Extracellular chemosymbiont populations in a shallow-water thyasirid clam potentially shaped by priority effect

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Chemosymbiosis is a highly successful strategy that evolved in several animal groups, best known for dominating chemosynthetic ecosystems such as deep-sea hot vents and hydrocarbon seeps but also found in other systems such as reducing sediments in shallow water. The symbiont population structure can be determined by the host genetic inheritance, geographic partitions, and environmental factors, among others if the symbionts are acquired horizontally from the environment. Here, we suggest that the earliest colonies can also influence the episymbiont population, known as the “priority effect”, using the thyasirid cleftclam Thyasira tokunagai. This species is abundant in reducing sediments in Yellow Sea, hosting an extracellular sulfide-oxidizing symbiont (genus Sedimenticola ) in the pouch-like structure in the gill. From samples taken across the whole Yellow Sea, complete symbiont genomes revealed only two dominant strains which were also verified by phylogenomic analysis. The two strains share key functional genes but exhibit a single-base difference in the 16S rDNA. We found mutually exclusive communities of these two strains in the 30 individual hosts studied, typically dominated or even monopolized by one strain. Inconsistent phylogenetic relationships between hosts and symbiont indicate the genetic heterogeneity of the holobiont, and the mean fixation index F ST of each symbiont population within sampling sites showed a lack of correlation with geographic distance and environmental factors, suggesting another driving force. We deduce that the likely scenario is 1) the dominant symbiont strain is determined during initial acquisition; 2) the propagation of this initial strain as the host develops; 3) the continuous but restricted recruitment of the other strain during the adult stage. Overall, our results highlight the importance of “priority effect” in shaping the chemosymbiont population structures even in the horizontally transmitted episymbiont in a whole marginal sea area.

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