Li Mengna, Chen Hao, Wang Minxiao, Zhong Zhaoshan, Lian Chao, Zhou Li, Zhang Huan, Wang Hao, Cao Lei, Li Chaolun
Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; National Deep Sea Center, Qingdao 266071, China.
Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China; CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China.
Sci Total Environ. 2025 Jan 1;958:178048. doi: 10.1016/j.scitotenv.2024.178048. Epub 2024 Dec 16.
Methane hydrates stored in cold seeps are an important source of energy and carbon for both the endemic chemosynthetic community and humanity. However, the methane fluids may cease and even stop naturally or anthropogenically, calling for a thorough evaluation of its potential impact on the endemic species and local chemosynthetic ecosystems. As one dominant megafauna in cold seeps, some of the deep-sea mussels rely on methanotrophic endosymbionts for nutrition and therefore could serve as a promising model in monitoring the dynamic changes of methane hydrate. However, knowledge on the long-term responses of deep-sea mussels to environmental stresses induced by methane reduction and deprivation, is still lacking. Here, we set up a laboratory system and cultivated methanotrophic deep-sea mussel Gigantidas platifrons without methane supply to survey the phenotypic changes after methane deprivation. While the mussels managed to survive for >10 months after the methane deprivation, drastic changes in the metabolism, function, and development of gill tissue, and in the association with methanotrophic symbionts were observed. In detail, the mussel digested all methanotrophic endosymbionts shortly after methane deprivation for nutrition and remodeled the global metabolism of gill to conserve energy. As the methane deprivation continued, the mussel replaced its bacteriocytes with ciliated cells to support filter-feeding, which is an atavistic trait in non-symbiotic mussels. During the long-term methane deprivation assay, the mussel also retained the generation of new cells to support the phenotypic changes of gill and even promoted the activity after being transplanted back to deep-sea, showing the potential resilience after long-term methane deprivation. Evidences further highlighted the participation of symbiont sterol metabolism in regulating these processes. These results collectively show the phenotypic plasticity of deep-sea mussels and their dynamic responses to methane deprivation, providing essential information in assessing the long-term influence of methane hydrate extinction.
储存在冷泉中的甲烷水合物是地方化化学合成群落和人类重要的能量和碳源。然而，甲烷流体可能会自然或人为地停止甚至中断，因此需要全面评估其对地方物种和当地化学合成生态系统的潜在影响。作为冷泉中一种占主导地位的大型动物，一些深海贻贝依靠甲烷营养型内共生体获取营养，因此可以作为监测甲烷水合物动态变化的一个很有前景的模型。然而，关于深海贻贝对甲烷减少和缺乏所引起的环境压力的长期反应，目前仍缺乏相关了解。在此，我们建立了一个实验室系统，培养不供应甲烷的甲烷营养型深海贻贝扁巨贻贝，以研究甲烷缺乏后的表型变化。虽然贻贝在甲烷缺乏后存活了超过10个月，但观察到鳃组织的代谢、功能和发育以及与甲烷营养型共生体的关系发生了剧烈变化。具体而言，贻贝在甲烷缺乏后不久就消化了所有甲烷营养型内共生体以获取营养，并重塑了鳃的整体代谢以保存能量。随着甲烷缺乏的持续，贻贝用纤毛细胞取代了含菌细胞以支持滤食，这是非共生贻贝的一种返祖特征。在长期甲烷缺乏试验中，贻贝还保留了新细胞的生成以支持鳃的表型变化，甚至在被重新移植到深海后还促进了其活性，显示出长期甲烷缺乏后的潜在恢复力。证据进一步突出了共生体固醇代谢在调节这些过程中的作用。这些结果共同表明了深海贻贝的表型可塑性及其对甲烷缺乏的动态反应，为评估甲烷水合物消失的长期影响提供了重要信息。
