Comparative genomic analysis of Thermus provides insights into the evolutionary history of an incomplete denitrification pathway

Abstract

Impact statement For decades, Thermus was always considered to be aerobic. However, recent studies have suggested that the denitrification abilities of Thermus species may be widely underestimated. In the present study, we used comparative genomic analysis to investigate the evolutionary history of the denitrification pathway in Thermus and other members of the phylum Deinococcota. We revealed incomplete denitrification pathways to be common in Thermus and showed they are inherited mostly vertically, which further supports the importance of Thermus as a significant denitrifier in hydrothermal environments.

Incomplete denitrification phenotypes in diverse Thermus species from diverse geothermal spring sediments and adjacent soils in southwest China

“…3 ). A similar genotype and phenotype was observed for T. oshimai YIM 77923-2, and similar genotypes ( nar and nir genes but lacking nor genes) have been observed previously in genomes from T. antranikianii DSM 12462 T , Thermus parrtaviensis RL T , Thermus thermamylovorans CFH72773 T , Caldithermus terrae DSM 26712 T , and Caldithermus chliarophilus DSM 9957 T (Jiao et al 2022 ). These genomes also lack nrf systems that could support dissimilatory nitrite reduction to ammonium as an alternative pathway.…”

“…Several genetic and genomic studies have shed light on nitrate reduction and denitrification pathways in Thermus . Genes for nitrate reduction are found within the nar gene cluster and neighboring genes code for other denitrification genes (Gounder et al 2011 ; Jiao et al 2022 ; Mefferd et al 2016 ; Murugapiran et al 2013 ; Zhou et al 2016 ). Thermus denitrification genes are sometimes present on plasmids (Ramirez-Arcos et al 1998 ; Brüggemann et al 2006 ).…”

“…These studies have shed some light on denitrification pathways in Thermus and inferred an important role for them in heterotrophic denitrification; however, they only encompass a few species and a limited geographic range, and do not provide a comprehensive characterization of the denitrification phenotypes across the genus. A recent paper describes the presence and evolution of denitrification gene clusters in representatives of most species of Thermus , but did not examine phenotypes (Jiao et al 2022 ). The goal of this study was to characterize denitrification phenotypes in a diversity of Thermus species to gain insight into their potential roles in the nitrogen cycle in high-temperature environments.…”

Chelatococcus albus sp. nov., a bacterium isolated from hot spring microbial mat

“…Terrestrial geothermal spring systems are typical extreme environments with extremely high temperature and extensive pH ranges [1]. There are abundant thermophilic microbial resources in hot springs that are actively involved in the biogeochemical cycle and energy flow in this ecosystem [2][3][4]. Additionally, thermophilic microbes generally have high metabolic activity and enzyme thermal stability, which has good application prospects in industrial production, environmental recovery, pollutant degradation and other domains [5][6][7].…”

Phylogenomic analyses and comparative genomic studies of Thermus strains isolated from Tengchong and Tibet hot springs, China

“…Strain T. parvatiensis RL also containing genes for arsenic resistance (Tripathi et al 2017). Thermus members have incomplete set of genes for denitri cation pathways (Hedlund et al 2011;Mefferd et al 2022), and genes encoded for enzymes in denitri cation pathway (narG, nirS, and norB) have acquired by the last common ancestor of Thermales and were inherited vertically expect nirK (Jiao et al 2022). Thermus genomes have high plasticity (Brüggemann and Chen 2006) and natural competence to transform DNA (Lorenz and Wackernagel 1994).…”