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Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species.

ABSTRACT: Lucinidae clams harbor gammaproteobacterial thioautotrophic gill endosymbionts that are environmentally acquired. Thioautotrophic lucinid symbionts are related to metabolically similar symbionts associated with diverse marine host taxa and fall into three distinct phylogenetic clades. Most studies on the lucinid-bacteria chemosymbiosis have been done with seagrass-dwelling hosts, whose symbionts belong to the largest phylogenetic clade. In this study, we examined the taxonomy and functional repertoire of bacterial endosymbionts at an unprecedented resolution from Phacoides pectinatus retrieved from mangrove-lined coastal sediments, which are underrepresented in chemosymbiosis studies. The P. pectinatus thioautotrophic endosymbiont expressed metabolic gene variants for thioautotrophy, respiration, and nitrogen assimilation distinct from previously characterized lucinid thioautotrophic symbionts and other marine symbionts. At least two other bacterial species with different metabolisms were also consistently identified in the P. pectinatus gill microbiome, including a Kistimonas-like species and a Spirochaeta-like species. Bacterial transcripts involved in adhesion, growth, and virulence and mixotrophy were highly expressed, as were host-related hemoglobin and lysozyme transcripts indicative of sulfide/oxygen/CO₂ transport and bactericidal activity. This study suggests the potential roles of P. pectinatus and its gill microbiome species in mangrove sediment biogeochemistry and offers insights into host and microbe metabolisms in the habitat.

SUBMITTER: Lim SJ

PROVIDER: S-EPMC6461927 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The present study compared the taxonomic diversity and evaluated the functional attributes of the bacterial species from Mandovi and Zuari mangrove sediments, Goa, using paired-end amplicon sequencing of 16S rDNA and culture-based analyses, respectively. 16S rDNA sequencing revealed Proteobacteria, Firmicutes, and Actinobacteria as the dominant phyla in both the sediments. However, the abundance of these phyla significantly differed between the samples. Bacteroidetes from Mandovi sediment, and Acidobacteria and Gemmatimonadetes from Zuari sediment were the other exclusive major phyla. Chloroflexi, Cyanobacteria, Nitrospirae, Planctomycetes, Verrucomicrobia, and WS3 were the minor phyla observed in both. However, a significant difference in the distribution of minor phyla and lower bacterial taxa under each phylum was noted between the sediments, indicating that the resident microbial flora completely differed between them. This was further validated by high values from distance matrix analyses between the samples. In addition, the pathogenic Vibrio sp. was recorded exclusively in Mandovi sediment, while higher abundance of ecologically important bacterial classes including Gammaproteobacteria, Alphaproteobacteria, Deltaproteobacteria, and Bacilli was observed in Zuari sediment. Taken together, the data indicated that Zuari sediment was taxonomically richer than Mandovi sediment, while a greater incidence of anthropogenic activities occurred in the latter. This observation was further validated by non-parametric richness estimators which were found to be higher for Zuari sediment. The cultured bacterial isolates, all identified as Firmicutes, were tested for activities related to biofertilization and production of enzymes to be used for bioremediation and chemotherapeutic applications. Higher number of bacterial isolates from Mandovi was found to produce indole-acetic-acid, tannase, xylanase, and glutaminase enzymes, and could solubilize phosphate. In contrast, higher proportion of bacterial isolates from Zuari sediment were capable of producing amylase, cellulase, gelatinase, laccase, lipase, protease, and asparaginase enzymes, emphasizing the fact that the Zuari mangrove sediment is a rich reservoir for economically and biotechnologically important bacterial species.

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Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species.

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