Metabolic and physiological interdependencies in the Bathymodiolus azoricus symbiosis

Abstract

The hydrothermal vent mussel Bathymodiolus azoricus lives in an intimate symbiosis with two types of chemosynthetic Gammaproteobacteria in its gills: a sulfur oxidizer and a methane oxidizer. Despite numerous investigations over the last decades, the degree of interdependence between the three symbiotic partners, their individual metabolic contributions, as well as the mechanism of carbon transfer from the symbionts to the host are poorly understood. We used a combination of proteomics and genomics to investigate the physiology and metabolism of the individual symbiotic partners. Our study revealed that key metabolic functions are most likely accomplished jointly by B. azoricus and its symbionts: (1) CO2 is pre-concentrated by the host for carbon fixation by the sulfur-oxidizing symbiont, and (2) the host replenishes essential biosynthetic TCA cycle intermediates for the sulfur-oxidizing symbiont. In return (3), the sulfur oxidizer may compensate for the host's putative deficiency in amino acid and cofactor biosynthesis. We also identified numerous ‘symbiosis-specific' host proteins by comparing symbiont-containing and symbiont-free host tissues and symbiont fractions. These proteins included a large complement of host digestive enzymes in the gill that are likely involved in symbiont digestion and carbon transfer from the symbionts to the host.

The evolution of host-symbiont dependence

“…In marine systems, horizontal acquisition of symbionts from surrounding sea water is common, as seen in Bathymodiolus mussels, but hosts may still rely on symbionts for fundamental needs, such as nutrition1930.…”

Sulfur-oxidizing symbionts without canonical genes for autotrophic CO2fixation

“…This is metabolically demanding, and it is telling that the bathymodioline and vesicomyid bivalves, whose symbionts have the most autotrophic features, are relatively large animals with intracellular symbionts that are located in their gill tissues, which can better maintain ventilation and homeostasis than smaller hosts that have extracellular symbionts. Specialization for high autotrophic production rates is also seen in the pre-concentration of CO 2 by the bivalve Bathymodiolus azoricus for its symbionts, and in its thiotrophic symbiont's metabolic dependence on the animal to replenish TCA cycle intermediates (56).…”

Genomic Evidence that Methanotrophic Endosymbionts Likely Provide Deep-Sea Bathymodiolus Mussels with a Sterol Intermediate in Cholesterol Biosynthesis

“…Although Bathymodiolus species are considered to largely depend on these endosymbionts for nutrition, our knowledge regarding how the biochemical pathways of these host mussels and bacterial symbionts are interwoven is very limited (although Ponnudurai et al 2017 recently analyzed the comprehensive metabolic interaction in the symbiosis of B . azoricus ).…”