Abstract
Most aerobic bacteria exist in dormant states within natural environments. In these states, they endure adverse environmental conditions such as nutrient starvation by decreasing metabolic expenditure and using alternative energy sources. In this study, we investigated the energy sources that support persistence of two aerobic thermophilic strains of the environmentally widespread but understudied phylum Chloroflexi. A transcriptome study revealed that Thermomicrobium roseum (class Chloroflexia) extensively remodels its respiratory chain upon entry into stationary phase due to nutrient limitation. Whereas primary dehydrogenases associated with heterotrophic respiration were downregulated, putative operons encoding enzymes involved in molecular hydrogen (H2), carbon monoxide (CO), and sulfur compound oxidation were significantly upregulated. Gas chromatography and microsensor experiments showed that T. roseum aerobically respires H2 and CO at a range of environmentally relevant concentrations to sub-atmospheric levels. Phylogenetic analysis suggests that the hydrogenases and carbon monoxide dehydrogenases mediating these processes are widely distributed in Chloroflexi genomes and have probably been horizontally acquired on more than one occasion. Consistently, we confirmed that the sporulating isolate Thermogemmatispora sp. T81 (class Ktedonobacteria) also oxidises atmospheric H2 and CO during persistence, though further studies are required to determine if these findings extend to mesophilic strains. This study provides axenic culture evidence that atmospheric CO supports bacterial persistence and reports the third phylum, following Actinobacteria and Acidobacteria, to be experimentally shown to mediate the biogeochemically and ecologically important process of atmospheric H2 oxidation. This adds to the growing body of evidence that atmospheric trace gases are dependable energy sources for bacterial persistence.
Highlights
Bacteria from the phylum Chloroflexi are widespread and abundant in free-living microbial communities [1,2,3,4]
We compared the transcriptomes of triplicate T. roseum cultures under nutrient-rich and nutrient-limited conditions
Two primary respiratory dehydrogenases involved in heterotrophic growth were downregulated, whereas complexes involved in lithotrophic energy generation and a succinate dehydrogenase were upregulated (Fig. 1a; Table S1)
Summary
Bacteria from the phylum Chloroflexi are widespread and abundant in free-living microbial communities [1,2,3,4]. While H2 oxidation has yet to be reported in aerobic heterotrophic Chloroflexi, strains of the phylum are known to encode the high-affinity group 1h [NiFe]hydrogenase [24, 27] This enzyme class has been shown to support bacterial persistence by mediating oxidation of atmospheric H2 (0.53 ppmv) [26, 28,29,30,31,32,33,34,35,36]. We focused primarily on Thermomicrobium roseum (class Chloroflexia, formerly class Thermomicrobia [6]), a strain originally isolated from Toadstool Spring of Yellowstone National Park, USA [10] This obligately aerobic bacterium is known to grow heterotrophically on a variety of carbohydrates, organic acids, and proteinaceous substrates [10, 13, 21]. Our results demonstrate that atmospheric H2 and CO serve as important energy sources that support the persistence of members of this phylum
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