The growth and survival of Mycobacterium smegmatis is enhanced by co-metabolism of atmospheric H2

Chris Greening, Silas G. Villas-Bôas, Jennifer R. Robson, Michael Berney, Gregory M. Cook

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

The soil bacterium Mycobacterium smegmatis is able to scavenge the trace concentrations of H2 present in the atmosphere, but the physiological function and importance of this activity is not understood. We have shown that atmospheric H2 oxidation in this organism depends on two phylogenetically and kinetically distinct high-affinity hydrogenases, Hyd1 (MSMEG-2262-2263) and Hyd2 (MSMEG-2720-2719). In this study, we explored the effect of deleting Hyd2 on cellular physiology by comparing the viability, energetics, transcriptomes, and metabolomes of wild-type vs. Δhyd2 cells. The long-term survival of the Δhyd2 mutant was significantly reduced compared to the wild-type. The mutant additionally grew less efficiently in a range of conditions, most notably during metabolism of short-chain fatty acids; there was a twofold reduction in growth rate and growth yield of the Δhyd2 strain when acetate served as the sole carbon source. Hyd1 compensated for loss of Hyd2 when cells were grown in a high H2 atmosphere. Analysis of cellular parameters showed that Hyd2 was not necessary to generate the membrane potential, maintain intracellular pH homeostasis, or sustain redox balance. However, microarray analysis indicated that Δhyd2 cells were starved for reductant and compensated by rewiring central metabolism; transcripts encoding proteins responsible for oxidative decarboxylation pathways, the urea cycle, and ABC transporter-mediated import were significantly more abundant in the Δhyd2 mutant. Metabolome profiling consistently revealed an increase in intracellular amino acids in the Δhyd2 mutant. We propose that atmospheric H2 oxidation has two major roles in mycobacterial cells: to generate reductant during mixotrophic growth and to sustain the respiratory chain during dormancy.

Original languageEnglish (US)
Article numbere103034
JournalPLoS One
Volume9
Issue number7
DOIs
StatePublished - Jul 24 2014

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Mycobacterium smegmatis
Reducing Agents
Metabolism
Hydrogenase
metabolome
Oxidation
mutants
metabolism
ATP-Binding Cassette Transporters
reducing agents
Metabolome
Volatile Fatty Acids
Physiology
Microarrays
Growth
Atmosphere
Urea
Bacteria
Acetates
Carbon

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

The growth and survival of Mycobacterium smegmatis is enhanced by co-metabolism of atmospheric H2. / Greening, Chris; Villas-Bôas, Silas G.; Robson, Jennifer R.; Berney, Michael; Cook, Gregory M.

In: PLoS One, Vol. 9, No. 7, e103034, 24.07.2014.

Research output: Contribution to journalArticle

Greening, Chris ; Villas-Bôas, Silas G. ; Robson, Jennifer R. ; Berney, Michael ; Cook, Gregory M. / The growth and survival of Mycobacterium smegmatis is enhanced by co-metabolism of atmospheric H2. In: PLoS One. 2014 ; Vol. 9, No. 7.
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