Aerobic soil bacteria adapt to hypoxia by hybridizing fermentation with carbon storage
Abstract
In soil ecosystems, aerobic bacteria survive oxygen deprivation (hypoxia) by entering nonreplicative persistent states. In contrast to the well-studied metabolism of obligate and facultative anaerobes, little is known about how obligately aerobic bacteria adapt their metabolism to stay viable during hypoxia. The model obligate aerobe Mycobacterium smegmatis maintains redox homeostasis during hypoxia by mediating fermentative hydrogen production. However, the fate of organic carbon during fermentation is unresolved. Here we systematically profiled the metabolism of M. smegmatis during aerobic growth, hypoxic persistence, and the transition between these states. By integrating a differentially 13 C-labeled glucose isotopologue assay with paired metabolomics and proteomics, we observed M. smegmatis rerouted central carbon metabolism through the pentose phosphate pathway and/or Entner–Doudoroff pathways during hypoxia, while excreting high levels of hydrogen and acetate. Lipid and cryoelectron tomography analyses suggest M. smegmatis also stores carbon as glycerides in lipid droplets during hypoxia, which serve as a major reductant sink. Gene knockouts and knockdowns revealed that, while M. smegmatis depends on its hydrogen-producing hydrogenase for hypoxic survival, it can compensate for the disruption of acetate production and glyceride synthesis by producing and excreting other organic acids. We confirmed through an extensive genomic survey and biogeochemical measurements that diverse aerobic soil bacteria can store organic carbon and mediate fermentation during hypoxia. Altogether, this hybrid fermentative metabolism likely provides a competitive advantage in soils and other resource-variable environments by enabling bacteria, such as M. smegmatis , to simultaneously dispose excess reductant and maintain carbon stores during hypoxia.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (26)
David L. Gillett
Department of Microbiology, Monash University
Thilini Koralegedara
Department of Microbiology, Monash University
Tess F. Hutchinson
Department of Microbiology, Monash University
Thanh Nguyen-Dinh
Department of Microbiology, Monash University
Thomas D. Watts
Department of Microbiology, Monash University
Jessica Solari
Department of Microbiology, Monash University
Manasi Mudaliyar
Department of Biochemistry and Pharmacology, Bio21 Institute, The University of Melbourne
William J. Jowsey
Department of Microbiology and Immunology, University of Otago
Nadeesha Athukorala
Department of Microbiology, Monash University
Wei Wen Wong
Water Studies, School of Chemistry, Monash University
Jake U. S. Locop
Department of Microbiology, Monash University
Ning Hall
Department of Microbiology, Monash University
Luis Jimenez
Department of Microbiology, Monash University
Iresha Hanchapola
Monash Proteomics and Metabolomics Platform, Department of Biochemistry and Molecular Biology, Monash Biomedicine Discovery Institute, Monash University
Han-Chung Lee
Monash Proteomics and Metabolomics Platform, Department of Biochemistry and Molecular Biology, Monash Biomedicine Discovery Institute, Monash University
Erwin Tanuwidjaya
Monash Proteomics and Metabolomics Platform, Department of Biochemistry and Molecular Biology, Monash Biomedicine Discovery Institute, Monash University
Joel R. Steele
Monash Proteomics and Metabolomics Platform, Department of Biochemistry and Molecular Biology, Monash Biomedicine Discovery Institute, Monash University
Ralf B. Schittenhelm
Monash Proteomics and Metabolomics Platform, Department of Biochemistry and Molecular Biology, Monash Biomedicine Discovery Institute, Monash University
Christopher K. Barlow
Rhys Grinter
Department of Microbiology, Biomedicine Discovery Institute, Monash University
Gregory M. Cook
Department of Microbiology and Immunology, University of Otago
Matthew B. McNeil
Department of Microbiology and Immunology, University of Otago
Debnath Ghosal
Department of Biochemistry and Pharmacology, Bio21 Institute, The University of Melbourne
Pok Man Leung
Department of Microbiology, Biomedicine Discovery Institute, Monash University
Perran L. M. Cook
Water Studies, School of Chemistry, Monash University
Chris Greening