The Cell Envelope Structure of Cable Bacteria

Open Access

Abstract

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 by combining different sample preparation methods (chemical fixation, resin-embedding, and cryo-fixation) with a portfolio of imaging techniques (scanning electron microscopy, transmission 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 were 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. ; This research was financially supported by the European Research Council under the European Union's Seventh Framework Program (FP/2007-2013) through ERC Grant 306933 (FM), the Research Foundation Flanders (FWO project grant G031416N to FM and JM), and the Netherlands Organization for Scientific Research (VICI grant 016.VICI.170.072 to FM). RB is supported by an aspirant grant from Research Foundation Flanders. LN, AB, LD, and TB were supported by the Danish Council for Independent Research, Technology and Production Sciences—project on Microcable-based Nanoelectronics and the Danish National Research Foundation Center of Excellence CEM—Center for Electromicrobiology.