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 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.

Metagenomic Insights Into the Structure and Function of Intestinal Microbiota of the Hadal Amphipods

“…In detail, the functional pathways of PTS, Glycolysis/Gluconeogenesis, Homologous Recombination, Bacterial Chemotaxis, and Flagellar Assembly were detected as the common functional types in all the amphipod gut samples, suggesting that the existence of a set of similar functional components in gut microbes of the hadal amphipod species ( Figure 4 and Supplementary Figures 1 , 2 ). However, the previous study on the H. gigas from Mariana Trench and Japan Trench have shown that different geographical locations lead to functional differentiation of their gut microbes ( Zhang et al, 2019 ) and which was inconsistent with the results of the present study. This difference may result from a combination of selection factors, such as habitat environment, microbial interaction, and host genetic background, and the details remain to be analyzed.…”

“…For instance, Candidatus Hepatoplasma was detected as the dominant bacterium in the gut of the S. schellenbergi and A. gigantea , whereas relative absence in the H. gigas. Given that the New Britain Trench is closest to the coast followed by the Marceau Trench, and finally the Mariana Trench, the decaying plant material content in these trenches should show a decreasing trend, which may be the reason for the difference in the abundance of Candidatus Hepatoplasma in the gut of different amphipod species, and similar conclusions have been mentioned in previous studies ( Zhang et al, 2019 ). Moreover, the difference in the abundance of Psychromonas of gut microbial composition was also detected among the three geographically isolated amphipod species, especially the almost absence of Psychromonas in the S. schellenbergi and A. gigantea , which suggested that their function is dispensable or their counterparts have emerged in the guts of these amphipods, as Zhang et al (2019) mentioned in the previous study.…”

“…In our study, based on the composition of the gut microbial communityfrom three hadal amphipod species, the common dominant taxa at phylum and genus levels were detected ( Figures 2 , 3 ), which suggested that the gut microbial compositions of the co-dwelling hadal amphipods were relatively constant inter-species. We noted that the dominant bacterial taxa at the genus level, such as Candidatus Hepatoplasma and Burkholderia , have been reported to be abundant in different populations of hadal amphipod species ( Zhang et al, 2018 , 2019 ; Cheng et al, 2019 ) and also been reported to be symbionts of bean bugs ( Kim et al, 2015 ) and terrestrial isopods ( Wang et al, 2004 ). Candidatus Hepatoplasma , identified as a Mycoplasma -like symbiont abundant in terrestrial isopods, showed a positive correlation between the host and survivorship on low-quality food ( Sebastian and Martin, 2008 ).…”

Distinctive gene and protein characteristics of extremely piezophilic Colwellia

“…[95]) and the microbial activity of the gut contents of deep-sea animals shows high levels of piezophily [131]. However, the genus Colwellia is not present in recognizable abundances within hadal amphipod metagenomes [154], their high % GC is not indicative of an endosymbiont [89], and the obligate piezophile Colwellia sp. TT2012 was isolated from sediments rather than amphipods.…”

Structure and Function of the Arctic and Antarctic Marine Microbiota as Revealed by Metagenomics

“…Recent advances in molecular ecological techniques, such as metagenomics, have enabled a more efficient pathway to address the taxonomic and functional composition of marine microbiota, including the free-living bacterioplankton [1,2,3], the sediment-dwelling microbes [4,5,6], the surface-attached biofilms [7,8,9], and the animal-associated symbionts [10,11,12]. Pursuing the goal characterisng the global seawater microbiota, the Tara Oceans expedition collected seawater samples from 68 locations, representing all main oceanic regions, and performed metagenomics to study the structure and function of the global ocean microbiota [1].…”