Ancestral Absence of Electron Transport Chains in Patescibacteria and DPANN

Jacob P Beam; Eric D Becraft; Julia M Brown; Frederik Schulz; Jessica K Jarett; Oliver Bezuidt; Nicole J Poulton; Kayla Clark; Peter F Dunfield; Nikolai V Ravin; John R Spear; Brian P Hedlund; Konstantinos A Kormas; Stefan M Sievert; Mostafa S Elshahed; Hazel A Barton; Matthew B Stott; Jonathan A Eisen; Duane P Moser; Tullis C Onstott; Tanja Woyke; Ramunas Stepanauskas

doi:10.3389/fmicb.2020.01848

Ancestral Absence of Electron Transport Chains in Patescibacteria and DPANN

Front Microbiol. 2020 Aug 17:11:1848. doi: 10.3389/fmicb.2020.01848. eCollection 2020.

Authors

Jacob P Beam¹, Eric D Becraft¹, Julia M Brown¹, Frederik Schulz², Jessica K Jarett², Oliver Bezuidt¹, Nicole J Poulton¹, Kayla Clark¹, Peter F Dunfield³, Nikolai V Ravin⁴, John R Spear⁵, Brian P Hedlund⁶, Konstantinos A Kormas⁷, Stefan M Sievert⁸, Mostafa S Elshahed⁹, Hazel A Barton¹⁰, Matthew B Stott¹¹, Jonathan A Eisen¹², Duane P Moser¹³, Tullis C Onstott¹⁴, Tanja Woyke², Ramunas Stepanauskas¹

Affiliations

¹ Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, United States.
² Department of Energy Joint Genome Institute, Berkeley, CA, United States.
³ Department of Biological Sciences, University of Calgary, Calgary, AB, Canada.
⁴ Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow, Russia.
⁵ Civil and Environmental Engineering, Colorado School of Mines, Golden, CO, United States.
⁶ School of Life Sciences - Nevada Institute of Personalized Medicine, University of Nevada, Las Vegas, Las Vegas, NV, United States.
⁷ Department of Ichthyology and Aquatic Environment, University of Thessaly, Volos, Greece.
⁸ Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United States.
⁹ Department of Microbiology and Molecular Genetics, Oklahoma State University, Stillwater, OK, United States.
¹⁰ Department of Biology, University of Akron, Akron, OH, United States.
¹¹ School of Biological Sciences, University of Canterbury, Christchurch, New Zealand.
¹² Department of Evolution and Ecology, Department of Medical Microbiology and Immunology, Genome Center, University of California, Davis, Davis, CA, United States.
¹³ Desert Research Institute, Las Vegas, NV, United States.
¹⁴ Department of Geosciences, Princeton University, Princeton, NJ, United States.

Abstract

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.

Keywords: Archaea; Bacteria; evolution; genomics fermentation; oxidoreductases; respiration.

Copyright © 2020 Beam, Becraft, Brown, Schulz, Jarett, Bezuidt, Poulton, Clark, Dunfield, Ravin, Spear, Hedlund, Kormas, Sievert, Elshahed, Barton, Stott, Eisen, Moser, Onstott, Woyke and Stepanauskas.