and we speculate that changes in epizoan presence and health could potentially explain some nodule samples that have been observed to have outlier microbial communities, such as the three nodules from studies in the central Pacific that were each highly enriched in the chemoheterotrophic genus Colwellia (Tully and Heidelberg, 2013;Blöthe et al, 2015), which includes piezophilic members with chitin-degradation pathways (Peoples et al, 2020).…”