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Fdileague Group

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Nolan Thompson
Nolan Thompson

Ls Land Issue 11 Variety 637

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.

ls land issue 11 variety 637

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.

Stress-response genes are also differentially present in the genomes. Deoxyribopyrimidine photolyase (DNA photolyase; phrB), which is involved in repairing DNA damaged by ultraviolet light, is found in strains 34H and ND2E but notably absent in all piezophilic Colwellia. Both piezophilic and piezosensitive strains contain superoxide dismutase and catalase for responding to oxidative stress. The genes araC and lysR, whose products control the expression of a variety of stress response systems, are more abundant in the piezosensitive Colwellia. The piezophilic Colwellia are distinct in having multicopper oxidases and copper chaperones for coping with heavy metal damage and maintaining copper homeostasis. Phenotypic analysis of the Colwellia showed that the piezophiles appear more resistant to copper exposure compared to their non-piezophilic counterparts (Supplementary Fig. 6). Some of the genes which putatively confer heavy metal resistance are similar to other piezophiles and are located near genomic islands or other horizontally transferred elements, consistent with the hypothesis that heavy metal genes can be horizontally transferred (e.g. [20, 96, 101]).

A number of the genes specific to piezophiles are present near one another, rather than individually spread throughout the genome (Table 2). Many of these genes are near variable regions containing genomic islands, phage genes, transposases, and toxin-antitoxin system genes (Supplementary Fig. 7). For example, the d-alanine-d-alanine ligase in strain MT41 is next to two putative genomic island regions, one of which is different than that present in strain TT2012 (Fig. 4). Because genomic islands are identified based on nucleotide bias across the genome and the Colwellia sp. TT2012 genome is fragmented into short contigs, the lack of predicted genomic islands does not preclude their presence. In the piezophile Moritella yayanosii this gene is near a gene encoding a predicted phage integrase protein, while in Shewanella benthica KT99 it is present in a flagellar operon that also contains a transposase embedded within it. Similarly, the piezophile-specific alanine dehydrogenase is present near a number of phage and toxin/antitoxin genes and downstream from a genomic island. In strain TT2012, this gene is in the middle of a putative genomic island (Fig. 4), while in Photobacterium profundum SS9 it is flanked on one side by a transposase. Some of the genes present in these variable regions, when not specific to piezophiles, display low similarity to members of the genus Vibrio. The similarity of variable genes within Colwellia to species of Vibrio has been previously noted [24]. Horizontal gene transfer has been shown to be important in the evolution of Vibrio species [40].

We identified a number of gene abundance characteristics that could confer adaptation to the deep ocean. Enrichments in COG J (translation), L (replication and repair), M (cell wall/membrane biogenesis), and N (cell motility) appear enriched in the piezophiles. An enrichment of category M and L has previously been observed within deep ecotypes of Alteromonas [55]. The enrichment within the piezophiles of COG M is in part due to higher abundances of glycosyltransferases, which appear to correlate with depth within metagenome datasets [31]. Glycosyltransferases have been predicted to contribute to low temperature-adaptation [91] and could be more abundant in the psychropiezophiles because they are more stenothermic. In contrast, a fatty acid cis/trans isomerase was present only in the piezosensitive strains. The rapid cis-to-trans isomerization of unsaturated fatty acids via this isomerase has been observed in Pseudomonas putida P8 in response to changes in temperature and salinity [50, 76]. Furthermore, the COG category for transcription (K) is significantly enriched in non-piezophiles compared to piezophiles. This is in part due to an enrichment in the transcription factors AraC and LysR, which have a wide variety of regulatory functions including carbon metabolism and stress response [44, 80]. The enrichment of COG category K in shallow-water organisms has been observed in the surface-water ecotype of Alteromonas macleodii [55]. These findings could reflect the adaptation of non-piezophilic shallow-water microbes to a more dynamic environment, such as rapid salinity or temperature shifts associated with sea-ice or surface seawater. In contrast, autochthonous, obligate deep-ocean microbes would not be expected to experience similar rates or magnitudes of these changes.

Horizontal gene transfer (HGT) can provide genetic material that enhances fitness in new environments. An experimental demonstration of this impact is the introduction of a DNA photolyase gene, missing in piezophilic Colwellia and other deep-sea species [31, 61, 67, 110], into the piezophile Photobacterium profundum SS9 to generate a UV resistant phenotype [70]. It is striking that many of the Colwellia genes most similar to those in other piezophiles appear in clusters within variable regions that include genomic islands, putative phage genes, transposases, and toxin-antitoxin systems. Despite their smaller genome sizes, laterally transferred elements such as transposase and toxin-antitoxin genes are more abundant in the piezophilic Colwellia examined here, consistent with their lower coding densities. Another notable feature of these variable regions is that they differ even between closely-related strains, such as between Colwellia marinimaniae MT41 and C. marinimaniae MTCD1.

Mobile genetic elements have been suggested to confer adaptations to extreme conditions (e.g. [5, 23, 43, 77, 84, 113]), such as in the known piezophile Photobacterium profundum SS9 [18]. Deep-sea specific toxin-antitoxin systems have been identified in members of the Shewanella [155] and have been shown to influence the growth of Pyrococcus yayanosii at different pressures [74, 75]. Mobile genetic elements may provide new metabolisms within strains of Colwellia psychrerythraea, including the transfer of sox genes involved in sarcosine metabolism [24, 134]. Because of the similarity of many genomic island-associated genes in members of the piezophilic Colwellia to those in other gammaproteobacterial piezophiles, we suggest that HGT is a significant evolutionary process governing high pressure adaptation. Future studies should evaluate these regions and their associated genes for their importance in piezophily.

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