Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups

Abstract

In the ocean, most hosts acquire their symbionts from the environment. Due to the immense spatial scales involved, our understanding of the biogeography of hosts and symbionts in marine systems is patchy, although this knowledge is essential for understanding fundamental aspects of symbiosis such as host–symbiont specificity and evolution. Lucinidae is the most species-rich and widely distributed family of marine bivalves hosting autotrophic bacterial endosymbionts. Previous molecular surveys identified location-specific symbiont types that “promiscuously” form associations with multiple divergent cooccurring host species. This flexibility of host–microbe pairings is thought to underpin their global success, as it allows hosts to form associations with locally adapted symbionts. We used metagenomics to investigate the biodiversity, functional variability, and genetic exchange among the endosymbionts of 12 lucinid host species from across the globe. We report a cosmopolitan symbiont species, Candidatus Thiodiazotropha taylori, associated with multiple lucinid host species. Ca. T. taylori has achieved more success at dispersal and establishing symbioses with lucinids than any other symbiont described thus far. This discovery challenges our understanding of symbiont dispersal and location-specific colonization and suggests both symbiont and host flexibility underpin the ecological and evolutionary success of the lucinid symbiosis.

Chemoautotrophy, symbiosis and sedimented diatoms support high biomass of benthic molluscs in the Namibian shelf

“…Stable isotopic analysis (SIA) has been widely used to study the trophic interactions of marine benthic communities 19 , 21 – 23 , and is a powerful tool for detecting nutrient sources and tracing nutrient exchanges in chemoautotrophic associations 24 – 26 . For example, the bulk δ 13 C values of chemosymbiotic lucinids (− 37‰ to − 23‰) 27 – 31 are approximately within the bulk δ 13 C range expected when a large proportion of their carbon is derived from autotrophy with the CO 2 -fixing enzyme Rubisco I (− 35‰ to − 27‰) 24 . In contrast, non-symbiotic benthic organisms typically have δ 13 C values between − 20 and − 16‰ 29 , 32 .…”

“…** These genes were only present in the high-quality MAGs of Ca . T. taylori associated with Stewartia floridana, from Florida, USA 13 .…”

“… Metagenomic data for all shallow-water lucinid symbionts reproduced from Osvatic et al 13 . +Gene(s) within the pathway were present in all the high-quality MAGs.…”

“…Quality filtering, genome assembly, and bacterial genome binning were carried out using the scripts and workflow previously described by Osvatic et al 13 . Only MAGs with over 90% completion (CheckM gammaproteobacterial gene set) and lower than 5% contamination were kept in subsequent downstream analysis.…”

“…Members of the bivalve family Lucinidae have a global distribution and all species studied thus far form a nutritional symbiosis with environmentally acquired sulfur-oxidizing gammaproteobacteria, which may also play an important role in detoxifying hydrogen sulfide for their host 7 – 9 . Most shallow-water lucinids studied to date host symbionts from the genus Candidatus Thiodiazotropha 10 – 13 , with the exception of the mangrove lucinid Phacoides pectinatus which hosts a symbiont from the genus Sedimenticola 14 . In addition to the oxidation of reduced sulfur compounds, like hydrogen sulfide, and carbon fixation, all the various Ca.…”