Mixotrophy in the deep sea: a dual endosymbiotic hydrothermal mytilid assimilates dissolved and particulate organic matter

Abstract

Bathymodiolus azoricus mussels thrive 840 to 2300 m deep at hydrothermal vents of the Azores Triple Junction on the Mid-Atlantic Ridge. Although previous studies have suggested a mixotrophic regime for this species, no analysis has yet yielded direct evidence for the assimilation of particulate material. In the present study, tracer experiments in aquaria with 13 C-and 15 N-labelled amino acids and marine cyanobacteria demonstrate for the first time the incorporation of dissolved and particulate organic matter in soft tissues of vent mussel. The observation of phytoplanktonic tests in wild mussel stomachs highlights the occurrence of in situ ingestion of sea-surface-derived material. Particulate organic carbon fluxes in sediment traps moored away from direct vent influence are in agreement with carbon export estimates from the surface ocean above the vents attenuated by microbial degradation. Stable isotope composition of trapped organic matter is similar to values published in the literature, but is enriched by + 7 ‰ in 13 C and +13 ‰ in 15 N, relative to mussel gill tissue from the Menez Gwen vent. Although this observation suggests a negligible contribution of photosynthetically produced organic matter to the diet of B. azoricus, the tracer experiments demonstrate that active suspension-feeding on particles and dissolved organic matter could contribute to the C and N budget of the mussel and should not be neglected.

Tracing carbon assimilation in endosymbiotic deep-sea hydrothermal vent Mytilid fatty acids by <sup>13</sup>C-fingerprinting

“…While from the present study (and Riou et al, 2008) it is now clear that B. azoricus' symbionts assimilate CH 4 or HCO − 3 in the presence of H 2 S, their potential for osmotrophy has never been studied. The gill tissue showed the most rapid evidence of 13 C incorporation from labeled amino acids (Riou et al, 2010). Since the symbionts are located in the gill tissue, they might thus have increased access to such organic food source.…”

“…The available quantity of labelled methane (25% 13 C) allowed running the tracer experiment with 13 CH 4 for a period of 15 days with a final dissolved concentration ranging between 14-200 µmol L −1 (Riou et al, 2008). The control experiment (with filtered seawater only) and the experiments with NaH 13 CO 3 (99% added to the filtered seawater to obtain a concentration of 2.85 mmol L −1 , 16.3% 13 C) + H 2 S (0-32 µmol L −1 , Riou et al, 2008) or with 9 mg L −1 of a 13 C-labeled amino acid mixture (98% 13 C, Riou et al, 2010) were continued over a period of 20 days. The amino acid mixture consisted of Gly 20-25%, Ala 15-20%, Tyr 10-15%, Leu 5-10%, Lys 5-10%, Ser 5-10%, Thr 2-5%, Phe 1-5%, Pro 1-5%, Val 1-5%, Met <3%, Trp <1%, Ile <1%, His <1%.…”

“…Bodelier et al, 2009Sorokin et al, 2007 12:0 X 3.9 14:0 X 2.5 X 0.5 15:0 X 1.5 X 0.6 16:0 X 14.5 X 25.4 18:0 X 0 X 0.5 16:1(n − 6) X 17.5 16:1(n − 7)c+t X 20 X 27.3 16:1(n − 8) X 39 16:1(n − 9) X 0 17:1(n − 8) X 0.9 18:1(n − 7)c+t X 1.5 X 11.8 18:1(n − 8) X 0 18:1(n − 9) X 0.5 X 5.1 18:1(n − 13)c+t X 0 20:1(n − 7) X 0 18:2(n − 7) X 0 tryptophan and tyrosine (accounting for 41 to 72% of the 13 C-amino acid mix used in our tracer experiment, see Riou et al, 2010) can be degraded into acetoacetyl CoenzymeA or acetyl-CoA, which constitutes the basis for de novo FA biosynthesis (e.g., Payne et al, 2001). Alanine, serine and cysteine can be converted to pyruvate which can further turn into acetyl CoA.…”

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

“…This confirms that multiple symbioses are highly adaptable to changing habitats, both in time and space, optimizing the use of resources. In Bathymodiolus, heterotrophy plays a limited role, but a fraction of carbon is derived from particulate and dissolved organic matter at shallower sites, as seen for B. azoricus at the 800 m deep Menez Gwen site (Riou et al, 2010), or during early life (Martins et al, 2008).…”

Phylogenetic relationships of hydrothermal vent mussels (Bathymodiolinae) and their symbionts

“…This cosmopolitan distribution may be attributed to their nutritional flexibility, in that they are capable of obtaining nutrition from filter feeding (Page et al 1991, Riou et al 2010a supplementary to nutrition obtained from single or dual symbioses with sulfide-oxidizing (thiotrophic) and methanotrophic bacteria (Distel et al 1995, DeChaine & Cavanaugh 2006, Duperron et al 2006). This mixotrophic lifestyle may allow bathymodiolines to survive fluctuations in energy sources more effectively than other invertebrate symbioses, which in turn may facilitate a broader environmental range (Distel et al 1995).…”