Previous studies have revealed tight metabolic complementarity between bivalves and their endosymbiotic chemosynthetic bacteria, but little is known about their interactions with ectosymbionts. Our analysis of the ectosymbiosis between a deep-sea scallop (Catillopecten margaritatus) and a gammaproteobacterium showed that bivalves could be highly interdependent with their ectosymbionts as well. Our microscopic observation revealed abundant sulfur-oxidizing bacteria (SOB) on the surfaces of the gill epithelial cells. Microbial 16S rRNA gene amplicon sequencing of the gill tissue showed the dominance of the SOB. An analysis of the SOB genome showed that it is substantially smaller than its free-living relatives and has lost cellular components required for free-living. Genomic and transcriptomic analyses showed that this ectosymbiont relies on rhodanese-like proteins and SOX multienzyme complex for energy generation and mainly on the CBB cycle for carbon assimilation. The symbiont encodes an incomplete TCA cycle that could also assimilate inorganic carbon via a phosphoenolpyruvate carboxylase. Observation of the scallop’s digestive gland and its nitrogen metabolism pathways indicates it does not fully rely on the ectosymbiont for nutrition. Analysis of the host’s gene expression provided evidence that it could offer intermediates for the ectosymbiont to complete its TCA cycle and some amino acid synthesis pathways using exosomes, and its phagosomes, endosomes, and lysosomes might be involved in harvesting nutrients from the symbionts. Overall, our study prompts us to rethink the intimacy between the hosts and ectosymbionts in Bivalvia and the evolution of chemosymbiosis in general.

中文翻译：

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来自深海的扇贝-细菌共生揭示了在没有细胞整合的情况下强烈的基因组耦合

先前的研究揭示了双壳类与其内共生化学合成细菌之间紧密的代谢互补性，但对其与外共生体的相互作用知之甚少。我们对深海扇贝（Catillopecten margaritatus）和γ变形菌之间的外共生的分析表明，双壳类动物也可能与其外共生体高度相互依赖。我们的显微镜观察发现，鳃上皮细胞表面存在丰富的硫氧化细菌（SOB）。鳃组织的微生物 16S rRNA 基因扩增子测序显示 SOB 占主导地位。对 SOB 基因组的分析表明，它比自由生活的亲戚小得多，并且失去了自由生活所需的细胞成分。基因组和转录组分析表明，这种外共生体依赖硫氰酸酶样蛋白和 SOX 多酶复合物产生能量，并主要依赖 CBB 循环进行碳同化。该共生体编码一个不完整的 TCA 循环，也可以通过磷酸烯醇丙酮酸羧化酶同化无机碳。对扇贝消化腺及其氮代谢途径的观察表明，扇贝并不完全依赖外共生体获取营养。对宿主基因表达的分析提供了证据，表明它可以为外共生体提供中间体，以完成其TCA循环和使用外泌体的一些氨基酸合成途径，并且其吞噬体、内体和溶酶体可能参与从共生体中获取营养物质。总的来说，我们的研究促使我们重新思考双壳纲宿主和外共生体之间的亲密关系以及化学共生的总体进化。