Genomic Insights into the Ecological Role and Evolution of a Novel Thermoplasmata Order, “ Candidatus Sysuiplasmatales”

Abstract

Recent omics studies have provided invaluable insights into the metabolic potential, adaptation and evolution of novel archaeal lineages from a variety of extreme environments. We have utilized a genome-resolved metagenomic approach to recover eight medium- to high-quality metagenome-assembled genomes (MAGs) that likely represent a new order (“Candidatus Sysuiplasmatales”) within Thermoplasmata from mine tailings and acid mine drainage (AMD) sediments sampled from two copper mines in South China. 16S rRNA gene based analyses revealed a narrow habitat range for these uncultured archaea limiting to AMD and hot spring-related environments. Metabolic reconstruction indicated a facultatively anaerobic heterotrophic lifestyle. This may allow the archaea to adapt to oxygen fluctuations and is thus in marked contrast to the majority of lineages in the domain Archaea which typically show obligately anaerobic metabolisms. Notably, “Ca. Sysuiplasmatales” could conserve energy through degradation of fatty acids, amino acid metabolism and oxidation of reduced inorganic sulfur compounds (RISCs), suggesting that they may contribute to acid generation in the extreme mine environments. Unlike its closely related Methanomassiliicoccales and “Ca. Gimiplasmatales”, “Ca. Sysuiplasmatales” lack the capacity to perform methanogenesis and carbon fixation. Ancestral state reconstruction indicated that “Ca. Sysuiplasmatales” and its closely related Methanomassiliicoccales, “Ca. Gimiplasmatales”, and the SG8-5 and the RBG-16-68-12 orders originated from a facultatively anaerobic ancestor capable of carbon fixation via the bacterial-type H₄F Wood–Ljungdahl pathway (WLP). Their metabolic divergence might be attributed to different evolutionary paths. Importance A wide array of archaea populate Earth’s extreme environments thereby they may play important roles in mediating biogeochemical processes such as iron and sulfur cycling. However, our knowledge of archaeal biology and evolution is still limited considering the uncultured majority of archaeal diversity. For instance, most order-level lineages except Thermoplasmatales, Aciduliprofundales and Methanomassiliicoccales within Thermoplasmata do not have cultured representatives. Here, we report the discovery and genomic characterization of a novel order, namely “Ca. Sysuiplasmatales”, within Thermoplasmata in the extremely acidic mine environments. “Ca. Sysuiplasmatales” are inferred to be facultatively anaerobic heterotrophs and likely contribute to acid generation through the oxidation of RISCs. The physiological divergence between “Ca. Sysuiplasmatales” and its closely related Thermoplasmata lineages may be attributed to different evolutionary paths. These results expand our knowledge of archaea in the extreme mine ecosystem.