Gene loss and symbiont switching during adaptation to the deep sea in a globally distributed symbiosis

Abstract

Chemosynthetic symbioses between bacteria and invertebrates occur worldwide from coastal sediments to the deep sea. Most host groups are restricted to either shallow or deep waters. In contrast, Lucinidae, the most species-rich family of chemosymbiotic invertebrates, has both shallow- and deep-sea representatives. Multiple lucinid species have independently colonized the deep sea, which provides a unique framework for understanding the role microbial symbionts play in evolutionary transitions between shallow and deep waters. Lucinids acquire their symbionts from their surroundings during early development, which may allow them to flexibly acquire symbionts that are adapted to local environments. Via metagenomic analyses of museum and other samples collected over decades, we investigated the biodiversity and metabolic capabilities of the symbionts of 22 mostly deep-water lucinid species. We aimed to test the theory that the symbiont played a role in adaptation to life in deep-sea habitats. We identified 16 symbiont species, mostly within the previously described genus Ca. Thiodiazotropha. Most genomic functions were shared by both shallow-water and deep-sea Ca. Thiodiazotropha, though nitrogen fixation was exclusive to shallow-water species. We discovered multiple cases of symbiont switching near deep-sea hydrothermal vents and cold seeps, where distantly related hosts convergently acquired novel symbionts from a different bacterial order. Finally, analyses of selection revealed consistently stronger purifying selection on symbiont genomes in two extreme habitats - hydrothermal vents and an oxygen-minimum zone. Our findings reveal that shifts in symbiont metabolic capability and, in some cases, acquisition of a novel symbiont accompanied adaptation of lucinids to challenging deep-sea habitats.

Sulfur oxidation and reduction are coupled to nitrogen fixation in the roots of a salt marsh foundation plant species

“…Thiodiazotropha spp. analyzed by Osvatic et al (2023). A maximum-likelihood phylogenetic tree using a 400 universal marker genes database was performed in PhyloPhlAn.…”

“…Publicly available genomes from all species from the Sedimenticolaceae family, according to GTDB R07-RS207, and all Candidatus Thiodiazotropha genomes from the Osvatic et al (2023) study were retrieved from NCBI. A full list and characteristics of genomes used for this analysis is found in Supplementary Table S11.…”

“…Thiodiazotropha genus was first discovered as bacterial symbionts of lucinid clams, where they provide both fixed carbon and nitrogen to their animal host by sulfur-mediated chemolithoautotrophy (Petersen et al, 2017). Most studies assessing the ecology and function of sulfur chemosymbiosis have been performed within marine invertebrates hosts (Petersen et al, 2017;Osvatic et al, 2021Osvatic et al, , 2023Lim et al, 2019aLim et al, , 2019b. In contrast, there is still no evidence for the coupling of sulfur oxidation with nitrogen and/or carbon fixation in the roots of coastal marine plants because the genomes, metabolic potential, and activity .…”

Adaptation during the transition fromOphiocordycepsentomopathogen to insect associate is accompanied by gene loss and intensified selection

“…Gene gain and loss are essential adaptive strategies employed by many fungi to respond to novel environmental stressors (Osvatic, et al 2023). To investigate gene loss in the OAc lineage, 524 orthologs were identified that were present in Clade 1 (Figure 3A) but absent in the OAc annotation (Figure 3A).…”

Metabolically-versatileCa.Thiodiazotropha symbionts of the deep-sea lucinid clamLucinoma kazanihave the genetic potential to fix nitrogen

“…The isotopic composition of each sample was expressed as the relative difference between isotopic ratios in the sample and that in conventional standards (Vienna Pee Dee Belemnite, atmospheric N2 and Canyon Diablo Troilite for carbon, nitrogen and sulfur, respectively). Measured isotope ratios are reported in the δ per mille (‰) notation representing the deviation from the standards: δ Sample = ( RSample /Rstandard − 1 ) ×10 3 where, R = 15 N/ 14 N, 13 C/ 12 C or 34 S/ 32 S ratios.…”