On the evolution and physiology of cable bacteria

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  • Kasper U Kjeldsen
  • Lars Schreiber, Energy, Mining and Environment Research Centre, National Research Council Canada, Montreal, QC H4P 2R2, Canada.
  • ,
  • Casper A Thorup
  • Thomas Boesen
  • Jesper T Bjerg
  • Tingting Yang, Department of Biological Oceanography, Leibniz Institute for Baltic Sea Research, Warnemünde (IOW), 18119 Rostock, Germany.
  • ,
  • Morten S Dueholm, Center for Microbial Communities, Department of Chemistry and Biosciences, Aalborg University
  • ,
  • Steffen Larsen
  • ,
  • Nils Risgaard-Petersen
  • Marta Nierychlo, Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, 9220 Aalborg, Denmark.
  • ,
  • Markus Schmid, Centre for Microbiology and Environmental Systems Science, University of Vienna, 1090 Vienna, Austria.
  • ,
  • Andreas Bøggild
  • Jack van de Vossenberg, Environmental Engineering and Water Technology (EEWT) Department, IHE Delft Institute for Water Education, 2611 AX Delft, The Netherlands.
  • ,
  • Jeanine S Geelhoed, Department of Biology, University of Antwerp, 2610 Wilrijk (Antwerpen), Belgium.
  • ,
  • Filip J R Meysman
  • Michael Wagner, Centre for Microbiology and Environmental Systems Science, University of Vienna, 1090 Vienna, Austria., Center for Microbial Communities, Department of Chemistry and Biosciences, Aalborg University
  • ,
  • Per H Nielsen, Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, 9220 Aalborg, Denmark.
  • ,
  • Lars Peter Nielsen
  • Andreas Schramm

Cable bacteria of the family Desulfobulbaceae form centimeter-long filaments comprising thousands of cells. They occur worldwide in the surface of aquatic sediments, where they connect sulfide oxidation with oxygen or nitrate reduction via long-distance electron transport. In the absence of pure cultures, we used single-filament genomics and metagenomics to retrieve draft genomes of 3 marine Candidatus Electrothrix and 1 freshwater Ca. Electronema species. These genomes contain >50% unknown genes but still share their core genomic makeup with sulfate-reducing and sulfur-disproportionating Desulfobulbaceae, with few core genes lost and 212 unique genes (from 197 gene families) conserved among cable bacteria. Last common ancestor analysis indicates gene divergence and lateral gene transfer as equally important origins of these unique genes. With support from metaproteomics of a Ca. Electronema enrichment, the genomes suggest that cable bacteria oxidize sulfide by reversing the canonical sulfate reduction pathway and fix CO2 using the Wood-Ljungdahl pathway. Cable bacteria show limited organotrophic potential, may assimilate smaller organic acids and alcohols, fix N2, and synthesize polyphosphates and polyglucose as storage compounds; several of these traits were confirmed by cell-level experimental analyses. We propose a model for electron flow from sulfide to oxygen that involves periplasmic cytochromes, yet-unidentified conductive periplasmic fibers, and periplasmic oxygen reduction. This model proposes that an active cable bacterium gains energy in the anodic, sulfide-oxidizing cells, whereas cells in the oxic zone flare off electrons through intense cathodic oxygen respiration without energy conservation; this peculiar form of multicellularity seems unparalleled in the microbial world.

OriginalsprogEngelsk
TidsskriftProceedings of the National Academy of Sciences of the United States of America
Vol/bind116
Nummer38
Sider (fra-til)19116-19125
Antal sider10
ISSN0027-8424
DOI
StatusUdgivet - 17 sep. 2019

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