Eco-Evolutionary Interactions Group, Max Planck Institute for Marine Microbiology (MPIMM), Bremen, Germany.
Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, San Pedro, San José, Costa Rica.
PLoS Genet. 2024 May 31;20(5):e1011295. doi: 10.1371/journal.pgen.1011295. eCollection 2024 May.
Bacterial symbionts, with their shorter generation times and capacity for horizontal gene transfer (HGT), play a critical role in allowing marine organisms to cope with environmental change. The closure of the Isthmus of Panama created distinct environmental conditions in the Tropical Eastern Pacific (TEP) and Caribbean, offering a "natural experiment" for studying how closely related animals evolve and adapt under environmental change. However, the role of bacterial symbionts in this process is often overlooked. We sequenced the genomes of endosymbiotic bacteria in two sets of sister species of chemosymbiotic bivalves from the genera Codakia and Ctena (family Lucinidae) collected on either side of the Isthmus, to investigate how differing environmental conditions have influenced the selection of symbionts and their metabolic capabilities. The lucinid sister species hosted different Candidatus Thiodiazotropha symbionts and only those from the Caribbean had the genetic potential for nitrogen fixation, while those from the TEP did not. Interestingly, this nitrogen-fixing ability did not correspond to symbiont phylogeny, suggesting convergent evolution of nitrogen fixation potential under nutrient-poor conditions. Reconstructing the evolutionary history of the nifHDKT operon by including other lucinid symbiont genomes from around the world further revealed that the last common ancestor (LCA) of Ca. Thiodiazotropha lacked nif genes, and populations in oligotrophic habitats later re-acquired the nif operon through HGT from the Sedimenticola symbiont lineage. Our study suggests that HGT of the nif operon has facilitated niche diversification of the globally distributed Ca. Thiodiazotropha endolucinida species clade. It highlights the importance of nitrogen availability in driving the ecological diversification of chemosynthetic symbiont species and the role that bacterial symbionts may play in the adaptation of marine organisms to changing environmental conditions.
细菌共生体具有较短的世代时间和水平基因转移 (HGT) 的能力，在使海洋生物能够应对环境变化方面发挥着关键作用。巴拿马地峡的关闭在热带东太平洋 (TEP) 和加勒比地区创造了截然不同的环境条件，为研究密切相关的动物在环境变化下如何进化和适应提供了一个“自然实验”。然而，细菌共生体在这个过程中的作用经常被忽视。我们对在地峡两侧采集的两个化学共生双壳贝类属 Codakia 和 Ctena 的姐妹种的内共生细菌进行了基因组测序，以研究不同的环境条件如何影响共生体的选择及其代谢能力。Lucinidae 姐妹种宿主的共生细菌不同，只有加勒比地区的共生细菌具有固氮的遗传潜力，而 TEP 的则没有。有趣的是，这种固氮能力与共生体系统发育无关，表明在营养贫乏的条件下固氮潜力发生了趋同进化。通过包括来自世界各地的其他 Lucinidae 共生体基因组，重建 nifHDKT 操纵子的进化历史进一步表明，Ca. Thiodiazotropha 的最后共同祖先 (LCA) 缺乏 nif 基因，而贫营养生境中的种群后来通过 Sedimenticola 共生体谱系的 HGT 重新获得了 nif 操纵子。我们的研究表明，nif 操纵子的 HGT 促进了全球分布的 Ca. Thiodiazotropha endolucinida 物种分支的生态多样化。它强调了氮可用性在驱动化学合成共生物种生态多样化方面的重要性，以及细菌共生体在海洋生物适应不断变化的环境条件方面可能发挥的作用。
