Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 116, Issue 38, Pages 19116-19125Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.1903514116
Keywords
electromicrobiology; microbial genome; cable bacteria; microbial evolution; microbial physiology
Categories
Funding
- European Research Council [291650, 306933]
- Danish National Research Foundation [DNRF104, DNRF136]
- Research Foundation Flanders (FWO) [G031416N]
- Netherlands Organisation for Scientific Research (Vici Grant) [016.VICI.170.072]
- Danish Council for Independent Research \ Natural Sciences & Technology and Production Sciences
- European Research Council (ERC) [306933, 291650] Funding Source: European Research Council (ERC)
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Cable bacteria of the family Desulfobulbaceae form centimeter-long filaments comprising thousands of cells. They occur world-wide 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 N-2, 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.
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