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On the evolution and physiology of cable bacteria.
Proc Natl Acad Sci U S A. 2019 09 17; 116(38):19116-19125.PN

Abstract

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.

Authors+Show Affiliations

Section for Microbiology & Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus, Denmark.Section for Microbiology & Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus, Denmark. Energy, Mining and Environment Research Centre, National Research Council Canada, Montreal, QC H4P 2R2, Canada.Section for Microbiology & Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus, Denmark. Center for Electromicrobiology, Aarhus University, 8000 Aarhus, Denmark.Center for Electromicrobiology, Aarhus University, 8000 Aarhus, Denmark. Interdisciplinary Nanoscience Center & Department of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, Denmark.Section for Microbiology & Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus, Denmark. Center for Electromicrobiology, Aarhus University, 8000 Aarhus, Denmark.Section for Microbiology & Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus, Denmark. Department of Biological Oceanography, Leibniz Institute for Baltic Sea Research, Warnemünde (IOW), 18119 Rostock, Germany.Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, 9220 Aalborg, Denmark.Section for Microbiology & Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus, Denmark.Section for Microbiology & Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus, Denmark. Center for Electromicrobiology, Aarhus University, 8000 Aarhus, Denmark.Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, 9220 Aalborg, Denmark.Centre for Microbiology and Environmental Systems Science, University of Vienna, 1090 Vienna, Austria.Interdisciplinary Nanoscience Center & Department of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, Denmark.Environmental Engineering and Water Technology (EEWT) Department, IHE Delft Institute for Water Education, 2611 AX Delft, The Netherlands.Department of Biology, University of Antwerp, 2610 Wilrijk (Antwerpen), Belgium.Department of Biology, University of Antwerp, 2610 Wilrijk (Antwerpen), Belgium. Department of Biotechnology, Delft University of Technology, 2629 HZ Delft, The Netherlands.Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, 9220 Aalborg, Denmark. Centre for Microbiology and Environmental Systems Science, University of Vienna, 1090 Vienna, Austria.Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, 9220 Aalborg, Denmark.Section for Microbiology & Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus, Denmark. Center for Electromicrobiology, Aarhus University, 8000 Aarhus, Denmark.Section for Microbiology & Center for Geomicrobiology, Department of Bioscience, Aarhus University, 8000 Aarhus, Denmark; andreas.schramm@bios.au.dk. Center for Electromicrobiology, Aarhus University, 8000 Aarhus, Denmark.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

31427514

Citation

Kjeldsen, Kasper U., et al. "On the Evolution and Physiology of Cable Bacteria." Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 38, 2019, pp. 19116-19125.
Kjeldsen KU, Schreiber L, Thorup CA, et al. On the evolution and physiology of cable bacteria. Proc Natl Acad Sci U S A. 2019;116(38):19116-19125.
Kjeldsen, K. U., Schreiber, L., Thorup, C. A., Boesen, T., Bjerg, J. T., Yang, T., Dueholm, M. S., Larsen, S., Risgaard-Petersen, N., Nierychlo, M., Schmid, M., Bøggild, A., van de Vossenberg, J., Geelhoed, J. S., Meysman, F. J. R., Wagner, M., Nielsen, P. H., Nielsen, L. P., & Schramm, A. (2019). On the evolution and physiology of cable bacteria. Proceedings of the National Academy of Sciences of the United States of America, 116(38), 19116-19125. https://doi.org/10.1073/pnas.1903514116
Kjeldsen KU, et al. On the Evolution and Physiology of Cable Bacteria. Proc Natl Acad Sci U S A. 2019 09 17;116(38):19116-19125. PubMed PMID: 31427514.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - On the evolution and physiology of cable bacteria. AU - Kjeldsen,Kasper U, AU - Schreiber,Lars, AU - Thorup,Casper A, AU - Boesen,Thomas, AU - Bjerg,Jesper T, AU - Yang,Tingting, AU - Dueholm,Morten S, AU - Larsen,Steffen, AU - Risgaard-Petersen,Nils, AU - Nierychlo,Marta, AU - Schmid,Markus, AU - Bøggild,Andreas, AU - van de Vossenberg,Jack, AU - Geelhoed,Jeanine S, AU - Meysman,Filip J R, AU - Wagner,Michael, AU - Nielsen,Per H, AU - Nielsen,Lars Peter, AU - Schramm,Andreas, Y1 - 2019/08/19/ PY - 2019/8/21/pubmed PY - 2020/4/11/medline PY - 2019/8/21/entrez KW - cable bacteria KW - electromicrobiology KW - microbial evolution KW - microbial genome KW - microbial physiology SP - 19116 EP - 19125 JF - Proceedings of the National Academy of Sciences of the United States of America JO - Proc Natl Acad Sci U S A VL - 116 IS - 38 N2 - 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. SN - 1091-6490 UR - https://www.unboundmedicine.com/medline/citation/31427514/On_the_evolution_and_physiology_of_cable_bacteria_ L2 - http://www.pnas.org/cgi/pmidlookup?view=long&pmid=31427514 DB - PRIME DP - Unbound Medicine ER -