The Chloroflexi supergroup is metabolically diverse and representatives have novel genes for non-photosynthesis based CO₂ fixation

Abstract

The Chloroflexi superphylum have been investigated primarily from the perspective of reductive dehalogenation of toxic compounds, anaerobic photosynthesis and wastewater treatment, but remain relatively little studied compared to their close relatives within the larger Terrabacteria group, including Cyanobacteria, Actinobacteria, and Firmicutes. Here, we conducted a detailed phylogenetic analysis of the phylum Chloroflexota, the phylogenetically proximal candidate phylum Dormibacteraeota, and a newly defined sibling phylum proposed in the current study, Eulabeiota. These groups routinely root together in phylogenomic analyses, and constitute the Chloroflexi supergroup. Chemoautotrophy is widespread in Chloroflexi. Two Form I Rubisco ancestral subtypes that both lack the small subunit are prevalent in ca. Eulabeiota and Chloroflexota, suggesting that the predominant modern pathway for CO2 fixation evolved in these groups. The single subunit Form I Rubiscos are inferred to have evolved prior to oxygenation of the Earth's atmosphere and now predominantly occur in anaerobes. Prevalent in both Chloroflexota and ca. Eulabeiota are capacities related to aerobic oxidation of gases, especially CO and H2. In fact, aerobic and anaerobic CO dehydrogenases are widespread throughout every class-level lineage, whereas traits such as denitrification and reductive dehalogenation are heterogeneously distributed across the supergroup. Interestingly, some Chloroflexota have a novel clade of group 3 NiFe hydrogenases that is phylogenetically distinct from previously reported groups. Overall, the analyses underline the very high level of metabolic diversity in the Chloroflexi supergroup, suggesting the ancestral metabolic platform for this group enabled highly varied adaptation to ecosystems that appeared in the aerobic world.

Evolution of increased complexity and specificity at the dawn of form I Rubiscos

“…Interactions, dependencies, and catalytic properties of AncL and AncLS were qualitatively unchanged when validating their robustness to statistical uncertainty ( 31 ). Moreover, inferences of AncLS’s stoichiometry and SSU dependence were unchanged when AncLS was reconstructed using an alternative phylogeny ( 29 ) (figs. S6, S7, and S8 and supplementary text).…”

“…S1 and S2). On the LSU phylogeny, three clades of orthologs branch on the stem lineage toward form I Rubiscos (form I-α, form I′, and form I′′) ( 13 , 29 ). These orthologs were identified from metagenome-assembled genomes (MAGs), which do not encode SSUs (fig.…”

Global patterns of diversity and metabolism of microbial communities in deep-sea hydrothermal vent deposits

“…For example, putative homologs of the PKD repeat containing protein (MBS8122536.1), a hypothetical protein While the Patescibacteria likely rely on symbiotic or parasitic relationships, members of the Chloroflexota phylum are diverse and metabolically flexible organisms, capable of thriving in a wide variety of geochemical niches. Chloroflexota are abundant and widely distributed in a variety of environments, including terrestrial soils, sediments and groundwater, freshwater, pelagic oceans, and the marine subseafloor and sediments [49][50][51][52][53][54][55], and hydrothermal settings such as Guaymas Basin [11] and Brothers submarine volcano [8]. Genomic evidence suggests that Chloroflexota are associated with important metabolisms in the carbon cycle, including fermentation, carbon fixation, acetogenesis and the utilization of sugars, polymers, fatty acids, organic acids and other organic carbon compounds [50,51,54].…”

“…Chloroflexota are abundant and widely distributed in a variety of environments, including terrestrial soils, sediments and groundwater, freshwater, pelagic oceans, and the marine subseafloor and sediments [49][50][51][52][53][54][55], and hydrothermal settings such as Guaymas Basin [11] and Brothers submarine volcano [8]. Genomic evidence suggests that Chloroflexota are associated with important metabolisms in the carbon cycle, including fermentation, carbon fixation, acetogenesis and the utilization of sugars, polymers, fatty acids, organic acids and other organic carbon compounds [50,51,54].…”

Global patterns of diversity and metabolism of microbial communities in deep-sea hydrothermal vent deposits

“…While the Patescibacteria likely rely on symbiotic or parasitic relationships, members of the Chloro exota phylum are diverse and metabolically exible organisms, capable of thriving in a wide variety of geochemical niches. Chloro exota are abundant and widely distributed in a variety of environments, including terrestrial soils, sediments and groundwater, freshwater, pelagic oceans, and the marine subsea oor and sediments [49][50][51][52][53][54][55], and hydrothermal settings such as Guaymas Basin [11] and Brothers submarine volcano [8]. Genomic evidence suggests that Chloro exota are associated with important metabolisms in the carbon cycle, including fermentation, carbon xation, acetogenesis and the utilization of sugars, polymers, fatty acids, organic acids and other organic carbon compounds [50,51,54].…”