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Front. Microbiol. | doi: 10.3389/fmicb.2018.03044

The Cell Envelope Structure of Cable Bacteria

  • 1X-LAB, University of Hasselt, Belgium
  • 2Department of Bioscience, Faculty of Science and Technology, Aarhus University, Denmark
  • 3Interdisciplinary Nanoscience Centre (iNANO), Faculty of Science and Technology, Aarhus University, Denmark
  • 4Department of Cell and Chemical Biology, Leiden University Medical Center, Netherlands
  • 5Flanders Institute for Biotechnology, Belgium
  • 6Department of Biology, University of Antwerp, Belgium
  • 7Department of Marine Sciences, University of Gothenburg, Sweden
  • 8Department of Biotechnology, Delft University of Technology, Netherlands
  • 9IMO IMOMEC, Belgium

Cable bacteria are long, multicellular micro-organisms that are capable of transporting electrons from cell to cell along the longitudinal axis of their centimeter-long filaments. The conductive structures that mediate this long-distance electron transport are thought to be located in the cell envelope. Therefore, this study examines in detail the architecture of the cell envelope of cable bacterium filaments through a combination of classical electron microscopy, cryo-based electron microscopy and tomography, focused ion beam-scanning electron microscopy and atomic force microscopy. We systematically imaged intact filaments with varying diameters. In addition, we investigated the periplasmic fiber sheath that remains after the cytoplasm and membranes have been removed by chemical extraction. Based on these investigations, we present a quantitative structural model of a cable bacterium. Cable bacteria build their cell envelope by a parallel concatenation of ridge compartments that have a standard size. Larger diameter filaments simply incorporate more parallel ridge compartments. Each ridge compartment contains a ~50 nm diameter fiber in the periplasmic space. These fibers are continuous across cell-to-cell junctions, which display a conspicuous cartwheel structure that is likely made by invaginations of the outer cell membrane around the periplasmic fibers. The continuity of the periplasmic fibers across cells makes them a prime candidate for the sought-after electron conducting structure in cable bacteria.

Keywords: cable bacteria, Long-distance electron transfer, Cell envelope, periplasmic fibers, Electron microscopy, Atomic Force Microscopy

Received: 12 Jul 2018; Accepted: 26 Nov 2018.

Edited by:

Marc Bramkamp, Ludwig Maximilian University of Munich, Germany

Reviewed by:

Ida Helene Steen, University of Bergen, Norway
Reinhard Rachel, University of Regensburg, Germany  

Copyright: © 2018 Cornelissen, Boggild, Thiruvallur Eachambadi, Koning, Kremer, Hidalgo Martinez, Zetsche, Bonné, Drijkoningen, Geelhoed, Boesen, Boschker, Valcke, Nielsen, D'Haen, Manca and Meysman. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Filip J. Meysman, Department of Biology, University of Antwerp, Antwerp, Antwerp, Belgium, Filip.Meysman@uantwerpen.be