Comparative Analysis of Intestinal Microflora Between Two Developmental Stages of Rimicaris kairei, a Hydrothermal Shrimp From the Central Indian Ridge

Abstract

Despite extreme physical and chemical characteristics, deep-sea hydrothermal vents provide a place for fauna survival and reproduction. The symbiotic relationship of chemotrophic microorganisms has been investigated in the gill of Rimicaris exoculata, which are endemic to the hydrothermal vents of the Mid-Atlantic Ridge. However, only a few studies have examined intestinal symbiosis. Here, we studied the intestinal fauna in juvenile and adult Rimicaris kairei, another species in the Rimicaris genus that was originally discovered at the Kairei and Edmond hydrothermal vent fields in the Central Indian Ridge. The results showed that there were significant differences between juvenile and adult gut microbiota in terms of species richness, diversity, and evenness. The values of Chao1, observed species, and ASV rarefaction curves indicated almost four times the number of species in adults compared to juveniles. In juveniles, the most abundant phylum was Deferribacterota, at 80%, while in adults, Campilobacterota was the most abundant, at 49%. Beta diversity showed that the intestinal communities of juveniles and adults were clearly classified into two clusters based on the evaluations of Bray-Curtis and weighted UniFrac distance matrices. Deferribacteraceae and Sulfurovum were the main featured bacteria contributing to the difference. Moreover, functional prediction for all of the intestinal microbiota showed that the pathways related to ansamycin synthesis, branched-chain amino acid biosynthesis, lipid metabolism, and cell motility appeared highly abundant in juveniles. However, for adults, the most abundant pathways were those of sulfur transfer, carbohydrate, and biotin metabolism. Taken together, these results indicated large differences in intestinal microbial composition and potential functions between juvenile and adult vent shrimp (R. kairei), which may be related to their physiological needs at different stages of development.

Keywords: Deferribacteraceae; Rimicaris kairei; Sulfurovum; hydrothermal vent; intestine microflora.

FIGURE 1

Gut microbial compositions of juvenile and adult samples at the phylum level. (A) The phylum level in the juvenile group; (B) the phylum level in the adult group.

FIGURE 2

Alpha diversities of gut microbiota in the two developmental stages of R. kairei. (A–F): Chao1, Faith_phylogenetic diversity, Pielou’s evenness, observed_species, Shannon and Simpson indices are displayed in the box plots (Non-parametric Kruskal–Wallis tests, ***p < 0.001). The middle lines in the boxes indicate the median. The upper and lower lines of the box indicate the upper and lower quartiles, respectively. The scattered dots represent the values of each sample. The larger dots represent outliers.

FIGURE 3

Beta diversities of the two gut microbial communities. (A) NMDS was calculated by Bray–Curtis distance for juvenile and adult shrimp (stress = 0.07). Red dots indicate adult samples. Green triangles indicate juvenile samples. (B) PCoA indicated the similarity of microbiota composition and the phylogenetic distance between the two groups based on the weighted UniFrac algorithm. Component axes indicate the degree of variance.

FIGURE 4

Random forest analysis was performed between the two different developmental stages of R. kairei. The bar plot shows the influence of the top 20 bacteria based on the accuracy of the random forest model. The heatmap shows the bacteria with normalized abundance in the two different groups. Cam, Campilobacterota; Def, Deferribacterota; Fir, Firmicutes; Bac, Bacteroidetes; Pro, Proteobacteria; Ver, Verrucomicrobia; Act, Actinobacteria; Pat, Patescibacteria. F, foregut; H, hindgut. * indicates the shared bacteria with STAMP.

FIGURE 5

The pathways with significant differences between juveniles and adults. Pathways with more than 1% abundance were included in this differential analysis. The diverse pathways are displayed on the y-axis. Relative abundances are displayed on the x-axis. Orange bars indicate adult samples. Blue bars indicate juvenile samples. Asterisks indicate a significant difference. (Non-parametric Kruskal–Wallis tests, *p < 0.05, **p < 0.01).