Persistence and resistance: survival mechanisms of Candidatus Dormibacterota from nutrient‐poor Antarctic soils

Abstract

Summary Candidatus Dormibacterota is an uncultured bacterial phylum found predominantly in soil that is present in high abundances within cold desert soils. Here, we interrogate nine metagenome‐assembled genomes (MAGs), including six new MAGs derived from soil metagenomes obtained from two eastern Antarctic sites. Phylogenomic and taxonomic analyses revealed these MAGs represent four genera and five species, representing two order‐level clades within Ca. Dormibacterota. Metabolic reconstructions of these MAGs revealed the potential for aerobic metabolism, and versatile adaptations enabling persistence in the ‘extreme’ Antarctic environment. Primary amongst these adaptations were abilities to scavenge atmospheric H2 and CO as energy sources, as well as using the energy derived from H2 oxidation to fix atmospheric CO2 via the Calvin–Bassham–Benson cycle, using a RuBisCO type IE. We propose that these allow Ca. Dormibacterota to persist using H2 oxidation and grow using atmospheric chemosynthesis in terrestrial Antarctica. Fluorescence in situ hybridization revealed Ca. Dormibacterota to be coccoid cells, 0.3–1.4 μm in diameter, with some cells exhibiting the potential for a symbiotic or syntrophic lifestyle.

Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts

“…Dormibacterota and Ca. Eremiobacterota 62,63 . Of these 25 MAGs, eight also encoded CODH with an active-site loop 61 , The eight MAGs containing all three genes (rbcL1E, hhyL/hylL/hhmL and CODH) belong to the Actinobacteriota (order Mycobacteriales including novel genus QHCD01, and order Solirubrobacterales including novel genus Palsa-465), Chloro exota (two novel genera in the family Ktedonobacteraceae, CF-113 and UBA11361), and Ca.…”

Expanding Antarctic biogeography: microbial ecology of Antarctic island soils

“…This included the bacterial genus Acidibacter and the fungal order Helotiales, members of which have been isolated from acidic biomes (Zijlstra et al 2005, Falagán and Johnson 2014). A potentially important taxon over‐represented in the sub‐Antarctic region was an uncultured bacterium from the Chloroflexi family Ktedonobacteraceae, which has been recently shown to have the ability to persist on atmospheric hydrogen and carbon monoxide (Islam et al 2019), and therefore could play an important role in carbon and energy acquisition in the community by atmospheric chemotrophy (Ji et al 2017, Montgomery et al 2021). It is also notable that an unidentified genus from the Phylum WPS‐2 was also over‐represented in sub‐Antarctic islands; this taxon is also a potential candidate for trace gas scavenging autotrophy.…”

Taxonomic Re-Classification and Expansion of the Phylum Chloroflexota Based on over 5000 Genomes and Metagenome-Assembled Genomes

“…However, a common observation in several studies is that the phylum Chloroflexota and Ca. Dormibacterota appear to be monophyletic [22,28]. For additional genome-based testing on the monophyly of the two lineages, we constructed different phylogenetic trees of the "Terrabacteria" based on 19 marker genes present in at least 10,089 genomes representing a species within the clade.…”

“…The capability of other members of the phylum to successfully cope with low energy fluxes is illustrated by the abundant recovery of various aerobic Chloroflexota among very slow-growing soil bacteria [98], as well as the high prevalence of Ca. Dormibacteria in cold soils [28] and of CL500-11 (Anaerolinea) in the ultraoligotrophic Lake Michigan [9].…”

“…Based on phylogenomics, the phylum is part of the "Terrabacteria" superphylum together with other monoderms [24][25][26], i.e., taxa lacking a lipopolysaccharidecontaining outer membrane, atypical diderms, and potentially the candidate phyla radiation (CPR) [27]. The closest lineage considered to be next to the Chloroflexota is the Candidatus Dormibacterota, which comprises yet-uncultured ubiquitous terrestrial bacteria [28]. Their relative abundance increases in cold soils where they are apparently able to use atmospheric trace gases as electron donors for aerobic respiration [29].…”