School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA.
Department of Microbiology & Cell Biology, Montana State University, Bozeman, Montana, USA.
Appl Environ Microbiol. 2024 Apr 17;90(4):e0209923. doi: 10.1128/aem.02099-23. Epub 2024 Mar 6.
Marine oxygen-deficient zones (ODZs) are portions of the ocean where intense nitrogen loss occurs primarily via denitrification and anammox. Despite many decades of study, the identity of the microbes that catalyze nitrogen loss in ODZs is still being elucidated. Intriguingly, high transcription of genes in the same family as the nitric oxide dismutase () gene from Methylomirabilota has been reported in the anoxic core of ODZs. Here, we show that the most abundantly transcribed genes in the Eastern Tropical North Pacific ODZ belong to a new order (UBA11136) of Alphaproteobacteria rather than Methylomirabilota as previously assumed. Gammaproteobacteria and Planctomycetia also transcribe , but at lower relative abundance than UBA11136 in the upper ODZ. The -transcribing Alphaproteobacteria likely use formaldehyde and formate as a source of electrons for aerobic respiration, with additional electrons possibly from sulfide oxidation. They also transcribe multiheme cytochrome (here named ) genes for a putative porin-cytochrome protein complex of unknown function, potentially involved in extracellular electron transfer. Molecular oxygen for aerobic respiration may originate from nitric oxide dismutation via cryptic oxygen cycling. Our results implicate Alphaproteobacteria order UBA11136 as a significant player in marine nitrogen loss and highlight their potential in one-carbon, nitrogen, and sulfur metabolism in ODZs.IMPORTANCEIn marine oxygen-deficient zones (ODZs), microbes transform bioavailable nitrogen to gaseous nitrogen, with nitric oxide as a key intermediate. The Eastern Tropical North Pacific contains the world's largest ODZ, but the identity of the microbes transforming nitric oxide remains unknown. Here, we show that highly transcribed nitric oxide dismutase () genes belong to Alphaproteobacteria of the novel order UBA11136, which lacks cultivated isolates. These Alphaproteobacteria show evidence for aerobic respiration, using oxygen potentially sourced from nitric oxide dismutase, and possess a novel porin-cytochrome protein complex with unknown function. Gammaproteobacteria and Planctomycetia transcribe at lower levels. Our results pinpoint the microbes mediating a key step in marine nitrogen loss and reveal an unexpected predicted metabolism for marine Alphaproteobacteria.
海洋缺氧区（ODZ）是海洋中氮素强烈损失的主要通过反硝化和厌氧氨氧化发生的区域。尽管已经研究了几十年，但催化 ODZ 中氮素损失的微生物的身份仍在阐明之中。有趣的是，在 ODZ 的缺氧核心中，已经报道了与甲基拟杆菌中的一氧化氮二硫化物（）基因同一家族的基因的高转录。在这里，我们表明，东热带北太平洋 ODZ 中最转录的基因属于新的α变形菌目（UBA11136），而不是以前假设的甲基拟杆菌。γ变形菌和浮霉菌也转录，但在 ODZ 上层的相对丰度低于 UBA11136。进行转录的α变形菌可能使用甲醛和甲酸盐作为有氧呼吸的电子源，并且可能还有来自硫化物氧化的额外电子。它们还转录多血红素细胞色素（此处命名为）基因，用于一种未知功能的假定孔细胞色素蛋白复合物，可能参与细胞外电子转移。有氧呼吸所需的分子氧可能来自通过隐匿氧循环的一氧化氮歧化。我们的结果表明，α变形菌目 UBA11136 是海洋氮素损失的重要参与者，并强调了它们在 ODZ 中一碳、氮和硫代谢中的潜力。
重要性：在海洋缺氧区（ODZ）中，微生物将生物可利用的氮转化为气态氮，其中一氧化氮是关键的中间产物。东热带北太平洋拥有世界上最大的 ODZ，但将一氧化氮转化的微生物的身份仍然未知。在这里，我们表明，高度转录的一氧化氮二硫化物（）基因属于新型 UBA11136α变形菌目，该目缺乏培养的分离物。这些α变形菌表现出有氧呼吸的证据，可能使用源自一氧化氮二硫化物的氧气，并具有一种具有未知功能的新型孔细胞色素蛋白复合物。γ变形菌和浮霉菌的转录水平较低。我们的结果确定了介导海洋氮素损失关键步骤的微生物，并揭示了海洋α变形菌目出乎意料的预测代谢。
