State Key Laboratory of Marine Environmental Science, College of the Environment and Ecology, Xiamen University, Xiamen 361005, China.
Department of Microbiology, Key Laboratory of Agricultural and Environmental Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China.
ISME J. 2024 Jan 8;18(1). doi: 10.1093/ismejo/wrad002.
Ammonia-oxidizing archaea (AOA) are among the most ubiquitous and abundant archaea on Earth, widely distributed in marine, terrestrial, and geothermal ecosystems. However, the genomic diversity, biogeography, and evolutionary process of AOA populations in subsurface environments are vastly understudied compared to those in marine and soil systems. Here, we report a novel AOA order Candidatus (Ca.) Nitrosomirales which forms a sister lineage to the thermophilic Ca. Nitrosocaldales. Metagenomic and 16S rRNA gene-read mapping demonstrates the abundant presence of Nitrosomirales AOA in various groundwater environments and their widespread distribution across a range of geothermal, terrestrial, and marine habitats. Terrestrial Nitrosomirales AOA show the genetic capacity of using formate as a source of reductant and using nitrate as an alternative electron acceptor. Nitrosomirales AOA appear to have acquired key metabolic genes and operons from other mesophilic populations via horizontal gene transfer, including genes encoding urease, nitrite reductase, and V-type ATPase. The additional metabolic versatility conferred by acquired functions may have facilitated their radiation into a variety of subsurface, marine, and soil environments. We also provide evidence that each of the four AOA orders spans both marine and terrestrial habitats, which suggests a more complex evolutionary history for major AOA lineages than previously proposed. Together, these findings establish a robust phylogenomic framework of AOA and provide new insights into the ecology and adaptation of this globally abundant functional guild.
氨氧化古菌 (AOA) 是地球上最普遍和丰富的古菌之一，广泛分布于海洋、陆地和地热生态系统中。然而，与海洋和土壤系统相比，地下环境中 AOA 种群的基因组多样性、生物地理学和进化过程的研究还远远不够。在这里，我们报告了一种新型的氨氧化古菌目——候选古菌（Ca.）硝化螺旋菌目，它与嗜热 Ca. 硝化杆菌目形成姐妹谱系。宏基因组和 16S rRNA 基因读段映射表明，硝化螺旋菌目 AOA 在各种地下水环境中大量存在，并广泛分布于一系列地热、陆地和海洋生境中。陆地硝化螺旋菌目 AOA 显示出使用甲酸盐作为还原剂和使用硝酸盐作为替代电子受体的遗传能力。硝化螺旋菌目 AOA 似乎通过水平基因转移从其他嗜温种群中获得了关键的代谢基因和操纵子，包括编码脲酶、亚硝酸盐还原酶和 V 型 ATP 酶的基因。获得的功能赋予的额外代谢灵活性可能促进了它们辐射到各种地下、海洋和土壤环境中。我们还提供了证据表明，四个 AOA 目中的每一个都跨越了海洋和陆地生境，这表明主要 AOA 谱系的进化历史比以前提出的更为复杂。总之，这些发现建立了氨氧化古菌的稳健系统发育框架，并为该全球丰富的功能类群的生态学和适应性提供了新的见解。
