Chemosynthetic alphaproteobacterial diazotrophs reside in deep-sea cold-seep bottom waters.

IF 5 2区 生物学 Q1 MICROBIOLOGY mSystems Pub Date : 2024-09-17 Epub Date: 2024-08-06 DOI:10.1128/msystems.00176-24
Jiawei Chen, Lixia Deng, Xiao Wang, Cheng Zhong, Xiaomin Xia, Hongbin Liu
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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.

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化合藻类重氮营养细菌栖息于深海冷渗底层水域。
固氮(N)生物(又称重氮营养体)通过控制生物可用氮的产生,在氮受限的生态系统中发挥着至关重要的作用。以碳为主的冷深生态系统本身就存在氮受限的问题,因此成为固氮的热点地区。然而,与其他海洋生态系统相比,人们对冷深生态系统中重氮营养体的了解十分有限。在这项研究中,我们利用多组学技术研究了深海冷渗底层水域重氮营养体的多样性和分解代谢。研究结果表明,与冷深上层水域和非冷深底层水域相比,冷深底层水域细菌群落中重氮营养体的相对丰度达到最高水平。值得注意的是,在冷深底层水域重氮营养体上对齐的元转录组读数中,98%以上属于Sagittula属,这是一种α蛋白细菌。其元基因组组装的基因组被命名为 Seep-BW-D1,包含固氮催化基因(nifHDK),nifH 基因在原位被积极转录。Seep-BW-D1 还具有氧化 C1 化合物(甲醇、甲醛和甲酸盐)和硫代硫酸盐(S2O32-)的化合能力。此外,我们还观察到大量转录本映射到参与乙酸盐、精胺/泼尼松碱和果胶低聚物运输系统的基因,这表明 Seep-BW-D1 可以利用甲烷氧化微生物合成的中间产物、冷沉底栖动物的腐烂组织以及来自上层光合生态系统的难溶性果胶中的有机物。总之,我们的研究证实了以碳为主的冷深底层水域会选择重氮营养体,并揭示了冷深底层水域中一种新型化学合成α蛋白细菌重氮营养体的分解过程:生物可用氮(N)是细胞生长和分裂的关键元素,其生产由重氮营养体控制。海洋重氮营养体占全球固定氮的近一半,并在各种海洋生态系统中进行氮固定。以往的研究主要集中在日照海洋和最小含氧区的重氮营养体,而最近的研究发现,冷渗漏生态系统是被忽视的固氮热点,因为冷渗漏生态系统中的渗漏液引入了丰富的生物可利用碳,但生物可利用氮却很少,这使得大多数冷渗漏本身就存在固氮限制。过去几十年中,在全球大陆边缘发现了数千个冷渗漏生态系统,冷渗漏在海洋氮的生物地球化学循环中的重要作用得到了强调。然而,人们对冷渗底水中的重氮营养盐仍然知之甚少。通过多组学研究,本研究发现了一种隶属于Sagittula的新型α蛋白细菌化合异养菌,它是冷渗底水中最活跃的重氮营养体之一,并揭示了它的分解代谢过程。
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来源期刊
mSystems
mSystems Biochemistry, 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.
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