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

ABSTRACT: 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 amphipod Hirondellea gigas from 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 two H. gigas populations. 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 of Psychromonas, Propionibacterium, and Pseudoalteromonas species 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 of H. gigas specimens 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.IMPORTANCE The 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 two Hirondellea gigas populations 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.

SUBMITTER: Zhang W

PROVIDER: S-EPMC6293092 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Deciphering the mechanisms governing population genetic divergence and local adaptation across heterogeneous environments is a central theme in marine ecology and conservation. While population divergence and ecological adaptive potential are classically viewed at the genetic level, it has recently been argued that their microbiomes may also contribute to population genetic divergence. We explored whether this might be plausible along the well-described environmental gradient of the Baltic Sea in two species of sand lance (Ammodytes tobianus and Hyperoplus lanceolatus). Specifically, we assessed both their population genetic and gut microbial composition variation and investigated not only which environmental parameters correlate with the observed variation, but whether host genome also correlates with microbiome variation. RESULTS:We found a clear genetic structure separating the high-salinity North Sea from the low-salinity Baltic Sea sand lances. The observed genetic divergence was not simply a function of isolation by distance, but correlated with environmental parameters, such as salinity, sea surface temperature, and, in the case of A. tobianus, possibly water microbiota. Furthermore, we detected two distinct genetic groups in Baltic A. tobianus that might represent sympatric spawning types. Investigation of possible drivers of gut microbiome composition variation revealed that host species identity was significantly correlated with the microbial community composition of the gut. A potential influence of host genetic factors on gut microbiome composition was further confirmed by the results of a constrained analysis of principal coordinates. The host genetic component was among the parameters that best explain observed variation in gut microbiome composition. CONCLUSIONS:Our findings have relevance for the population structure of two commercial species but also provide insights into potentially relevant genomic and microbial factors with regards to sand lance adaptation across the North Sea-Baltic Sea environmental gradient. Furthermore, our findings support the hypothesis that host genetics may play a role in regulating the gut microbiome at both the interspecific and intraspecific levels. As sequencing costs continue to drop, we anticipate that future studies that include full genome and microbiome sequencing will be able to explore the full relationship and its potential adaptive implications for these species.

Project description:Background:The hadal zone encompasses the deepest parts of the world's ocean trenches from depths of ?6,000-11,000 m. The communities observed at these depths are dominated by scavenging amphipods that rapidly intercept and consume carrion as it falls to the deepest parts of the trenches. New samples collected in the Tonga Trench provide an opportunity to compare the amphipod assemblages and the population structure of a dominant species, Hirondellea dubia Dahl, 1959, between trenches and with earlier data presented for the Tonga Trench, and other trenches in the South Pacific. Methods:Over 3,600 individual scavenging amphipods across 10 species were collected in seven baited traps at two sites; in the Horizon Deep site, the deepest part of the Tonga Trench (10,800 m) and a site directly up-slope at the trench edge (6,250 m). The composition of the bait-attending amphipods is described and a morphometric analysis of H. dubia examines the bathymetric distribution of the different life stages encountered. Results:The amphipod assemblage was more diverse than previously reported, seven species were recorded for the first time from the Tonga Trench. The species diversity was highest at the shallower depth, with H. dubia the only species captured at the deepest site. At the same time, the abundance of amphipods collected at 10,800 m was around sevenfold higher than at the shallower site. H. dubia showed clear ontogenetic vertical structuring, with juveniles dominant at the shallow site and adults dominant at the deep site. The amphipods of the deeper site were always larger at comparable life stage. Discussion:The numbers of species encountered in the Tonga Trench is less than reported from the New Hebrides and Kermadec trenches, and six species encountered are shared across trenches. These findings support the previous suggestion that the fauna of the New Hebrides, Tonga and Kermadec Trenches may represent a single biogeographic province. The ontogenetic shift in H. dubia between the two Tonga Trench sites supports the hypothesis of interspecific competition at the shallower bathymetric range of the species, and the presence of competitive physiological advantages that allow the adults at the trench axis to exploit the more labile organic material that reaches the bottom of the trench.

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

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