Genome Reduction in
            <i>Psychromonas</i>
            Species within the Gut of an Amphipod from the Ocean’s Deepest Point

Zhang, Weipeng; Tian, Ren Mao; Sun, Jin; Bougouffa, Salim; Ding, Wei; Lin, Chunye; Lan, Yi; Tong, Haoya; Li, Yongxin; Jamieson, Alan J.; Bajic, Vladimir B.; Drazen, Jeffrey C.; Bartlett, Douglas H.; Qian, Pei‐Yuan

doi:10.1128/msystems.00009-18

Cited by 25 publications

(21 citation statements)

References 76 publications

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“…In contrast, we found that TMAO reductase (torECAD), which reduces TMAO to TMA, was not present in any of the piezophilic Colwellia. A similar finding has been noted in genomes of Psychromonas from the guts of hadal amphipods, where the lack of TMAO reductase was attributed to the preferential need for TMAO as a piezolyte in the host amphipod over its use as an electron acceptor by the microbe [153]. An alternative hypothesis is that TMAO is used by microbial piezophiles as a piezolyte as it is in deep-sea metazoans [147,148].…”

Section: Discussionsupporting

confidence: 73%

“…Finding differences in respiratory capacity within piezophiles is not unexpected. Others have previously noted the influence of collection depth and pressure on the presence and regulation of respiratory membrane-bound cytochrome c oxidases and hydrogenases [ 22 , 72 , 92 , 132 , 140 , 141 , 144 , 145 , 153 ]. These changes could stem directly from pressure influences or from a greater reliance on the colonization of reduced oxygen niches associated with particles or animals [ 15 , 109 ].…”

Section: Discussionmentioning

confidence: 99%

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Distinctive gene and protein characteristics of extremely piezophilic Colwellia

et al. 2020

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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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Section: Discussionsupporting

confidence: 73%

Section: Discussionmentioning

confidence: 99%

Distinctive gene and protein characteristics of extremely piezophilic Colwellia

et al. 2020

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“…Previous marine isolates of Verrucomicrobiae and Oceanospirillaceae (dominant family of Oceanospirillales in our study) were aerobes with broad substrate spectra (including monosaccharides, amino acids, alcohols, organic acids), and some Oceanospirillaceae additionally perform nitrate reduction ( 36 , 37 ). Opitutae , Psychromonadaceae (dominant family of Alteromonadales ), and BD7-8 subgroup commonly live in symbiotic relations with marine sediment invertebrates and are facultatively anaerobic carbohydrate degraders ( Opitutae , Psychromonadaceae ) or putatively chemoautotrophic, aerobic sulfide oxidizers (BD7-8) ( 38 – 40 ).…”

Section: Discussionmentioning

confidence: 99%

Macrofaunal control of microbial community structure in continental margin sediments

Deng

Bölsterli

Kristensen

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Through a process called “bioturbation,” burrowing macrofauna have altered the seafloor habitat and modified global carbon cycling since the Cambrian. However, the impact of macrofauna on the community structure of microorganisms is poorly understood. Here, we show that microbial communities across bioturbated, but geochemically and sedimentologically divergent, continental margin sites are highly similar but differ clearly from those in nonbioturbated surface and underlying subsurface sediments. Solid- and solute-phase geochemical analyses combined with modeled bioturbation activities reveal that dissolved O2introduction by burrow ventilation is the major driver of archaeal community structure. By contrast, solid-phase reworking, which regulates the distribution of fresh, algal organic matter, is the main control of bacterial community structure. In nonbioturbated surface sediments and in subsurface sediments, bacterial and archaeal communities are more divergent between locations and appear mainly driven by site-specific differences in organic carbon sources.

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“…A Psychromonas strain (CNPT3) has been isolated from the gut of a decaying amphipod collected at a depth of 5,700 m in the North Pacific Ocean (21), suggesting a close relationship between Psychromonas and amphipods in certain deep-sea habitats. In a more recent study of the amphipod gut microbiota from the Mariana Trench, the draft genome of a Psychromonas strain (CDP1) was analyzed, which revealed a significant genome reduction driven by host association (22). Members of the genus Propionibacterium were found in the gut of the bark beetle Dendroctonus rhizophagus and are persistent in all life stages of this insect (23).…”

Section: Discussionmentioning

confidence: 99%

Gut Microbial Divergence between Two Populations of the Hadal Amphipod Hirondellea gigas

Zhang

Watanabe

Ding

et al. 2019

Appl Environ Microbiol

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Hadal environments sustain diverse microorganisms. A few studies have investigated hadal microbial communities consisting of free-living or particle-associated bacteria and archaea. However, animal-associated microbial communities in hadal environments remain largely unexplored, and comparative analyses of animal gut microbiota between two isolated hadal environments have never been done so far. In the present study, 228 Gb of gut metagenomes of the giant amphipodHirondellea gigasfrom two hadal trenches, the Mariana Trench and Japan Trench, were sequenced and analyzed. Taxonomic analysis identified 49 microbial genera commonly shared by the gut microbiota of the twoH. gigaspopulations. However, the results of statistical analysis, in congruency with the alpha and beta diversity analyses, revealed significant differences in gut microbial composition across the two trenches. Abundance variation ofPsychromonas,Propionibacterium, andPseudoalteromonasspecies was observed. Microbial cooccurrence was demonstrated for microbes that were overrepresented in the Mariana trench. Comparison of functional potential showed that the percentage of carbohydrate metabolic genes among the total microbial genes was significantly higher in the guts ofH. gigasspecimens from the Mariana Trench. Integrating carbon input information and geological characters of the two hadal trenches, we propose that the differences in the community structure might be due to several selective factors, such as environmental variations and microbial interactions.IMPORTANCEThe taxonomic composition and functional potential of animal gut microbiota in deep-sea environments remain largely unknown. Here, by performing comparative metagenomics, we suggest that the gut microbial compositions of twoHirondellea gigaspopulations from the Mariana Trench and the Japan Trench have undergone significant divergence. Through analyses of functional potentials and microbe-microbe correlations, our findings shed light on the contributions of animal gut microbiota to host adaptation to hadal environments.

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Genome Reduction in Psychromonas Species within the Gut of an Amphipod from the Ocean’s Deepest Point

Cited by 25 publications

References 76 publications

Distinctive gene and protein characteristics of extremely piezophilic Colwellia

Distinctive gene and protein characteristics of extremely piezophilic Colwellia

Macrofaunal control of microbial community structure in continental margin sediments

Gut Microbial Divergence between Two Populations of the Hadal Amphipod Hirondellea gigas

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