{"title":"Thaumarchaeota from deep-sea methane seeps provide novel insights into their evolutionary history and ecological implications.","authors":"Yingdong Li, Jiawei Chen, Yanxun Lin, Cheng Zhong, Hongmei Jing, Hongbin Liu","doi":"10.1186/s40168-024-01912-y","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota mediate the rate-limiting step of nitrification and remove the ammonia that inhibits the aerobic metabolism of methanotrophs. However, the AOA that inhabit deep-sea methane-seep surface sediments (DMS) are rarely studied. Here, we used global DMS metagenomics and metagenome-assembled genomes (MAGs) to investigate the metabolic activity, evolutionary history, and ecological contributions of AOA. Expression of AOA-specific ammonia-oxidizing gene (amoA) was examined in the sediments collected from the South China Sea (SCS) to identify their active ammonia metabolism in the DMS.</p><p><strong>Results: </strong>Our analysis indicated that AOA contribute > 75% to the composition of ammonia-utilization genes within the surface layers (above 30 cm) of global DMS. The AOA-specific ammonia-oxidizing gene was actively expressed in the DMS collected from the SCS. Phylogenomic analysis of medium-/high-quality MAGs from 18 DMS-AOA indicated that they evolved from ancestors in the barren deep-sea sediment and then expanded from the DMS to shallow water forming an amoA-NP-gamma clade-affiliated lineage. Molecular dating suggests that the DMS-AOA origination coincided with the Neoproterozoic oxidation event (NOE), which occurred ~ 800 million years ago (mya), and their expansion to shallow water coincided with the Sturtian glaciation (~ 713 mya). Comparative genomic analysis suggests that DMS-AOA exhibit higher requirement of carbon source for protein synthesis with enhanced genomic capability for osmotic regulation, motility, chemotaxis, and utilization of exogenous organic compounds, suggesting it could be more heterotrophic compared with other lineages.</p><p><strong>Conclusion: </strong>Our findings provide new insights into the evolutionary history of AOA within the Thaumarchaeota, highlighting their critical roles in nitrogen cycling in the global DMS ecosystems. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"197"},"PeriodicalIF":13.8000,"publicationDate":"2024-10-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11463064/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiome","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s40168-024-01912-y","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: Ammonia-oxidizing archaea (AOA) of the phylum Thaumarchaeota mediate the rate-limiting step of nitrification and remove the ammonia that inhibits the aerobic metabolism of methanotrophs. However, the AOA that inhabit deep-sea methane-seep surface sediments (DMS) are rarely studied. Here, we used global DMS metagenomics and metagenome-assembled genomes (MAGs) to investigate the metabolic activity, evolutionary history, and ecological contributions of AOA. Expression of AOA-specific ammonia-oxidizing gene (amoA) was examined in the sediments collected from the South China Sea (SCS) to identify their active ammonia metabolism in the DMS.
Results: Our analysis indicated that AOA contribute > 75% to the composition of ammonia-utilization genes within the surface layers (above 30 cm) of global DMS. The AOA-specific ammonia-oxidizing gene was actively expressed in the DMS collected from the SCS. Phylogenomic analysis of medium-/high-quality MAGs from 18 DMS-AOA indicated that they evolved from ancestors in the barren deep-sea sediment and then expanded from the DMS to shallow water forming an amoA-NP-gamma clade-affiliated lineage. Molecular dating suggests that the DMS-AOA origination coincided with the Neoproterozoic oxidation event (NOE), which occurred ~ 800 million years ago (mya), and their expansion to shallow water coincided with the Sturtian glaciation (~ 713 mya). Comparative genomic analysis suggests that DMS-AOA exhibit higher requirement of carbon source for protein synthesis with enhanced genomic capability for osmotic regulation, motility, chemotaxis, and utilization of exogenous organic compounds, suggesting it could be more heterotrophic compared with other lineages.
Conclusion: Our findings provide new insights into the evolutionary history of AOA within the Thaumarchaeota, highlighting their critical roles in nitrogen cycling in the global DMS ecosystems. 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.