Aix-Marseille Université, Université de Toulon, CNRS, IRD, MIO UM 110, Marseille, France.
Department of Microbiology and Molecular Genetics, Michigan State Universitygrid.17088.36, East Lansing, Michigan, USA.
mSystems. 2022 Aug 30;7(4):e0032822. doi: 10.1128/msystems.00328-22. Epub 2022 Aug 1.
Serpentinizing hydrothermal systems result from water circulating into the subsurface and interacting with mantle-derived rocks notably near mid-ocean ridges or continental ophiolites. Serpentinization and associated reactions produce alkaline fluids enriched in molecular hydrogen, methane, and small organic molecules that are assumed to feed microbial inhabitants. In this study, we explored the relationships linking serpentinization to associated microbial communities by comparative metagenomics of serpentinite-hosted systems, basalt-hosted vents, and hot springs. The shallow Prony bay hydrothermal field (PBHF) microbiome appeared to be more related to those of ophiolitic sites than to the Lost City hydrothermal field (LCHF) microbiome, probably because of the meteoric origin of its fluid, like terrestrial alkaline springs. This study emphasized the ubiquitous importance of a set of genes involved in the catabolism of phosphonates and highly enriched in all serpentinizing sites compared to other ecosystems. Because most of the serpentinizing systems are depleted in inorganic phosphate, the abundance of genes involved in the carbon-phosphorus lyase pathway suggests that the phosphonates constitute a source of phosphorus in these ecosystems. Additionally, hydrocarbons such as methane, released upon phosphonate catabolism, may contribute to the overall budget of organic molecules in serpentinizing systems. This first comparative metagenomic study of serpentinite-hosted environments provides an objective framework to understand the functioning of these peculiar ecosystems. We showed a taxonomic similarity between the PBHF and other terrestrial serpentinite-hosted ecosystems. At the same time, the LCHF microbial community was closer to deep basalt-hosted hydrothermal fields than continental ophiolites, despite the influence of serpentinization. This study revealed shared functional capabilities among serpentinite-hosted ecosystems in response to environmental stress, the metabolism of abundant dihydrogen, and the metabolism of phosphorus. Our results are consistent with the generalized view of serpentinite environments but provide deeper insight into the array of factors that may control microbial activities in these ecosystems. Moreover, we show that metabolism of phosphonate is widespread among alkaline serpentinizing systems and could play a crucial role in phosphorus and methane biogeochemical cycles. This study opens a new line of investigation of the metabolism of reduced phosphorus compounds in serpentinizing environments.
蛇纹石化热液系统是水在地下循环并与地幔衍生岩石相互作用的结果，特别是在大洋中脊或大陆蛇绿岩附近。蛇纹石化作用和相关反应产生富含分子氢、甲烷和小分子有机分子的碱性流体，这些流体被认为是微生物栖息的食物来源。在这项研究中，我们通过对蛇纹石化系统、玄武岩热液喷口和温泉的比较宏基因组学，探索了蛇纹石化作用与相关微生物群落之间的关系。浅层 Prony 湾热液场（PBHF）微生物组似乎与蛇绿岩区的微生物组更为相关，而与失落城热液场（LCHF）微生物组关系不大，这可能是因为其流体的大气成因，类似于陆地碱性泉。这项研究强调了一组参与膦酸盐分解代谢的基因的普遍重要性，这些基因在所有蛇纹石化区都高度富集，而在其他生态系统中则相对较少。由于大多数蛇纹石化系统中无机磷酸盐含量较低，因此参与碳-磷裂解酶途径的基因的丰度表明，在这些生态系统中，膦酸盐构成了磷的来源。此外，在膦酸盐分解代谢过程中释放的碳氢化合物，如甲烷，可能有助于蛇纹石化系统中有机分子的总体预算。这是首次对蛇纹石化环境进行的比较宏基因组学研究，为理解这些特殊生态系统的功能提供了客观框架。我们发现 PBHF 与其他陆地蛇纹石化生态系统在分类上具有相似性。同时，尽管受到蛇纹石化的影响，LCHF 微生物群落与深海玄武岩热液场比大陆蛇绿岩更为接近。这项研究揭示了蛇纹石化环境中生态系统之间的共享功能能力，包括对环境压力的适应、大量二氢的代谢以及磷的代谢。我们的研究结果与蛇纹石化环境的普遍观点一致，但对可能控制这些生态系统中微生物活动的一系列因素提供了更深入的了解。此外，我们表明，在碱性蛇纹石化系统中，膦酸盐的代谢是广泛存在的，它在磷和甲烷生物地球化学循环中可能发挥着关键作用。这项研究为蛇纹石化环境中还原磷化合物代谢的研究开辟了新的途径。
