Hydrogen-Based Metabolism as an Ancestral Trait in Phyla Related to the Cyanobacteria

Common ancestor of oxygenic cyanobacteria may have been an anaerobe with fermentation and hydrogen metabolism as central metabolic features.

The Science

Bacteria from multiple phyla related to Cyanobacteria were genomically described using metagenomics and single cell genomics, and genes were predicted for all genomes. Metabolic capacities, some featuring novel complexes, were predicted using genome-based analyses. Capacities were mapped across lineages to detect environment- and lineage-specific lifestyles.

The Impact

The results suggest that the common ancestor of all of the phyla investigated may have been an anaerobe in which fermentation and H2 metabolism were central metabolic features. Capacities of phylogenetic neighbors to Cyanobacteria (the group in which oxygenic photosynthesis arose), such as Margulisbacteria, Saganbacteria, Melainabacteria and Sericytochromatia, constrain the metabolic platform in which aerobic respiration arose. The evolution of aerobic respiration was likely linked to the origins of oxygenic Cyanobacteria.

Summary

Margulisbacteria (RBX-1 and ZB3), Saganbacteria (WOR-1), Melainabacteria, and Sericytochromatia, close phylogenetic neighbors to Cyanobacteria, may constrain the metabolic platform in which aerobic respiration arose. In this study, the authors predict that sediment-associated Margulisbacteria have a fermentation-based metabolism featuring a variety of hydrogenases, a streamlined nitrogenase, and electron bifurcating complexes involved in cycling of reducing equivalents. The genomes of ocean-associated Margulisbacteria encode an electron transport chain that may support aerobic growth. Some Saganbacteria genomes encode various hydrogenases, and others may have the ability to use O2 under certain conditions via a putative novel type of heme copper O2 reductase. Similarly, Melainabacteria have diverse energy metabolisms and are capable of fermentation and aerobic or anaerobic respiration. The ancestor of all of these groups may have been an anaerobe in which fermentation and H2 metabolism were central metabolic features. The ability to use O2 as a terminal electron acceptor must have been subsequently acquired by these lineages.

Principal Investigator

Jillian Banfield
University of California, Berkeley
jbanfield@berkeley.edu

Program Manager

Paul Bayer
U.S. Department of Energy Office of Science, Office of Biological and Environmental Research
Earth and Environmental Systems Sciences Division (SC-33.1)
Environmental System Science and DOE Environmental Molecular Sciences Laboratory
paul.bayer@science.doe.gov

Funding

This work was supported by the Office of Biological and Environmental Research within the U.S. Department of Energy Office of Science.

References

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P. B. Matheus Carnevali, F. Schulz, C. J. Castelle, R. S. Kantor, P. M. Shih, I. Sharon, J. M. Santini, M.R. Olm, Y. Amano, B.C. Thomas, K. Anantharaman, D. Burnstein, E. D. Becraft, R. Stepanauskas, T. Woyke, and J. F. Banfield. "Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria". Nature Communications 10  463  (2019). https://doi.org/10.1038/s41467-018-08246-y,