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.
Highlights
Cable bacteria are long, multicellular, filamentous micro-organisms that are capable of generating and mediating electrical currents across centimeter-scale distances (Nielsen et al, 2010; Pfeffer et al, 2012; Meysman, 2017)
The Scanning electron microscopy (SEM) images confirmed that the surface of cable bacterium filaments has a conspicuous ultrastructure, as already previously observed (Pfeffer et al, 2012; Malkin et al, 2014)
When cable bacterium filaments were dehydrated in an ethanol series and subsequently critically point dried with carbon dioxide, they retained a rounded cylindrical shape (Figure 1A)
Summary
Multicellular, filamentous micro-organisms that are capable of generating and mediating electrical currents across centimeter-scale distances (Nielsen et al, 2010; Pfeffer et al, 2012; Meysman, 2017). By transporting electrons from cell to cell along the longitudinal axis of their centimeter-long filamentous bodies, cable bacteria can utilize electron donors and electron acceptors in widely segregated locations, which provides them with a competitive advantage for survival in aquatic sediments (Nielsen and Risgaard-Petersen, 2015; Meysman, 2017) This process of long-distance electron transport overthrows some long-held ideas about energy metabolism and entails a whole new type of electrical cooperation between the cells of multicellular organisms (Meysman, 2017). Neither the conductive structures nor the mechanism of electron conduction have been identified
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