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.
Highlights
IntroductionChemosymbiosis is widespread in marine habitats, where endosymbiotic or episymbiotic chemolithoautotrophs use inorganic chemical energy for the synthesis of organic compounds that benefit their hosts [1, 2]
Electronic supplementary material The online version of this article contains supplementary material, which is available to authorized users.Chemosymbiosis is widespread in marine habitats, where endosymbiotic or episymbiotic chemolithoautotrophs use inorganic chemical energy for the synthesis of organic compounds that benefit their hosts [1, 2]
Live P. pectinatus had clumped distributions at Wildcat Cove in all sample years, with the highest concentrations being near the mangrove-lined coast where total organic carbon content in the sediment was highest [26]
Summary
Chemosymbiosis is widespread in marine habitats, where endosymbiotic or episymbiotic chemolithoautotrophs use inorganic chemical energy for the synthesis of organic compounds that benefit their hosts [1, 2]. Despite being capable of suspension feeding, all living lucinids studied to date fulfill a considerable proportion of their nutritional needs through obligate chemosymbiotic associations with gammaproteobacterial endosymbionts occupying bacteriocytes in their gills [3]. Lucinid species examined so far acquire their thioautotrophic endosymbionts from free-living environmental bacterial populations [5,6,7,8,9]. Stable isotope analyses, and clone-based amplicon sequencing methods demonstrate that lucinid endosymbionts mainly use energy derived from the oxidation of reduced sulfur compounds to fix inorganic carbon for their hosts [10]. Other reported functions of Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid
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