Candidatus Eremiobacterota, a metabolically and phylogenetically diverse terrestrial phylum with acid-tolerant adaptations

Abstract

Candidatus phylum Eremiobacterota (formerly WPS-2) is an as-yet-uncultured bacterial clade that takes its name from Ca. Eremiobacter, an Antarctic soil aerobe proposed to be capable of a novel form of chemolithoautotrophy termed atmospheric chemosynthesis, that uses the energy derived from atmospheric H 2 -oxidation to fix CO 2 through the Calvin-Benson-Bassham (CBB) cycle via type 1E RuBisCO. To elucidate the phylogenetic affiliation and metabolic capacities of Ca. Eremiobacterota, we analysed 63 public metagenome-assembled genomes (MAGs) and nine new MAGs generated from Antarctic soil metagenomes. These MAGs represent both recognized classes within Ca. Eremiobacterota, namely Ca. Eremiobacteria and UBP9. Ca. Eremiobacteria are inferred to be facultatively acidophilic with a preference for peptides and amino acids as nutrient sources. Epifluorescence microscopy revealed Ca. Eremiobacteria cells from Antarctica desert soil to be coccoid in shape. Two orders are recognized within class Ca. Eremiobacteria: Ca. Eremiobacterales and Ca. Baltobacterales. The latter are metabolically versatile, with individual members having genes required for trace gas driven autotrophy, anoxygenic photosynthesis, CO oxidation, and anaerobic respiration. UBP9, here renamed Ca. Xenobia class. nov., are inferred to be obligate heterotrophs with acidophilic adaptations, but individual members having highly divergent metabolic capacities compared to Ca. Eremiobacteria, especially with regard to respiration and central carbon metabolism. We conclude Ca. Eremiobacterota to be an ecologically versatile phylum with the potential to thrive under an array of "extreme" environmental conditions.

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.…”

“…Amino acid sequences encoding the 1m [NiFe]-hydrogenase small subunit (hhmS) and large subunits (hhmL), as well as the surrounding genes were extracted from four of the MAGs assembled in this study (bin #: 90,63,45,35). All sequences were submitted to ExPASy BLAST (using the 'UniProtKB/Swiss-Prot only' option) 126 and to InterProScan 127 to identify functional domains, and potential subcellular location (e.g., transmembrane helices).…”

“…Several recently proposed bacterial candidate phyla were also represented by MAGs including Ca. Eremiobacterota 29 , Ca. Dormibacterota 30 , Ca.…”

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

“…Abundances of the set of dereplicated MAGs were calculated, with CoverM used for clustering and dereplication (‐‐precluster‐method dashing, ‐‐ani 95). Reads were then mapped and abundances were calculated following methods used for the full set of MAGs (Ji et al ., 2017; Ji et al ., 2021).…”

Prokaryotic communities in the historic silver mine Reiche Zeche

“…It was shown by metagenomics analysis that members of Ca. Eremiobacterota are well adapted to survive under extreme conditions in a diverse range of environments, including acidic, oligotrophic, and metal-rich habitats (Ji et al 2021 ). Ca.…”