Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide

Zahra Fatima Islam, Paul Rodrigo Cordero, Joanna Feng, Ya-Jou Chen, Sean Keith Bay, Thanavit Jirapanjawat, Roslyn M Gleadow, Carlo C. Carere, Matthew Sttot, Eleonora Chiri, Christopher Andrew Greening

Research output: Contribution to journalArticleResearchpeer-review

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 (H 2 ), carbon monoxide (CO), and sulfur compound oxidation were significantly upregulated. Gas chromatography and microsensor experiments showed that T. roseum aerobically respires H 2 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 H 2 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 H 2 oxidation. This adds to the growing body of evidence that atmospheric trace gases are dependable energy sources for bacterial persistence.

Original languageEnglish
Pages (from-to)1801-1813
Number of pages13
JournalISME Journal
Volume13
Issue number7
DOIs
Publication statusPublished - 1 Jul 2019

Cite this

Islam, Zahra Fatima ; Cordero, Paul Rodrigo ; Feng, Joanna ; Chen, Ya-Jou ; Bay, Sean Keith ; Jirapanjawat, Thanavit ; Gleadow, Roslyn M ; Carere, Carlo C. ; Sttot, Matthew ; Chiri, Eleonora ; Greening, Christopher Andrew. / Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide. In: ISME Journal. 2019 ; Vol. 13, No. 7. pp. 1801-1813.
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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 (H 2 ), carbon monoxide (CO), and sulfur compound oxidation were significantly upregulated. Gas chromatography and microsensor experiments showed that T. roseum aerobically respires H 2 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 H 2 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 H 2 oxidation. This adds to the growing body of evidence that atmospheric trace gases are dependable energy sources for bacterial persistence.",
author = "Islam, {Zahra Fatima} and Cordero, {Paul Rodrigo} and Joanna Feng and Ya-Jou Chen and Bay, {Sean Keith} and Thanavit Jirapanjawat and Gleadow, {Roslyn M} and Carere, {Carlo C.} and Matthew Sttot and Eleonora Chiri and Greening, {Christopher Andrew}",
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Islam, ZF, Cordero, PR, Feng, J, Chen, Y-J, Bay, SK, Jirapanjawat, T, Gleadow, RM, Carere, CC, Sttot, M, Chiri, E & Greening, CA 2019, 'Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide' ISME Journal, vol. 13, no. 7, pp. 1801-1813. https://doi.org/10.1038/s41396-019-0393-0

Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide. / Islam, Zahra Fatima; Cordero, Paul Rodrigo; Feng, Joanna; Chen, Ya-Jou; Bay, Sean Keith; Jirapanjawat, Thanavit; Gleadow, Roslyn M; Carere, Carlo C.; Sttot, Matthew; Chiri, Eleonora; Greening, Christopher Andrew.

In: ISME Journal, Vol. 13, No. 7, 01.07.2019, p. 1801-1813.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Islam, Zahra Fatima

AU - Cordero, Paul Rodrigo

AU - Feng, Joanna

AU - Chen, Ya-Jou

AU - Bay, Sean Keith

AU - Jirapanjawat, Thanavit

AU - Gleadow, Roslyn M

AU - Carere, Carlo C.

AU - Sttot, Matthew

AU - Chiri, Eleonora

AU - Greening, Christopher Andrew

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