Microaerobic Lifestyle at Nanomolar O-2 Concentrations Mediated by Low-Affinity Terminal Oxidases in Abundant Soil Bacteria
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2021-07
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Journal Article
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Abstract
High-affinity terminal oxidases (TOs) are believed to permit microbial respiration at low oxygen (O-2) levels. Genes encoding such oxidases are widespread, and their existence in microbial genomes is taken as an indicator for microaerobic respiration. We combined respiratory kinetics determined via highly sensitive optical trace O-2 sensors, genomics, and transcriptomics to test the hypothesis that high-affinity TOs are a prerequisite to respire micro- and nanooxic concentrations of O-2 in environmentally relevant model soil organisms: acidobacteria. Members of the Acidobacteria harbor branched respiratory chains terminating in low-affinity (caa(3)-type cytochrome c oxidases) as well as high-affinity (cbb(3)-type cytochrome c oxidases and/or bd-type quinol oxidases) TOs, potentially enabling them to cope with varying O(2 )concentrations. The measured apparent K-m (K-m(app())) values for O(2 )of selected strains ranged from 37 to 288 nmol O(2 )liter(-1), comparable to values previously assigned to low-affinity TOs. Surprisingly, we could not detect the expression of the conventional high-affinity TO (cbb3 type) at micro- and nanomolar O(2 )concentrations but detected the expression of low-affinity TOs. To the best of our knowledge, this is the first observation of microaerobic respiration imparted by low-affinity TOs at O-2 concentrations as low as 1 nM. This challenges the standing hypothesis that a microaerobic lifestyle is exclusively imparted by the presence of high-affinity TOs. As low-affinity TOs are more efficient at generating ATP than high-affinity TOs, their utilization could provide a great benefit, even at low-nanomolar O(2 )levels. Our findings highlight energy conservation strategies that could promote the success of Acidobacteria in soil but might also be important for as-yet-unrevealed microorganisms.
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6 (4)
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American Society for Microbiology
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terminal oxidase; oxygen; acidobacteria; kinetics; transcriptomics