Li, Ming

Summary The KTK 4A‐related Thermoplasmata thrives in the sediment of saline lakes; however, systematic research on its taxonomy, environmental adaptation and metabolism is lacking. Here, we detected this abundant lineage in the sediment of five artificially separated ponds (salinity 7.0%–33.0%) within a Chinese soda‐saline lake using culture‐independent metagenomics and archaeal 16S rRNA gene amplicons. The phylogenies based on the 16S rRNA gene, and 122 archaeal ubiquitous single‐copy proteins and genome‐level identity analyses among the metagenome‐assembled genomes demonstrate this lineage forming a novel order, Candidatus Haloplasmatales, comprising four genera affiliated with the identical family. Isoelectric point profiles of predicted proteomes suggest that most members adopt the energetically favourable ‘salt‐in’ strategy. Functional prediction indicates the lithoheterotrophic nature with the versatile metabolic potentials for carbohydrate and organic acids as well as carbon monoxide and hydrogen utilization. Additionally, hydrogenase genes hdrABC ‐ mvhADG are linked with incomplete reductive citrate cycle genes in the genomes, suggesting their functional connection. Comparison with the coupling of HdrABC‐MvhADG and methanogenesis pathway provides new insights into the compatibility of laterally acquired methanogenesis with energy metabolism in the related order Methanomassiliicoccales . Globally, our research sheds light on the taxonomy, environmental adaptative mechanisms, metabolic potentials and evolutional significance of Ca . Haloplasmatales.

Abstract BackgroundArchaea were originally discovered in extreme environments, and thrive in many extreme habitats including soda lakes with high pH and salinity. Characteristic and diverse archaeal community played a significant role in biogeochemical cycles; however, the archaeal community and their functions are still less-studied in the intricate sediment of soda lakes. ResultsIn this article, the archaeal community of the deep sediment (40-50 cm depth) of five artificially-separated ponds with a salinity range from 7.0% to 33.0% in a soda saline lake was systematically surveyed using culture-independent metagenomics combined with the next-generation sequencing of the archaeal 16S rRNA amplicons. Nine archaeal phyla were detected, which accounted for 2.2% to 35.73% of microbial community in the five deep sediments. Besides the well-known class Halobacteria, one novel archaeal order (Candidatus Natranaeroarchaeales) of the class Thermoplasmata was even more abundant than Halobacteria in some deep sediment samples. Of 69 dereplicated archaeal metagenome-assembled genomes (MAGs), 30 MAGs belonged to Ca. Natranaeroarchaeales. Different genera of the Ca. Natranaeroarchaeales preferred to inhabit in the different salinities, and the divergent halophilic adaptation strategies (salt-out or salt-in) suggested the fast evolution adaptation within this lineage. Most high-quality MAGs had the genes of Wood-Ljungdahl pathway, organic acid fermentation and sulfur respiration, suggesting the putative functions in carbon fixation and sulfur reduction. Interestingly, heterodisulfide reductase and F420-non-reducing hydrogenase complex HdrABC-MvhADG were widely distributed in Ca. Natranaeroarchaeales and may play the core roles in energy metabolism from hydrogen. The regeneration of CoM-S-S-CoB was coupled to succinate or 2-oxoglutarate production in Ca. Natranaeroarchaeales instead of methanogenesis in the close related Methanomassiliicoccales. It suggested that methyl-coenzyme M reductase in Methanomassiliicoccales may be laterally transferred from other methanogens. ConclusionA novel archaeal order Ca. Natranaeroarchaeales of Thermoplasmata was found by culture-independent approaches. This order was the most abundant archaeal lineage in the deep sediment of soda lakes, with the characteristic environmental adaptation and biogeochemical potentials in carbon fixation and sulfur reduction. The difference in fermentation products coupled to energy metabolism between methanogens and Ca. Natranaeroarchaeales provided additional insights into the origination of methanogenesis in Thermoplasmata from the energy metabolism perspective.