Vigneron Adrien, Cloarec Lilian A, Brochier-Armanet Céline, Flandrois Jean Pierre, Troussellier Marc, Bernard Cécile, Agogué Hélène, Oger Philippe M, Hugoni Mylène
INSA Lyon, CNRS, UMR5240 Microbiologie Adaptation et Pathogénie, Universite Claude Bernard Lyon 1, 69621, Villeurbanne, France.
CNRS, VetAgro Sup, Laboratoire de Biométrie et Biologie Évolutive, UMR5558, Universite Claude Bernard Lyon 1, Villeurbanne, France.
Environ Microbiome. 2025 May 6;20(1):48. doi: 10.1186/s40793-025-00699-1.
Extreme environments are useful systems to investigate limits of life, microbial biogeography and ecology, and the adaptation and evolution of microbial lineages. Many novel microbial lineages have been discovered in extreme environments, especially from the Planctomycetota-Verrucomicrobiota-Chlamydiota (PVC) superphyla. However, their evolutionary history and roles in ecosystem functioning and microbiome assemblage are poorly understood.
Applying a genome-centric approach on an 8-year metagenomic timeseries produced from the hypersaline and hyperalkaline waters of Lake Dziani Dzaha (Mayotte), we recovered 5 novel PVC extremophilic candidate lineages from the biosphere of the lake. Sibling to Elusimicrobia and Omnitrophota, these lineages represented novel halophilic clades, with global distributions bounded to soda lakes and hypersaline hydrosystems. Genome mining of these newly defined clades revealed contrasted, but ecologically relevant, catabolic capabilities involved in the carbon, hydrogen and iron/electron cycles of the Dziani Dzaha ecosystem. This also includes extracellular electron transfer for two of them, suggesting metal reduction or potential electron exchanges with other members of the lake community. By contrast, a putative extracellular giant protein with multiple carbohydrate binding domains and toxin-like structures, as observed in virulence factors, was identified in the genome of another of these clades, suggesting predatory capabilities.
Our results provided genomic evidences for original metabolism in novel extremophile lineages of the PVC superphyla, revealing unforeseen implications for members of this widespread and diverse bacterial radiation in aquatic saline ecosystems. Finally, monitoring the in-situ distribution of these lineages through the timeseries reveals the drastic effects of environmental perturbations on extreme ecosystem biodiversity.
极端环境是研究生命极限、微生物生物地理学和生态学以及微生物谱系的适应与进化的有用系统。在极端环境中发现了许多新的微生物谱系，尤其是来自浮霉菌门-疣微菌门-衣原体门（PVC）超门的谱系。然而，它们的进化历史以及在生态系统功能和微生物群落组装中的作用却知之甚少。
通过对取自迪亚尼扎哈湖（马约特岛）高盐和高碱性水域的8年宏基因组时间序列应用以基因组为中心的方法，我们从该湖的生物圈中获得了5个新的PVC嗜极端候选谱系。这些谱系与迷踪菌门和全营养菌门是姐妹谱系，代表了新的嗜盐分支，其全球分布局限于苏打湖和高盐水系。对这些新定义分支的基因组挖掘揭示了与迪亚尼扎哈湖生态系统的碳、氢和铁/电子循环相关的、形成对比但具有生态相关性的分解代谢能力。其中两个分支还包括细胞外电子转移，这表明存在金属还原或与湖泊群落其他成员进行潜在电子交换的情况。相比之下，在其中一个分支的基因组中发现了一种推定的细胞外巨型蛋白，它具有多个碳水化合物结合结构域和类似毒素的结构，这在毒力因子中也有观察到，表明其具有捕食能力。
我们的研究结果为PVC超门新嗜极端谱系中的原始代谢提供了基因组证据，揭示了这一广泛多样的细菌辐射成员在水生盐生态系统中意想不到的影响。最后，通过时间序列监测这些谱系的原位分布，揭示了环境扰动对极端生态系统生物多样性的巨大影响。
