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Metabolic differences between morphologically distinct symbiont populations in the tubeworm Riftia pachyptila

ABSTRACT: The endosymbiont population of the hydrothermal vent tube worm Riftia pachyptila consists of a single 16S phylotype of sulfur-oxidizing gammaproteobacteria. The intracellular symbiont exhibits remarkable morphological heterogeneity, from small rod-shaped or coccoid cells to large cocci, which were suggested to be part of a common cell cycle. To assess whether these morphological differences are accompanied by distinct metabolic profiles, we physically enriched individual symbiont cells sizes by density gradient centrifugation and subjected these enrichments to metaproteomic analysis and statistical evaluation using clustering and random forests. Unlike previous molecular studies, which examined the metabolism of the symbiont population as whole, we were thus able to unravel comprehensive protein abundance patterns of individual symbiont subpopulations. Supported by microscopic analyses, our metaproteomic results show that Riftia symbiont cells of different sizes are stages of a physiological differentiation process: Small symbionts actively divide and may establish cellular symbiont-host interaction, as indicated by highest abundance of the cell division key protein FtsZ and highly abundant chaperones and porins in this initial phase. We furthermore present evidence that large symbionts, on the other hand, do not divide, but still replicate DNA, leading to DNA endoreduplication. Highest abundance of enzymes for CO2 fixation, carbon storage and biosynthesis indicates that in its late differentiation stage, the symbiont’s metabolism is efficiently geared on the production of organic material. We propose that this symbiont aging process enhances the productivity of the symbiosis as a whole.

OTHER RELATED OMICS DATASETS IN: PRJEB13047

INSTRUMENT(S): LTQ Orbitrap Velos

ORGANISM(S): Candidatus Endoriftia Persephone Riftia Pachyptila

SUBMITTER: Tjorven Hinzke

LAB HEAD: Stephanie Markert

PROVIDER: PXD016986 | Pride | 2020-12-21

REPOSITORIES: Pride

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Project description:Bathymodiolus mussels inhabiting deep-sea hydrothermal vents harbor bacterial symbionts in their gills, which support the animals’ diet. While the basic mechanisms of energy generation and CO2 fixation that drive these symbioses are largely established, details of molecular interactions between the symbiotic partners and adaptations to their respective habitats remain unknown. In this study, we therefore comparatively examined the genomes and proteomes of two Bathymodiolus hosts and their respective symbionts from different geographical locations. Two mussel species were proteomically compared: i) B. thermophilus mussel containing sulfur-oxidizing symbiont from the east pacific rise. thermophilus and ii) B. azoricus containing thiotrophic and methanotrophic symbionts from the mid-atlantic ridge. Symbionts (for both species) and host components (for B. azoricus) were selectively enriched using a multi-step centrifugation procedure. Enriched host and symbiont fractions along with unenriched gill foot tissue were subject to in-depth semi-quantitative proteomic analyses using the orbitrap and velos mass spectrometers. Proteins were quantified based on their spectral counts using the normalized spectral abundance factor (NSAF) method. We identified common strategies of metabolic interactions that provide mutual nutritional support between host and symbionts, such as the detoxification of ambient sulfide by the Bathymodiolus host, which provides a stable thiosulfate reservoir for the thiotrophic symbionts, and a putative amino acid cycling mechanism that could supply the host with symbiont-derived amino acids. A suite of genes and proteins putatively related to virulence or defense functions was particularly abundant in the B. thermophilus symbiont, compared to its symbiont relatives, and may pose a host species-specific adaptation. Our results reveal both, a high degree of integration between the symbiotic partners, and great potential to adapt to the prevailing environment, which facilitate the holobiont’s survival in its hydrothermal vent habitat.

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Metabolic differences between morphologically distinct symbiont populations in the tubeworm Riftia pachyptila

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