Adaptive radiation of chemosymbiotic deep-sea mussels.

Adaptive radiations present fascinating opportunities for studying the evolutionary process. Most cases come from isolated lakes or islands, where unoccupied ecological space is filled through novel adaptations. Here, we describe an unusual example of an adaptive radiation: symbiotic mussels that colonized island-like chemosynthetic environments such as hydrothermal vents, cold seeps and sunken organic substrates on the vast deep-sea floor. Our time-calibrated molecular phylogeny suggests that the group originated and acquired sulfur-oxidizing symbionts in the Late Cretaceous, possibly while inhabiting organic substrates and long before its major radiation in the Middle Eocene to Early Oligocene. The first appearance of intracellular and methanotrophic symbionts was detected only after this major radiation. Thus, contrary to expectations, the major radiation may have not been triggered by the evolution of novel types of symbioses. We hypothesize that environmental factors, such as increased habitat availability and/or increased dispersal capabilities, sparked the radiation. Intracellular and methanotrophic symbionts were acquired in several independent lineages and marked the onset of a second wave of diversification at vents and seeps. Changes in habitat type resulted in adaptive trends in shell lengths (related to the availability of space and energy, and physiological trade-offs) and in the successive colonization of greater water depths.

Bacterial communities associated with the wood-feeding gastropod Pectinodonta sp. (Patellogastropoda, Mollusca).

Even though their occurrence was reported a long time ago, sunken wood ecosystems at the deep-sea floor have only recently received specific attention. Accumulations of wood fragments in the deep sea create niches for a diverse fauna, but the significance of the wood itself as a food source remains to be evaluated. Pectinodonta sp. is a patellogastropod that exclusively occurs on woody substrates, where individuals excavate deep depressions, and is thus a potential candidate for a wood-eating lifestyle. Several approaches were used on Pectinodonta sampled close to Tongoa island (Vanuatu) to investigate its dietary habits. Host carbon is most likely derived from the wood material based on stable isotopes analyses, and high cellulase activity was measured in the digestive mass. Electron microscopy and FISH revealed the occurrence of two distinct and dense bacterial communities, in the digestive gland and on the gill. Gland-associated 16S rRNA gene bacterial phylotypes, confirmed by in situ hybridization, included members of three divisions (Alpha- and Gammaproteobacteria, Bacteroidetes), and were moderately related (90-96% sequence identity) to polymer-degrading and denitrifying bacteria. Gill-associated phylotypes included representatives of the Delta- and Epsilonproteobacteria. The possible involvement of these two bacterial communities in wood utilization by Pectinodonta sp. is discussed.

New insights into diversity and evolution of deep-sea Mytilidae (Mollusca: Bivalvia).

Bathymodiolinae mussels have been used as a biological model to better understand the evolutionary origin of faunas associated with deep-sea hydrothermal vents and cold seeps. Most studies to date, however, have sampled with a strong bias towards vent and seep species, mainly because of a lack of knowledge of closely related species from organic falls. Here we reassess the species diversity of deep-sea mussels using two genes and a large taxon sample from the South-Western Pacific. This new taxonomic framework serves as a basis for a phylogenetic investigation of their evolutionary history. We first highlight an unexpected allopatric pattern and suggest that mussels usually reported from organic falls are in fact poorly specialized with regard to their environment. This challenges the adaptive scenarios proposed to explain the diversification of the group. Second, we confirm that deep-sea mussels arose from organic falls and then colonized hydrothermal vents and cold seeps in multiple events. Overall, this study constitutes a new basis for further phylogenetic investigations and a global systematic revision of deep-sea mussels.

Symbioses between deep-sea mussels (Mytilidae: Bathymodiolinae) and chemosynthetic bacteria: diversity, function and evolution.

Mussels of the subfamily Bathymodiolinae thrive around chimneys emitting hot fluids at deep sea hydrothermal vents, as well as at cold seeps and on sunken organic debris (sunken wood, whale falls). Despite the absence of light-driven primary production in these deep-sea ecosystems, mussels succeed reaching high biomasses in these harsh conditions thanks to chemosynthetic, carbon-fixing bacterial symbionts located in their gill tissue. Since the discovery of mussel symbioses about three decades ago our knowledge has increased, yet new findings are published regularly regarding their diversity, role and evolution. This article attempts to summarize current knowledge about symbiosis in Bathymodiolinae, focusing on mussel species for which information is available regarding both hosts and symbionts. Moreover, new data obtained from small mussels inhabiting sunken woods around the Philippines are provided. Indeed, mussel species from organic falls remain poorly studied compared to their vent and seep relatives despite their importance for the understanding of the evolution of symbiosis in the subfamily Bathymodiolinae.

Several deep-sea mussels and their associated symbionts are able to live both on wood and on whale falls.

Bathymodiolin mussels occur at hydrothermal vents and cold seeps, where they thrive thanks to symbiotic associations with chemotrophic bacteria. Closely related genera Idas and Adipicola are associated with organic falls, ecosystems that have been suggested as potential evolutionary 'stepping stones' in the colonization of deeper and more sulphide-rich environments. Such a scenario should result from specializations to given environments from species with larger ecological niches. This study provides molecular-based evidence for the existence of two mussel species found both on sunken wood and bones. Each species specifically harbours one bacterial phylotype corresponding to thioautotrophic bacteria related to other bathymodiolin symbionts. Phylogenetic patterns between hosts and symbionts are partially congruent. However, active endocytosis and occurrences of minor symbiont lineages within species which are not their usual host suggest an environmental or horizontal rather than strictly vertical transmission of symbionts. Although the bacteria are close relatives, their localization is intracellular in one mussel species and extracellular in the other, suggesting that habitat choice is independent of the symbiont localization. The variation of bacterial densities in host tissues is related to the substrate on which specimens were sampled and could explain the abilities of host species to adapt to various substrates.

Unexpected co-occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp. (Bivalvia: Mytilidae).

Bathymodioline mussels occur in chemosynthesis-based ecosystems such as cold seeps, hydrothermal vents and organic debris worldwide. Their key adaptation to these environments is their association with bacterial endosymbionts which ensure a chemosynthetic primary production based on the oxidation of reduced compounds such as methane and sulfide. We herein report a multiple symbiosis involving six distinct bacterial 16S rRNA phylotypes, including two belonging to groups not yet reported as symbionts in mytilids, in a small Idas mussel found on carbonate crusts in a cold seep area located north to the Nile deep-sea fan (Eastern Mediterranean). Symbionts co-occur within hosts bacteriocytes based on fluorescence in situ hybridizations, and sequencing of functional genes suggests they have the potential to perform autotrophy, and sulfide and methane oxidation. Previous studies indicated the presence of only one or two symbiont 16S rRNA phylotypes in bathymodioline mussels. Together with the recent discovery of four bacterial symbionts in the large seep species Bathymodiolus heckerae, this study shows that symbiont diversity has probably been underestimated, and questions whether the common ancestor of bathymodioline mussels was associated with multiple bacteria.

Molecular phylogeny in mytilids supports the wooden steps to deep-sea vents hypothesis.

Molecular data were used to study the diversity of mytilids associated with sunken-woods sampled in the Solomon Islands and discuss the 'wooden steps to deep-sea vent' hypothesis proposed by Distel et al. First, COI data used in a barcoding approach confirm the presence of four distinct species. Analyses of the 18S rDNA and COI dataset then confirmed that these sunken-wood mytilids belonged to a monophyletic group including all species from deep-sea reducing environments. Finally, we analyzed the relationships within this monophyletic group that include the Bathymodiolinae using a COI dataset and a combined analysis of mitochondrial COI and ND4 genes and nuclear rDNA 18S and 28S. Our study supported the 'wooden steps to deep-sea vent' hypothesis: one of the sunken-wood species had a basal position within the Bathymodiolionae, and all described vent and seep mussels included in our analyses were derived taxa within Bathymodiolinae.