Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria: Insights from multi-omics analysis
Yi‐Tao Lin, 香港浸会大学生物系, 香港, 中国, Ting Xu, Jack Chi‐Ho Ip, Yanan Sun, Ling Fang, Tiangang Luan, Yu Zhang, Pei‐Yuan Qian, Jian‐Wen Qiu, 南方海洋科学与工程广东省实验室(广州), 广东 广州 511458, 中国, 香港科技大学海洋科学系, 香港, 中国, 中山大学测试中心, 广东 广州 510875, 中国, 中山大学生命科学学院有害生物控制与资源利用国家重点实验室, 广东 广州 510875, 中国, 广东工业大学环境生态工程研究院, 广东 广州 510006, 中国, 深圳大学生命与海洋科学学院, 广东 深圳 518060, 中国
Abstract
Endosymbiosis with Gammaproteobacteria is fundamental for the success of bathymodioline mussels in deep-sea chemosynthesis-based ecosystems. However, the recent discovery of Campylobacteria on the gill surfaces of these mussels suggests that these host-bacterial relationships may be more complex than previously thought. Using the cold-seep mussel (<i>Gigantidas haimaensis</i>) as a model, we explored this host-bacterial system by assembling the host transcriptome and genomes of its epibiotic Campylobacteria and endosymbiotic Gammaproteobacteria and quantifying their gene and protein expression levels. We found that the epibiont applies a sulfur oxidizing (SOX) multienzyme complex with the acquisition of <i>soxB</i> from Gammaproteobacteria for energy production and switched from a reductive tricarboxylic acid (rTCA) cycle to a Calvin-Benson-Bassham (CBB) cycle for carbon assimilation. The host provides metabolic intermediates, inorganic carbon, and thiosulfate to satisfy the materials and energy requirements of the epibiont, but whether the epibiont benefits the host is unclear. The endosymbiont adopts methane oxidation and the ribulose monophosphate pathway (RuMP) for energy production, providing the major source of energy for itself and the host. The host obtains most of its nutrients, such as lysine, glutamine, valine, isoleucine, leucine, histidine, and folate, from the endosymbiont. In addition, host pattern recognition receptors, including toll-like receptors, peptidoglycan recognition proteins, and C-type lectins, may participate in bacterial infection, maintenance, and population regulation. Overall, this study provides insights into the complex host-bacterial relationships that have enabled mussels and bacteria to thrive in deep-sea chemosynthetic ecosystems.