Isolation and characterization of a thermophilic sulfur- and iron-reducing thaumarchaeote from a terrestrial acidic hot spring

Abstract

A deep-branching clade of Thaumarchaeota, conventionally called Terrestrial hot spring creanarchaeotic group (THSCG), is a missing link between thaumarchaeotic ammonia oxidizers and the deeper-branching non-ammonia oxidizers, such as Crenarchaeota and Candidatus Korarchaeota. Here, we report isolation of the first cultivated representative from the THSCG, named as NAS-02. Physiological characterization demonstrated that the isolate was a thermoacidophilic, sulfurand iron-reducing organoheterotroph, which was supported by gene contents encoded in its complete genome. There was no evidence for ammonia oxidation by the isolate. Members in THSCG are likely thermophiles, and may play roles in degrading cell debris as a scavenger and in biogeochemical cycling of sulfur and iron in the hot environments, as suggested by the physiological characteristics of the isolate and the geographical distribution of the 16S rRNA gene sequences of THSCG in terrestrial hot springs and marine hydrothermal fields. Phylogenetic analysis suggests that the THSCG lineage represented by NAS-02 has gained the ability of sulfur reduction via horizontal gene transfer. Based on the phylogeny and physiology, we propose the name Conexivisphaera calidus gen. nov., sp. nov. to accommodate the isolate.

Conexivisphaera calida gen. nov., sp. nov., a thermophilic sulfur- and iron-reducing archaeon, and proposal of Conexivisphaeraceae fam. nov., Conexivisphaerales ord. nov., and Conexivisphaeria class. nov. in the phylum Thaumarchaeota

“…As consistent with our previous report [22], we confirmed that NAS-02 T was affiliated in THSCG that was located at the basal point of the phylum Thaumarchaeota in the phylogenetic tree of 16S rRNA genes ( Fig. 1a) and in the phylogenomic tree based on 122 archaeal marker proteins (Fig.…”

Community, Distribution, and Ecological Roles of Estuarine Archaea

“…Members of non-AOA can grow in both anaerobic and aerobic conditions, and oxygen may influence the diversity and structure of non-AOA community ( Biggs-Weber et al, 2020 ). Since only few genomes and enrichment cultures for non-AOA Thaumarchaeota are available ( Kato et al, 2019 ), most of their metabolic potentials remain underexplored. Hence, more detailed studies are needed to comprehensively describe their physiology.…”

Gene duplication drives genome expansion in a major lineage of Thaumarchaeota

“…While a substantial number of ecological studies and several cultures and enrichments confirm the ammonia-oxidising activity of Thaumarchaeota, there is also evidence that ammonia oxidation is not universal in this phylum 9 – 13 . In particular, there is evidence that the early-diverging lineages of Thaumarchaeota (including the Group 1.1c, Group 1.3 and pSL12 lineages) do not require ammonia oxidation for growth 10 , 13 , and the ammonia oxidation machinery may have been acquired subsequently to the origin of Thaumarchaeota during, or after, the Great Oxygenation Event 2300 My ago 12 . While oxygen and pH have been recognised as driving forces of massive diversification through their evolutionary history 12 , 14 , the evolutionary mechanisms leading to such high phylogenetic and metabolic diversity have received little attention.…”