Ancestral absence of electron transport chains in Patescibacteria and DPANN

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Beam, J. P., Becraft, E. D., Brown, J. M., Schulz, F., Jarett, J. K., Bezuidt, O., Poulton, N. J., Clark, K., Dunfield, P. F., Ravin, N. V., Spear, J. R., Hedlund, B. P., Kormas, K. A., Sievert, S. M., Elshahed, M. S., Barton, H. A., Stott, M. B., Eisen, J. A., Moser, D. P., Onstott, T. C., Woyke, T., & Stepanauskas, R. Ancestral absence of electron transport chains in Patescibacteria and DPANN. Frontiers in Microbiology, 11, (2020): 1848, doi:10.3389/fmicb.2020.01848.
Recent discoveries suggest that the candidate superphyla Patescibacteria and DPANN constitute a large fraction of the phylogenetic diversity of Bacteria and Archaea. Their small genomes and limited coding potential have been hypothesized to be ancestral adaptations to obligate symbiotic lifestyles. To test this hypothesis, we performed cell–cell association, genomic, and phylogenetic analyses on 4,829 individual cells of Bacteria and Archaea from 46 globally distributed surface and subsurface field samples. This confirmed the ubiquity and abundance of Patescibacteria and DPANN in subsurface environments, the small size of their genomes and cells, and the divergence of their gene content from other Bacteria and Archaea. Our analyses suggest that most Patescibacteria and DPANN in the studied subsurface environments do not form specific physical associations with other microorganisms. These data also suggest that their unusual genomic features and prevalent auxotrophies may be a result of ancestral, minimal cellular energy transduction mechanisms that lack respiration, thus relying solely on fermentation for energy conservation.
This work was funded by the USA National Science Foundation grants 1441717, 1826734, and 1335810 (to RS); and 1460861 (REU site at Bigelow Laboratory for Ocean Sciences). RS was also supported by the Simons Foundation grant 510023. TW, FS, and JJ were funded by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility supported under Contract No. DE-AC02-05CH11231. NR group was funded by the Russian Science Foundation (grant 19-14-00245). SS was funded by USA National Science Foundation grants OCE-0452333 and OCE-1136727. BH was funded by NASA Exobiology grant 80NSSC17K0548.