Lilian A Cloarec, Thomas Bacchetta, Maxime Bruto, Christophe Leboulanger, Vincent Grossi, Céline Brochier-Armanet, Jean-Pierre Flandrois, Adrian Zurmely, Cécile Bernard, Marc Troussellier, Hélène Agogué, Magali Ader, Christine Oger-Desfeux, Philippe M Oger, Adrien Vigneron, Mylène Hugoni
{"title":"Lineage-dependent partitioning of activities in chemoclines defines Woesearchaeota ecotypes in an extreme aquatic ecosystem.","authors":"Lilian A Cloarec, Thomas Bacchetta, Maxime Bruto, Christophe Leboulanger, Vincent Grossi, Céline Brochier-Armanet, Jean-Pierre Flandrois, Adrian Zurmely, Cécile Bernard, Marc Troussellier, Hélène Agogué, Magali Ader, Christine Oger-Desfeux, Philippe M Oger, Adrien Vigneron, Mylène Hugoni","doi":"10.1186/s40168-024-01956-0","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>DPANN archaea, including Woesearchaeota, encompass a large fraction of the archaeal diversity, yet their genomic diversity, lifestyle, and role in natural microbiomes remain elusive. With an archaeal assemblage naturally enriched in Woesearchaeota and steep vertical geochemical gradients, Lake Dziani Dzaha (Mayotte) provides an ideal model to decipher their in-situ activity and ecology.</p><p><strong>Results: </strong>Using genome-resolved metagenomics and phylogenomics, we identified highly diversified Woesearchaeota populations and defined novel halophilic clades. Depth distribution of these populations in the water column showed an unusual double peak of abundance, located at two distinct chemoclines that are hotspots of microbial diversity in the water column. Genome-centric metatranscriptomics confirmed this vertical distribution and revealed a fermentative activity, with acetate and lactate as end products, and active cell-to-cell processes, supporting strong interactions with other community members at chemoclines. Our results also revealed distinct Woesearchaeota ecotypes, with different transcriptional patterns, contrasted lifestyles, and ecological strategies, depending on environmental/host conditions.</p><p><strong>Conclusions: </strong>This work provides novel insights into Woesearchaeota in situ activity and metabolism, revealing invariant, bimodal, and adaptative lifestyles among halophilic Woesearchaeota. This challenges our precepts of an invariable host-dependent metabolism for all the members of this taxa and revises our understanding of their contributions to ecosystem functioning and microbiome assemblage. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"249"},"PeriodicalIF":13.8000,"publicationDate":"2024-11-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11606122/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiome","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s40168-024-01956-0","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Background: DPANN archaea, including Woesearchaeota, encompass a large fraction of the archaeal diversity, yet their genomic diversity, lifestyle, and role in natural microbiomes remain elusive. With an archaeal assemblage naturally enriched in Woesearchaeota and steep vertical geochemical gradients, Lake Dziani Dzaha (Mayotte) provides an ideal model to decipher their in-situ activity and ecology.
Results: Using genome-resolved metagenomics and phylogenomics, we identified highly diversified Woesearchaeota populations and defined novel halophilic clades. Depth distribution of these populations in the water column showed an unusual double peak of abundance, located at two distinct chemoclines that are hotspots of microbial diversity in the water column. Genome-centric metatranscriptomics confirmed this vertical distribution and revealed a fermentative activity, with acetate and lactate as end products, and active cell-to-cell processes, supporting strong interactions with other community members at chemoclines. Our results also revealed distinct Woesearchaeota ecotypes, with different transcriptional patterns, contrasted lifestyles, and ecological strategies, depending on environmental/host conditions.
Conclusions: This work provides novel insights into Woesearchaeota in situ activity and metabolism, revealing invariant, bimodal, and adaptative lifestyles among halophilic Woesearchaeota. This challenges our precepts of an invariable host-dependent metabolism for all the members of this taxa and revises our understanding of their contributions to ecosystem functioning and microbiome assemblage. Video Abstract.
期刊介绍:
Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.