Metabolic handoffs between multiple symbionts may benefit the deep-sea bathymodioline mussels

Abstract

Bathymodioline mussels rely on thiotrophic and/or methanotrophic chemosynthetic symbionts for nutrition, yet, secondary heterotrophic symbionts are often present and play an unknown role in the fitness of the organism. The bathymodioline Idas mussels that thrive in gas seeps and on sunken wood in the Mediterranean Sea and the Atlantic Ocean, host at least six symbiont lineages that often co-occur. These lineages include the primary symbionts chemosynthetic methane- and sulfur-oxidizing gammaproteobacteria, and the secondary symbionts, Methylophagaceae, Nitrincolaceae and Flavobacteriaceae, whose physiology and metabolism are obscure. Little is known about if and how these symbionts interact or exchange metabolites. Here we curated metagenome-assembled genomes of Idas modiolaeformis symbionts and used genome-centered metatranscriptomics and metaproteomics to assess key symbiont functions. The Methylophagaceae symbiont is a methylotrophic autotroph, as it encoded and expressed the ribulose monophosphate and Calvin-Benson-Bassham cycle enzymes, particularly RuBisCO. The Nitrincolaceae ASP10-02a symbiont likely fuels its metabolism with nitrogen-rich macromolecules and may provide the holobiont with vitamin B12. The Urechidicola (Flavobacteriaceae) symbionts likely degrade glycans and may remove NO. Our findings indicate that these flexible associations allow for expanding the range of substrates and environmental niches, via new metabolic functions and handoffs.

Metabolically-versatile Ca. Thiodiazotropha symbionts of the deep-sea lucinid clam Lucinoma kazani have the genetic potential to fix nitrogen

“…The bona fide chemosynthetic symbionts often co-occur with other microbes that can use small organic compounds as energy and carbon sources, expanding the range of substrates that fuel these symbioses. For example, Cycloclasticus use short-chain alkanes in Bathymodiolus heckerae and Methylophaga methylotrophs sustain growth using methanol, a byproduct of methane oxidation [ 9 , 10 ].…”

Animal burrowing at cold seep ecotones boosts productivity by linking macromolecule turnover with chemosynthesis and nutrient cycling

“…Our results suggest the presence of productive burrow communities, that cycle carbon, sulfur and nitrogen, potentially 465 through the turnover of hydrogen or other fermentation products. Examples of similar communities, comprising Bacteroidota degraders of macromolecules, sulfate reducers (Desulfobacterota and others), and chemotrophs (mainly Campylobacteria and Gammaproteobacteria) are common among a wide range of biomes, including burrowed sediments (Fang et al, 2023), epibionts of invertebrates in chemosynthetic habitats (Xu et al, 2022;Bai et al, 2021) and endosymbiotic communities in Idas mussels (Zvi-Kedem et al, 2023). The interactions between these organisms are not 470 limited to the exchange of key metabolites (Zoccarato et al, 2022).…”