Genomic Inference of the Metabolism and Evolution of the Archaeal Phylum Aigarchaeota

Zheng-Shuang Hua, Guangdong Key Laboratory of Plant Resources
Yan-Ni Qu, Guangdong Key Laboratory of Plant Resources
Qiyun Zhu, University of California San Diego
En-Min Zhou, Guangdong Key Laboratory of Plant Resources
Yan-Ling Qi, Guangdong Key Laboratory of Plant Resources
Yi-Rui Yin, Guangdong Key Laboratory of Plant Resources
Yang-Zhi Rao, Guangdong Key Laboratory of Plant Resources
Ye Tian, Guangdong Key Laboratory of Plant Resources
Yu-Xian Li, Guangdong Key Laboratory of Plant Resources
Lan Liu, Sun Yat-Sen University
Cindy J. Castelle, University of California, Berkeley
Brian P. Hedlund, University of Nevada, Las Vegas
Wen-Sheng Shu, South China Normal University
Rob Knight, University of California San Diego
Wen-Jun Li, Guangdong Key Laboratory of Plant Resources

Abstract

Microbes of the phylum Aigarchaeota are widely distributed in geothermal environments, but their physiological and ecological roles are poorly understood. Here we analyze six Aigarchaeota metagenomic bins from two circumneutral hot springs in Tengchong, China, to reveal that they are either strict or facultative anaerobes, and most are chemolithotrophs that can perform sulfide oxidation. Applying comparative genomics to the Thaumarchaeota and Aigarchaeota, we find that they both originated from thermal habitats, sharing 1154 genes with their common ancestor. Horizontal gene transfer played a crucial role in shaping genetic diversity of Aigarchaeota and led to functional partitioning and ecological divergence among sympatric microbes, as several key functional innovations were endowed by Bacteria, including dissimilatory sulfite reduction and possibly carbon monoxide oxidation. Our study expands our knowledge of the possible ecological roles of the Aigarchaeota and clarifies their evolutionary relationship to their sister lineage Thaumarchaeota.