Dong Y et al. (2021), Gut Microbial Composition and Diversity in Four...

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Front Microbiol 2021 Mar 19;12:645070. doi: 10.3389/fmicb.2021.645070.

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Gut Microbial Composition and Diversity in Four Ophiuroid Species: Divergence Between Suspension Feeder and Scavenger and Their Symbiotic Microbes.

Dong Y , Li Y , He P , Wang Z , Fan S , Zhang Z , Zhang X , Xu Q .

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Gut microbiota have important roles in the survival and adaptation of the host. Ophiuroids, as the worldwide dominant benthos, have ecological roles in benthic-pelagic coupling in the sea floor. However, little is known about the composition and diversity of their gut microbiota and its potential functions in benthic ecosystems. In present study, we preformed 16S rRNA sequencing and function analysis in four dominant species (Stegophiura sladeni, Ophiopholis mirabilis, Ophiura sarsii vadicola, and Ophiura kinbergi) with two feeding types (suspension feeding/herbivores and scavenger/carnivores) from the Yellow Sea, China. Results showed that 56 phyla and 569 genera of microbiota were identified among ophiuroid guts. Multivariate and diversity analyses showed that the ophiuroid gut microbiota were independent and have higher biodiversity to the sediment microbial in the Yellow Sea. Phyla Proteobacteria, Firmicutes, Tenericutes, and Bacteroidetes were the dominant bacteria, with more than 80% abundance among the four ophiuroid species. A comparison among the gut microbial compositions among four ophiuroids showed the similarity of two offshore carnivore ophiuroids (S. sladeni and O. sarsii vadicola) and variation in the dominant microbiota types of three nearshore ophiuroids (S. sladeni, O. mirabilis, and O. kinbergi). The functional analysis revealed the significant differences of the environment-related expression in S. sladeni gut microbiota between nearshore and offshore environments. The Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) functional annotation showed the significant divergence of metabolism pathways between two nearshore species, the herbivores O. mirabilis and carnivores S. sladeni, such as the Lipid metabolism, Carbohydrate metabolism, and Metabolism of cofactors and vitamins. The homolog search and phylogenetic analysis identified the first gut symbiotic Candidatus Hepatoplasma in S. sladeni with important roles for the nutrient metabolisms. Overall, our study reported the comprehensive data of ophiuroid gut microbiota, while the functional microbiome provides insight into the physiology and environmental adaptation in ophiuroids.

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	FIGURE 1. Location of sampling sites in the southern Yellow Sea. Ophiuroids were collected from nearshore (station Y) with blue color and offshore (station H) with red color. Sediment stations were H05, H18, H19, H09, HS1, H11, and H26 (Zhang et al., 2019).
	FIGURE 2. Taxonomic abundance of gut microbiota at the phylum level (A) and genera level (B) in ophiuroid species from the Yellow Sea, China. Other, the taxonomic groups with abundances less than 1%; Y, the nearshore environment; H, the offshore environment.
	FIGURE 3. Amplicon sequence variant (ASV) Venn diagram of gut microbiota of ophiuroids and alpha diversity analyses of the ophiuroid gut and sediment microbial communities. (A) ASVs of ophiuroids’ gut microbiota are depicted in a Venn diagram. Alpha diversity was calculated using (B) the Shannon index and (C) the Simpson index. Statistical analysis was conducted on alpha diversity using Mann–Whitney U tests. ns, not significant; p > 0.05. Y, the nearshore environment; H, the offshore environment.
	FIGURE 4. The heatmap of relative abundance of gut microbiota at the genus level (>1%) in ophiuroid species from the Yellow Sea. Y, the nearshore environment; H, the offshore environment.
	FIGURE 5. Principal component analysis (PCA) of gut microbiota in ophiuroids and sediment microbiome under genus level. Y, the nearshore environment; H, the offshore environment.
	FIGURE 6. Characterization of gut microbiota in ophiuroids by LEfSe analysis and histogram of the linear discriminant analysis (LDA) scores (log 10). Y, the nearshore environment; H, the offshore environment; g, the genus; f, the family; o, the order; c, the class; p, the phylum.
	FIGURE 7. The significant expression pathways based on (A) Tax4Fun and (B) PICRUSt analysis of gut microbial community between the nearshore and offshore Stegophiura sladeni at Kyoto Encyclopedia of Genes and Genomes level 2.
	FIGURE 8. Variation analysis of gut microbial community between nearshore environment ophiuroid species Stegophiura sladeni and Ophiopholis mirabilis at Kyoto Encyclopedia of Genes and Genomes level 2 by PICRUSt. Dotted line: division of p < 0.05.
	FIGURE 9. Variation analysis of gut microbial community between offshore environment ophiuroid species Stegophiura sladeni and Ophiura sarsii vadicola at Kyoto Encyclopedia of Genes and Genomes level 2 by PICRUSt. Dotted line: division of p < 0.05.
	FIGURE 10. Phylogenetic analysis of Candidatus Hepatoplasma. The percentage represented the relative abundance in Stegophiura sladeni at nearshore and offshore. The bootstrap values (>50%) of relevant nodes are shown based on 1,000 replicates. The two numbers on the branch were the result of the maximum likelihood (ML), with neighbor-joining (NJ) algorithm in brackets. Sequences from this study are shown in bold.