School of Biological Sciences, Monash University, Clayton, VIC, 3800, Australia.
Department of Microbiology, Biomedicine Discovery Institute, Clayton, VIC, 3800, Australia.
ISME J. 2020 Nov;14(11):2649-2658. doi: 10.1038/s41396-020-0713-4. Epub 2020 Jul 9.
Diverse aerobic bacteria persist by consuming atmospheric hydrogen (H) using group 1h [NiFe]-hydrogenases. However, other hydrogenase classes are also distributed in aerobes, including the group 2a [NiFe]-hydrogenase. Based on studies focused on Cyanobacteria, the reported physiological role of the group 2a [NiFe]-hydrogenase is to recycle H produced by nitrogenase. However, given this hydrogenase is also present in various heterotrophs and lithoautotrophs lacking nitrogenases, it may play a wider role in bacterial metabolism. Here we investigated the role of this enzyme in three species from different phylogenetic lineages and ecological niches: Acidithiobacillus ferrooxidans (phylum Proteobacteria), Chloroflexus aggregans (phylum Chloroflexota), and Gemmatimonas aurantiaca (phylum Gemmatimonadota). qRT-PCR analysis revealed that the group 2a [NiFe]-hydrogenase of all three species is significantly upregulated during exponential growth compared to stationary phase, in contrast to the profile of the persistence-linked group 1h [NiFe]-hydrogenase. Whole-cell biochemical assays confirmed that all three strains aerobically respire H to sub-atmospheric levels, and oxidation rates were much higher during growth. Moreover, the oxidation of H supported mixotrophic growth of the carbon-fixing strains C. aggregans and A. ferrooxidans. Finally, we used phylogenomic analyses to show that this hydrogenase is widely distributed and is encoded by 13 bacterial phyla. These findings challenge the current persistence-centric model of the physiological role of atmospheric H oxidation and extend this process to two more phyla, Proteobacteria and Gemmatimonadota. In turn, these findings have broader relevance for understanding how bacteria conserve energy in different environments and control the biogeochemical cycling of atmospheric trace gases.
多样的需氧细菌通过消耗大气中的氢气（H）来维持生存，它们使用的是第 1h 组 [NiFe]-氢化酶。然而，其他氢化酶类也分布在好氧菌中，包括第 2a 组 [NiFe]-氢化酶。基于对蓝细菌的研究，第 2a 组 [NiFe]-氢化酶的报告生理作用是回收固氮酶产生的 H。然而，鉴于这种氢化酶也存在于各种缺乏固氮酶的异养生物和自养生物中，它可能在细菌代谢中发挥更广泛的作用。在这里，我们研究了这种酶在来自不同进化谱系和生态位的三个物种中的作用：氧化亚铁硫杆菌（变形菌门）、聚球藻（绿弯菌门）和金黄色矿杆菌（芽单胞菌门）。qRT-PCR 分析显示，与静止期相比，所有三种细菌在指数生长期，第 2a 组 [NiFe]-氢化酶的表达显著上调，而与持久性相关的第 1h 组 [NiFe]-氢化酶的表达则相反。全细胞生化测定证实，所有三种菌株都能在有氧条件下将 H 氧化到亚大气水平，并且在生长过程中氧化速率要高得多。此外，H 的氧化支持固碳菌株 C. aggregans 和 A. ferrooxidans 的混合营养生长。最后，我们利用系统基因组学分析表明，这种氢化酶广泛分布，并由 13 个细菌门编码。这些发现挑战了大气 H 氧化的生理作用的当前持久性中心模型，并将这一过程扩展到了另外两个门，变形菌门和芽单胞菌门。反过来，这些发现对于理解细菌在不同环境中如何保存能量以及控制大气痕量气体的生物地球化学循环具有更广泛的意义。
