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

Abstract

Bathymodioline mussels rely on thiotrophic and 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, including the primary, chemosynthetic methane- and sulfur-oxidizing gammaproteobacteria, and the secondary Methylophagaceae, Nitrincolaceae and Flavobacteraceae symbionts, whose physiology and metabolism are obscure. Little is known about whether 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 Flavobacteriaceae Urechidicola 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.

Methane Anaerobic Oxidation on Carbonate in Cold Seep Environments with High-Pressure Enrichment Cultivation

“…Therefore, the lack of this vitamin may hinder DNA synthesis, methionine regeneration, and result in the accumulation of homocysteine. The ability of Nitrincolaceae to synthesize vitamin B12 may be crucial for the majority of symbiotic dependency on it [12]. In the in vitro cultivation process under different environmental conditions, temperature has been identified as a primary parameter influencing the AOM rates of ANME-1 and ANME-2 consortia, in contrast to variations in sulfate concentration, pH, and salinity [13].…”

“…Approximately 10-20% of the methane oxidized by AOM in cold-seep environments is incorporated into authigenic deposits [2,3]. It is estimated that these deposits account for 11-15% of carbonate accumulation in continental shelf sediments annually (11)(12)(13)(14)(15) Tmol yr-1) [4].…”

Metabolically-versatileCa.Thiodiazotropha symbionts of the deep-sea lucinid clamLucinoma kazanihave 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. For example, Cycloclasticus use short-chain alkanes in Bathymodiolus heckerae and Methylophaga methylotrophs sustain growth using methanol, a byproduct of methane oxidation [9, 10].…”