Dataset Information

Host-symbiont interactions in the chemosynthetic Riftia model symbiosis

ABSTRACT: The deep-sea tubeworm Riftia pachyptila is a model system for a mutualistic association: The adult worm has no digestive system, but completely relies on one phylotype of endosymbiotic chemosynthetic bacteria for nutrition. The bacteria, in turn, are provisioned by the host. Metabolism and physiology of this symbiosis, particularly of the uncultured symbiont, have been subject to various studies. Yet, how both partners interact on the molecular level remains largely unknown. To study these host-symbiont interactions in detail, we sequenced the R. pachyptila host transcriptome de novo, and conducted comprehensive metaproteomic comparisons of symbiont-containing and symbiont-free R. pachyptila tissues under energy-rich and energy-limiting conditions. Our results demonstrate that R. pachyptila invests a considerable part of its proteome to provision the symbionts with inorganic compounds. It acquires symbiont-derived biomass primarily by digesting parts of the symbiont population. The R. pachyptila immune system apparently not only protects the holobiont from pathogens, but is also involved in symbiont population control. The symbiont expresses a repertoire of proteins dedicated to communication with the host, including eukaryote-like proteins that may counteract phagocytosis. During energy limitation, i.e., when reduced sulfur compounds are lacking, the host apparently increases symbiont digestion. We show here an intricate network of interaction pathways that shapes the R. pachyptila holobiont. Together with the metabolic flexibility of the association under varying energy conditions, this probably forms the basis for the success of this tight association under the highly challenging deep-sea conditions.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Candidatus Endoriftia Persephone Riftia Pachyptila

SUBMITTER: Tjorven Hinzke

LAB HEAD: Manuel Kleiner

PROVIDER: PXD012439 | Pride | 2019-11-25

REPOSITORIES: Pride

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Publications

Host-Microbe Interactions in the Chemosynthetic Riftia pachyptila Symbiosis.

Hinzke Tjorven T Kleiner Manuel M Breusing Corinna C Felbeck Horst H Häsler Robert R Sievert Stefan M SM Schlüter Rabea R Rosenstiel Philip P Reusch Thorsten B H TBH Schweder Thomas T Markert Stephanie S

mBio 20191217 6

The deep-sea tubeworm Riftia pachyptila lacks a digestive system but completely relies on bacterial endosymbionts for nutrition. Although the symbiont has been studied in detail on the molecular level, such analyses were unavailable for the animal host, because sequence information was lacking. To identify host-symbiont interaction mechanisms, we therefore sequenced the Riftia transcriptome, which served as a basis for comparative metaproteomic analyses of symbiont-containing versu ...[more]

PMID: 31848270

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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.

Dataset Information

Host-symbiont interactions in the chemosynthetic Riftia model symbiosis

Publications

Host-Microbe Interactions in the Chemosynthetic <i>Riftia pachyptila</i> Symbiosis.

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