The symbiotic relationship between vestimentiferan tubeworms and their intracellular chemosynthetic bacteria is one of the more noteworthy examples of adaptation to deep-sea hydrothermal vent environments. The tubeworm symbionts have never been cultured in the laboratory. Nucleotide sequences from the small subunit rRNA gene suggest that the intracellular symbionts of the eastern Pacific vent tubeworms Oasisia alvinae, Riftia pachyptila, Tevnia jerichonana, and Ridgeia piscesae belong to the same phylotype of gammaproteobacteria, "Candidatus Endoriftia persephone." Comparisons of symbiont genomes between the East Pacific Rise tubeworms R. pachyptila and T. jerichonana confirmed that these two hosts share the same symbionts. Two Ridgeia symbiont genomes were assembled from trophosome metagenomes from worms collected from the Juan de Fuca Ridge (one and five individuals, respectively). We compared these assemblies to those of the sequenced Riftia and Tevnia symbionts. Pangenome composition, genome-wide comparisons of the nucleotide sequences, and pairwise comparisons of 2,313 orthologous genes indicated that "Ca. Endoriftia persephone" symbionts are structured on large geographical scales but also on smaller scales and possibly through host specificity. IMPORTANCERemarkably, the intracellular symbionts of four to six species of eastern Pacific vent tubeworms all belong to the same phylotype of gammaproteobacteria, "Candidatus Endoriftia persephone." Understanding the structure, dynamism, and interconnectivity of "Ca. Endoriftia persephone" populations is important to advancing our knowledge of the ecology and evolution of their host worms, which are often keystone species in vent communities. In this paper, we present the first genomes for symbionts associated with the species R. piscesae, from the Juan de Fuca Ridge. We then combine these genomes with published symbiont genomes from the East Pacific Rise tubeworms R. pachyptila and T. jerichonana to develop a portrait of the "Ca. Endoriftia persephone" pangenome and an initial outline of symbiont population structure in the different host species. Our study is the first to apply genome-wide comparisons of "Ca. Endoriftia persephone" assemblies in the context of population genetics and molecular evolution.A defining characteristic of hydrothermal vent ecosystems is the diversity and ubiquity of mutualistic partnerships between metazoa (multicellular organisms) and chemolithoautotrophic bacteria. Among these associations, one of the most remarkable is the well-studied model symbiosis between the giant tubeworm Riftia pachyptila and its unique sulfide-oxidizing gammaproteobacterial partner, "Candidatus Endoriftia persephone" (1). These intracellular symbionts are hosted within the specialized cells (bacteriocytes) of an organ known as the trophosome, which occupies most of the space in the coelomic cavity of the animal's trunk. In this mutualistic association, the worm supplies the bacteria with the inorganic compounds necessary for coupling sulfide oxidatio...
Epigenetic processes manage gene expression and products in a real‐time manner, allowing a single genome to display different phenotypes. In this paper, we discussed the relevance of assessing the different sources of epigenetic variation in natural populations. For a given genotype, the epigenetic variation could be environmentally induced or occur randomly. Strategies developed by organisms to face environmental fluctuations such as phenotypic plasticity and diversified bet‐hedging rely, respectively, on these different sources. Random variation can also represent a proxy of developmental stability and can be used to assess how organisms deal with stressful environmental conditions. We then proposed the microbiome as an extension of the epigenotype of the host to assess the factors determining the establishment of the community of microorganisms. Finally, we discussed these perspectives in the applied context of conservation.
Twenty one enteropneusts have been described from the west coast of North America, but those reports include no Spengelidae. Here we describe two species of acorn worms in the genus Schizocardium (S. californicum and S. peruvianum) on the basis of morphology. The former represent the first spengelid worm described from North American waters. The latter is a previously described species, and here we expand on its morphological description and extend its geographic range north from Peru to California. Notes on the habit and localization of each species, as well as a dichotomous key to the genera of the family Spengelidae are provided. Based on morphology, spengelids appears to represent an intermediate between the enteropneust families Harrimaniidae and Ptychoderidae, and Schizocardium is sister taxon to the ptychoderids. The disjunct and widely distributed populations of S. peruvianum and S. brasiliense, with populations in South American and North America, but none between, could represent the relict populations of formerly wide spread species, or the two extremes of ranges.
Vertical transmission of bacterial endosymbionts is accompanied by virtually irreversible gene loss that results in a progressive reduction in genome size. While the evolutionary processes of genome reduction have been well described in some terrestrial symbioses, they are less understood in marine systems where vertical transmission is rarely observed. The association between deep-sea vesicomyid clams and chemosynthetic Gammaproteobacteria is one example of maternally inherited symbioses in the ocean. Here, we assessed the contributions of drift, recombination and selection to genome evolution in two extant vesicomyid symbiont clades by comparing 15 representative symbiont genomes (1.017–1.586 Mb) to those of closely related bacteria and the hosts' mitochondria. Our analyses suggest that drift is a significant force driving genome evolution in vesicomyid symbionts, though selection and interspecific recombination appear to be critical for maintaining symbiont functional integrity and creating divergent patterns of gene conservation. Notably, the two symbiont clades possess putative functional differences in sulfide physiology, anaerobic respiration and dependency on environmental vitamin B12, which probably reflect adaptations to different ecological habitats available to each symbiont group. Overall, these results contribute to our understanding of the eco-evolutionary processes shaping reductive genome evolution in vertically transmitted symbioses.
The scaly-foot snail (Chrysomallon squamiferum) inhabiting deep-sea hydrothermal vents in the Indian Ocean relies on its sulphur-oxidising gammaproteobacterial endosymbionts for nutrition and energy. In this study, we investigate the specificity, transmission mode, and stability of multiple scaly-foot snail populations dwelling in five vent fields with considerably disparate geological, physical and chemical environmental conditions. Results of population genomics analyses reveal an incongruent phylogeny between the endosymbiont and mitochondrial genomes of the scaly-foot snails in the five vent fields sampled, indicating that the hosts obtain endosymbionts via horizontal transmission in each generation. However, the genetic homogeneity of many symbiont populations implies that vertical transmission cannot be ruled out either. Fluorescence in situ hybridisation of ovarian tissue yields symbiont signals around the oocytes, suggesting that vertical transmission co-occurs with horizontal transmission. Results of in situ environmental measurements and gene expression analyses from in situ fixed samples show that the snail host buffers the differences in environmental conditions to provide the endosymbionts with a stable intracellular micro-environment, where the symbionts serve key metabolic functions and benefit from the host’s cushion. The mixed transmission mode, symbiont specificity at the species level, and stable intracellular environment provided by the host support the evolutionary, ecological, and physiological success of scaly-foot snail holobionts in different vents with unique environmental parameters.
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