A sad tale: has the small mussel Idas argenteus lost its symbionts?

Idas argenteus (Bivalvia: Mytilidae) belongs to a genus of mussels that are often associated with sunken wood and vertebrate bones in the deep sea. By contrast to other species currently included within the genus Idas and other related genera, such as Bathymodiolus, I. argenteus was documented to lack chemosynthetic symbionts bacterial symbionts in its gills. In the present study, new specimens are assigned to I. argenteus based on shell and soft parts analysis. Molecular data confirm the absence or low abundance of symbionts. Phylogeny based on five genes indicates that the symbiont-bearing I. washingtonius is the closest relative of I. argenteus. Symbiosis loss or extreme reduction is thus inferred to have occurred subsequent to the speciation event, 11–13 Mya. This is the first report of a loss of symbiosis within the clade of deep-sea chemosynthetic mussels.

An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea

Deep-sea bivalves found at hydrothermal vents, cold seeps and organic falls are sustained by chemosynthetic bacteria that ensure part or all of their carbon nutrition. These symbioses are of prime importance for the functioning of the ecosystems. Similar symbioses occur in other bivalve species living in shallow and coastal reduced habitats worldwide. In recent years, several deep-sea species have been investigated from continental margins around Europe, West Africa, eastern Americas, the Gulf of Mexico, and from hydrothermal vents on the Mid-Atlantic Ridge. In parallel, numerous, more easily accessible shallow marine species have been studied. Herein we provide a summary of the current knowledge available on chemosymbiotic bivalves in the area ranging west-to-east from the Gulf of Mexico to the Sea of Marmara, and north-to-south from the Arctic to the Gulf of Guinea. Characteristics of symbioses in 53 species from the area are summarized for each of the five bivalve families documented to harbor chemosynthetic symbionts (Mytilidae, Vesicomyidae, Solemyidae, Thyasiridae and Lucinidae). Comparisons are made between the families, with special emphasis on ecology, life cycle, and connectivity. Chemosynthetic symbioses are a major adaptation to ecosystems and habitats exposed to reducing conditions. However, relatively little is known regarding their diversity and functioning, apart from a few “model species” on which effort has focused over the last 30 yr. In the context of increasing concern about biodiversity and ecosystems, and increasing anthropogenic pressure on oceans, we advocate a better assessment of the diversity of bivalve symbioses in order to evaluate the capacities of these remarkable ecological and evolutionary units to withstand environmental change.

Biogeochemical measurements associated to deep-sea wood falls

Large organic food falls to the deep sea - such as whale carcasses and wood logs - support the development of reduced, sulfidic niches in an otherwise oxygenated, oligotrophic deep-sea environment. These transient hot spot ecosystems may serve the dispersal of highly adapted chemosynthetic organisms such as thiotrophic bivalves and siboglinid worms. Here we investigated the biogeochemical and microbiological processes leading to the development of sulfidic niches. Wood colonization experiments were carried out for the duration of one year in the vicinity of a cold seep area in the Nile deep-sea fan (Eastern Mediterranean) at depths of 1690 m. Wood logs were deployed in 2006 during the BIONIL cruise (RV Meteor M70/2 with ROV Quest, Marum, Germany) and sampled in 2007 during the Medeco-2 cruise (RV Pourquoi Pas? with ROV Victor 6000, Ifremer, France). Wood-boring bivalves played a key role in the initial degradation of the wood, the dispersal of wood chips and fecal matter around the wood log, and the provision of colonization surfaces to other organisms. Total oxygen uptake measured with a ROV-operated benthic chamber module was higher at the wood (0.5 m away) in contrast to 10 m away at a reference site (25 mmol m-2 d-1 and 1 mmol m-2 d-1, respectively), indicating an increased activity of sedimentary communities around the wood falls. Bacterial cell numbers associated with wood increased substantially from freshly submerged wood to the wood chip/fecal matter layer next to the wood experiments, as determined with Acridine Orange Direct Counts (AODC) and DAPI-stained counts. Microsensor measurements of sulfide, oxygen and pH were conducted ex situ. Sulfide fluxes were higher at the wood experiments when compared to reference measurements (19 and 32 mmol m-2 d-1 vs. 0 and 16 mmol -2 d-1, respectively). Sulfate reduction (SR) rates at the wood experiments were determined in ex situ incubations (1.3 and 2.0 mmol m-2 d-1) and fell into the lower range of SR rates previously observed from other chemosynthetic habitats at cold seeps. There was no influence of wood deposition on phosphate, silicate and nitrate concentrations, but ammonium concentrations were elevated at the wood chip-sediment boundary layer. Concentrations of dissolved organic carbon were much higher at the wood experiments (wood chip-sediment boundary layer) in comparison to measurements at the reference sites, which may indicate that cellulose degradation was highest under anoxic conditions and hence enabled by anaerobic benthic bacteria, e.g. fermenters and sulfate reducers. Our observations demonstrate that, after one year, the presence of wood at the seafloor had led to the creation of sulfidic niches, comparable to what has been observed at whale falls, albeit at lower rates.