{"title":"Chemosynthetic alphaproteobacterial diazotrophs reside in deep-sea cold-seep bottom waters.","authors":"Jiawei Chen, Lixia Deng, Xiao Wang, Cheng Zhong, Xiaomin Xia, Hongbin Liu","doi":"10.1128/msystems.00176-24","DOIUrl":null,"url":null,"abstract":"<p><p>Nitrogen (N)-fixing organisms, also known as diazotrophs, play a crucial role in N-limited ecosystems by controlling the production of bioavailable N. The carbon-dominated cold-seep ecosystems are inherently N-limited, making them hotspots of N fixation. However, the knowledge of diazotrophs in cold-seep ecosystems is limited compared to other marine ecosystems. In this study, we used multi-omics to investigate the diversity and catabolism of diazotrophs in deep-sea cold-seep bottom waters. Our findings showed that the relative abundance of diazotrophs in the bacterial community reached its highest level in the cold-seep bottom waters compared to the cold-seep upper waters and non-seep bottom waters. Remarkably, more than 98% of metatranscriptomic reads aligned on diazotrophs in cold-seep bottom waters belonged to the genus <i>Sagittula</i>, an alphaproteobacterium. Its metagenome-assembled genome, named Seep-BW-D1, contained catalytic genes (<i>nifHDK</i>) for nitrogen fixation, and the <i>nifH</i> gene was actively transcribed <i>in situ</i>. Seep-BW-D1 also exhibited chemosynthetic capability to oxidize C1 compounds (methanol, formaldehyde, and formate) and thiosulfate (S<sub>2</sub>O<sub>3</sub><sup>2-</sup>). In addition, we observed abundant transcripts mapped to genes involved in the transport systems for acetate, spermidine/putrescine, and pectin oligomers, suggesting that Seep-BW-D1 can utilize organics from the intermediates synthesized by methane-oxidizing microorganisms, decaying tissues from cold-seep benthic animals, and refractory pectin derived from upper photosynthetic ecosystems. Overall, our study corroborates that carbon-dominated cold-seep bottom waters select for diazotrophs and reveals the catabolism of a novel chemosynthetic alphaproteobacterial diazotroph in cold-seep bottom waters.</p><p><strong>Importance: </strong>Bioavailable nitrogen (N) is a crucial element for cellular growth and division, and its production is controlled by diazotrophs. Marine diazotrophs contribute to nearly half of the global fixed N and perform N fixation in various marine ecosystems. While previous studies mainly focused on diazotrophs in the sunlit ocean and oxygen minimum zones, recent research has recognized cold-seep ecosystems as overlooked N-fixing hotspots because the seeping fluids in cold-seep ecosystems introduce abundant bioavailable carbon but little bioavailable N, making most cold seeps inherently N-limited. With thousands of cold-seep ecosystems detected at continental margins worldwide in the past decades, the significant role of cold seeps in marine N biogeochemical cycling is emphasized. However, the diazotrophs in cold-seep bottom waters remain poorly understood. Through multi-omics, this study identified a novel alphaproteobacterial chemoheterotroph belonging to <i>Sagittula</i> as one of the most active diazotrophs residing in cold-seep bottom waters and revealed its catabolism.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0017624"},"PeriodicalIF":5.0000,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11406894/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"mSystems","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/msystems.00176-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/8/6 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Nitrogen (N)-fixing organisms, also known as diazotrophs, play a crucial role in N-limited ecosystems by controlling the production of bioavailable N. The carbon-dominated cold-seep ecosystems are inherently N-limited, making them hotspots of N fixation. However, the knowledge of diazotrophs in cold-seep ecosystems is limited compared to other marine ecosystems. In this study, we used multi-omics to investigate the diversity and catabolism of diazotrophs in deep-sea cold-seep bottom waters. Our findings showed that the relative abundance of diazotrophs in the bacterial community reached its highest level in the cold-seep bottom waters compared to the cold-seep upper waters and non-seep bottom waters. Remarkably, more than 98% of metatranscriptomic reads aligned on diazotrophs in cold-seep bottom waters belonged to the genus Sagittula, an alphaproteobacterium. Its metagenome-assembled genome, named Seep-BW-D1, contained catalytic genes (nifHDK) for nitrogen fixation, and the nifH gene was actively transcribed in situ. Seep-BW-D1 also exhibited chemosynthetic capability to oxidize C1 compounds (methanol, formaldehyde, and formate) and thiosulfate (S2O32-). In addition, we observed abundant transcripts mapped to genes involved in the transport systems for acetate, spermidine/putrescine, and pectin oligomers, suggesting that Seep-BW-D1 can utilize organics from the intermediates synthesized by methane-oxidizing microorganisms, decaying tissues from cold-seep benthic animals, and refractory pectin derived from upper photosynthetic ecosystems. Overall, our study corroborates that carbon-dominated cold-seep bottom waters select for diazotrophs and reveals the catabolism of a novel chemosynthetic alphaproteobacterial diazotroph in cold-seep bottom waters.
Importance: Bioavailable nitrogen (N) is a crucial element for cellular growth and division, and its production is controlled by diazotrophs. Marine diazotrophs contribute to nearly half of the global fixed N and perform N fixation in various marine ecosystems. While previous studies mainly focused on diazotrophs in the sunlit ocean and oxygen minimum zones, recent research has recognized cold-seep ecosystems as overlooked N-fixing hotspots because the seeping fluids in cold-seep ecosystems introduce abundant bioavailable carbon but little bioavailable N, making most cold seeps inherently N-limited. With thousands of cold-seep ecosystems detected at continental margins worldwide in the past decades, the significant role of cold seeps in marine N biogeochemical cycling is emphasized. However, the diazotrophs in cold-seep bottom waters remain poorly understood. Through multi-omics, this study identified a novel alphaproteobacterial chemoheterotroph belonging to Sagittula as one of the most active diazotrophs residing in cold-seep bottom waters and revealed its catabolism.
mSystemsBiochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
10.50
自引率
3.10%
发文量
308
审稿时长
13 weeks
期刊介绍:
mSystems™ will publish preeminent work that stems from applying technologies for high-throughput analyses to achieve insights into the metabolic and regulatory systems at the scale of both the single cell and microbial communities. The scope of mSystems™ encompasses all important biological and biochemical findings drawn from analyses of large data sets, as well as new computational approaches for deriving these insights. mSystems™ will welcome submissions from researchers who focus on the microbiome, genomics, metagenomics, transcriptomics, metabolomics, proteomics, glycomics, bioinformatics, and computational microbiology. mSystems™ will provide streamlined decisions, while carrying on ASM''s tradition of rigorous peer review.