Heterogeneous composition of key metabolic gene clusters in a vent mussel symbiont population

Abstract

Chemosynthetic symbiosis is one of the successful systems for adapting to a wide range of habitats including extreme environments, and the metabolic capabilities of symbionts enable host organisms to expand their habitat ranges. However, our understanding of the adaptive strategies that enable symbiotic organisms to expand their habitats is still fragmentary. Here, we report that a single-ribotype endosymbiont population in an individual of the host vent mussel, Bathymodiolus septemdierum has heterogeneous genomes with regard to the composition of key metabolic gene clusters for hydrogen oxidation and nitrate reduction. The host individual harbours heterogeneous symbiont subpopulations that either possess or lack the gene clusters encoding hydrogenase or nitrate reductase. The proportions of the different symbiont subpopulations in a host appeared to vary with the environment or with the host's development. Furthermore, the symbiont subpopulations were distributed in patches to form a mosaic pattern in the gill. Genomic heterogeneity in an endosymbiont population may enable differential utilization of diverse substrates and confer metabolic flexibility. Our findings open a new chapter in our understanding of how symbiotic organisms alter their metabolic capabilities and expand their range of habitats.

Dual energy metabolism of the Campylobacterota endosymbiont in the chemosynthetic snail Alviniconcha marisindica

“…Based on the FISH and immunohistochemistry analyses and the radioisotope-labeled bicarbonate tracer experiments, Petersen et al [13] pointed out that hydrogenotrophy may serve as primary energy metabolism competitively with thiotrophy in the chemosynthetic holobiont. In addition, it has been reported that some chemosynthetic holobionts may use H 2 as an energy source because the genes encoding hydrogenase, and even the expression of the genes, were found in the symbiont genomes and transcriptomes [14,[16][17][18][19][20]. However, it has been also shown that these holobionts have molecular and physiological potentials of other energy metabolisms (sulfur and/or methane oxidation).…”

“…Subsequently, based on the newly developed in situ RNA extracting instrument and metatranscriptomic analysis, Sanders et al also demonstrated that some of the Sulfurimonas endosymbionts in Campylobacterota [15] expressed genes of Ni-Fe-hydrogenase in the northern ELSC vent fields with relatively abundant H 2 , implying that the specific Alviniconcha holobionts would also utilize H 2 as their chemosynthetic energy source [14,16]. Ikuta et al [17] also demonstrated that hupL and hupS genes, which encode small and large subunits of hydrogenase, were expressed in the symbiont of Bathymodiolus septemdierum from the Myojin Knoll hydrothermal vent site. In addition, genome-sequence analyses demonstrated that several holobionts of ventendemic chemosynthetic invertebrates have genes that are potentially involved in H 2 -oxidization, although the functional and molecular information of these genes is still not known [18][19][20].…”

Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated

“…In our model, bacteria are acquired from the environmental symbiont pool in juveniles 44 . The presence of a symbiont environmental pool was suggested before based on the detection of symbiont genes in adjacent seawater 45,46 . Nevertheless, the loss of central metabolic enzymes suggests that bacteria disperse in a dormant state 47 .…”

“…The new tissue is colonized by a self-infection process 26 , which involves infection of the newly formed filaments via endocytosis with bacteria that are released from old tissue via exocytosis (2). The spatial distribution of strains within the gill tissue also supports self-infection 45 . The continuous self-infection process imposes serial founder effects that lead to a reduction in strain diversity, which is mostly driven by drift.…”

Wolbachia and Cardinium infection found in threatened unionid species: a new concern for conservation of freshwater mussels?

“…In turn, the common presence of chemosynthetic symbiont in vent marine mussels inahibing extreme environments (e.g. Ikuta et al 2016) is the evidence for the support of host fitness benefits associated with the presence of symbionts (Zug and Hammerstein 2018).…”