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.

No abstract

Microbial life is surprisingly abundant and diverse in global desert ecosystems. In these environments, microorganisms endure a multitude of physicochemical stresses, including low water potential, carbon and nitrogen starvation, and extreme temperatures. In this review, we summarize our current understanding of the energetic mechanisms and trophic dynamics that underpin microbial function in desert ecosystems. Accumulating evidence suggests that dormancy is a common strategy that facilitates microbial survival in response to water and carbon limitation. Whereas photoautotrophs are restricted to specific niches in extreme deserts, metabolically versatile heterotrophs persist even in the hyper-arid topsoils of the Atacama Desert and Antarctica. At least three distinct strategies appear to allow such microorganisms to conserve energy in these oligotrophic environments: degradation of organic energy reserves, rhodopsin- and bacteriochlorophyll-dependent light harvesting, and oxidation of the atmospheric trace gases hydrogen and carbon monoxide. In turn, these principles are relevant for understanding the composition, functionality, and resilience of desert ecosystems, as well as predicting responses to the growing problem of desertification.

Summary Knowledge regarding mechanisms moderating methane (CH4) sink/source behaviour along the soil–tree stem–atmosphere continuum remains incomplete. Here, we applied stable isotope analysis (δ13C‐CH4) to gain insights into axial CH4 transport and oxidation in two globally distributed subtropical lowland species (Melaleuca quinquenervia and Casuarina glauca). We found consistent trends in CH4 flux (decreasing with height) and δ13C‐CH4 enrichment (increasing with height) in relation to stem height from ground. The average lower tree stem δ13C‐CH4 (0–40 cm) of Melaleuca and Casuarina (−53.96‰ and −65.89‰) were similar to adjacent flooded soil CH4 ebullition (−52.87‰ and −62.98‰), suggesting that stem CH4 is derived mainly by soil sources. Upper stems (81–200 cm) displayed distinct δ13C‐CH4 enrichment (Melaleuca −44.6‰ and Casuarina −46.5‰, respectively). Coupled 3D‐photogrammetry with novel 3D‐stem measurements revealed distinct hotspots of CH4 flux and isotopic fractionation on Melaleuca, which were likely due to bark anomalies in which preferential pathways of gas efflux were enhanced. Diel experiments revealed greater δ13C‐CH4 enrichment and higher oxidation rates in the afternoon, compared with the morning. Overall, we estimated that c. 33% of the methane was oxidised between lower and upper stems during axial transport, therefore potentially representing a globally significant, yet previously unaccounted for, methane sink.