Chemosymbiotic lucinid clams modify the physical, chemical and biological characteristics of marine sediments globally

Chemosynthetic symbioses are widespread throughout marine benthic ecosystems. Through the combined metabolic activity of the symbionts and their animal hosts, they alter the sediment’s available nutrients, affecting the surrounding biological communities from microbes to seagrasses. The chemosymbiotic bivalve family Lucinidae is a remarkable example.  Lucinidae is one of the most species-rich animal families in the oceans today, with more than 400 species described. They can be found worldwide from the tropics to the poles, and can reach abundances of more than 4000 individuals per square meter of sediment. All Lucinids detoxify sediments of hydrogen sulfide and one particular species, Loripes orbiculatus, which associates with a sulfur-oxidizing symbiont, Candidatus Thiodiazotropha endoloripes, has been shown to release nitrogen compounds into the surrounding environment (Cardini et al., ISME J 2019). The symbionts of all Lucinidae, including Loripes orbiculatus, are acquired from their surrounding environment during the animal’s development, termed horizontal transmission. Although a substantial environmental population must be present for the symbiosis to persist across generations, we know very little about the environmental reservoir of horizontally transmitted symbionts, as surprisingly, symbionts are rarely, if ever, detected in surveys of sediment microbial communities. We hunted for the free-living symbionts in habitats surrounding the lucinid species Loripes orbiculatus and its symbiont, Candidatus Thiodiazotropha endoloripes, in Fetovaia Bay, Elba, Italy. Symbionts in the environment may have been previously overlooked in molecular surveys of bulk sediment, thus, we did targeted sampling of distinct environmental microhabitats including porewater and sediment. There was little evidence for an environmental symbiont population in Fetovaia Bay. Extensive 16S rRNA amplicon surveys of sediment samples found that less than 0.05% of the bacterial population belong to the Sedimeticolaceae family, which contains Candidatus Thiodiazotropha and other lucinid symbionts, and none of the 400,000 sequences we analyzed matched the symbiont’s 16S rRNA sequence. Given the absence of detectable symbionts in sediment, we considered it possible that lucinid clams engineer an environment to ‘farm’ symbionts through their sulfide mining and general burrowing activities. We therefore assessed the microbial communities in the mucus-lined burrow walls of the bivalves with molecular methods. In contrast to the surrounding sediment, ~10% of operational taxonomic units (OTUs) found in the mucus tubes created by lucinid clams were Sedimenticolaceae, and sequences matching the genus Candidatus Thiodiazotropha could be detected. The enrichment of Sedimenticolaceae in the mucus tubes created by Loripes orbiculatus suggests that the clams create an environment more suitable for Sedimenticolaceae than the ‘background’ surrounding sediment. This suggests that the population of available symbionts is environmental, but only detectable in lucinid-associated or modified environments such as the burrow walls. Considering their worldwide distribution and enormous abundance at some locations, lucinid clams and their chemosynthetic symbionts potentially have an enormous impact on structuring microbial communities in marine sediments globally, both indirectly by altering carbon, nitrogen and sulfur cycling, and directly by selecting for certain microbial groups.