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The Hadal Amphipod Hirondellea gigas possessing a unique cellulase for digesting wooden debris buried in the deepest seafloor.

ABSTRACT: The Challenger Deep in the Mariana Trench is the deepest point in the ocean (10,994 m). Certain deep-sea animals can withstand the extreme pressure at this great depth. The amphipod Hirondellea gigas is a resident of the Challenger Deep. Amphipods are common inhabitants at great depths and serve as scavengers. However, there is relatively little information available regarding the physiology of H. gigas or this organism's ecological interactions in the hadopelagic zone. To understand the feeding behavior of this scavenger in the deepest oligotrophic hadal zone, we analyzed the digestive enzymes in whole-body extracts. We describe the detection of amylase, cellulase, mannanase, xylanase, and ?-glycosidase activities that are capable of digesting plant-derived polysaccharides. Our identification of glucose, maltose, and cellobiose in the H. gigas extracts indicated that these enzymes function under great pressure in situ. In fact, the glucose content of H. gigas averaged 0.4% (w/dry-w). The purified H. gigas cellulase (HGcel) converted cellulose to glucose and cellobiose at an exceptional molar ratio of 2:1 and efficiently produced glucose from dried wood, a natural cellulosic biomass, at 35 °C. The enzyme activity increased under a high hydrostatic pressure of 100 MPa at 2 °C, conditions equivalent to those found in the Challenger Deep. An analysis of the amino acid sequence of HGcel supported its classification as a family 31 glycosyl hydrolase. However, none of the enzymes of this family had previously been shown to possess cellulase activity. These results strongly suggested that H. gigas adapted to its extreme oligotrophic hadal oceanic environment by evolving digestive enzymes capable of digesting sunken wooden debris.

SUBMITTER: Kobayashi H

PROVIDER: S-EPMC3419748 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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The Hadal Amphipod Hirondellea gigas possessing a unique cellulase for digesting wooden debris buried in the deepest seafloor.

Kobayashi Hideki H Hatada Yuji Y Tsubouchi Taishi T Nagahama Takahiko T Takami Hideto H

PloS one 20120815 8

The Challenger Deep in the Mariana Trench is the deepest point in the ocean (10,994 m). Certain deep-sea animals can withstand the extreme pressure at this great depth. The amphipod Hirondellea gigas is a resident of the Challenger Deep. Amphipods are common inhabitants at great depths and serve as scavengers. However, there is relatively little information available regarding the physiology of H. gigas or this organism's ecological interactions in the hadopelagic zone. To understand the feeding ...[more]

PMID: 22905166

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Project description: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.

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.

Dataset Information

The Hadal Amphipod Hirondellea gigas possessing a unique cellulase for digesting wooden debris buried in the deepest seafloor.

Publications

The Hadal Amphipod Hirondellea gigas possessing a unique cellulase for digesting wooden debris buried in the deepest seafloor.

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