Search bioRxiv⌕ Search

Biology subjects

Manca, J. V.

Publications and source records attributed to Manca, J. V..

4 recordsLinked to original sources

Comparative electric and ultrastructural studies of cable bacteria reveal new components of conduction machinery

Cable bacteria encompass at least two genera, and they are known to vary greatly in habitat preferences and filament thickness. We systematically investigated variations and similarities in cellular structures and electrical properties of different cable bacteria strains. Using SEM, TEM, STEM-EDX and ToF-SIMS, we characterized shared features of cable bacteria, such as inner and outer membranes, surface layer and cell junction architecture, as well as strain specific features, like the number and size of periplasmic conductive fibers (PCFs). Our data indicates that the PCFs are organized as loose stranded rope-like structures. With spatially resolved elemental analysis we detected nickel-containing co-factors within the PCF of cable bacteria strains in both genera suggesting a conserved conduction mechanism. Electrical conductivity of different cable bacteria strains showed a range of values covering three orders of magnitude indicating an unknown metabolic adaptation. Using cryogenic electron tomography we discovered multiple polar chemosensory arrays, abundant cytoplasmic inner membrane-attached vesicles (IMVs), polysomes and inner membrane invaginations that shed light on cable bacteria metabolism including complex motility control mechanisms, localized protein synthesis, and membrane remodeling. We propose that the IMVs discovered in this work are novel metabolic hubs closely connected to the unique conductive fiber structure of cable bacteria.

microbiology↗

Enhanced laterally resolved ToF-SIMS and AFM imaging of the electrically conductive structures in cable bacteria

Cable bacteria are electroactive bacteria that form a long, linear chain of ridged cylindrical cells. These filamentous bacteria perform centimeter-scale long-range electron transport through parallel, interconnected conductive pathways of which the detailed chemical and electrical properties are still unclear. Here, we combine ToF-SIMS (time of flight secondary ion mass spectrometry) and AFM (atomic force microscopy) to investigate the structure and composition of this naturally-occurring electrical network. The enhanced lateral resolution achieved allows differentiation between the cell body and the cell-cell junctions that contain a conspicuous cartwheel structure. Three ToF-SIMS modes were compared in the study of so-called fiber sheaths (i.e., the cell material that remains after removal of cytoplasm and membranes and which embeds the electrical network). Among these, fast imaging delayed extraction (FI-DE) was found to balance lateral and mass resolution, thus yielding multiple benefits in the study of structure-composition relations in cable bacteria: (i) it enables the separate study of the cell body and cell-cell junctions, (ii) by combining FI-DE with in-situ AFM, the depth of Ni-containing protein - key in the electrical transport - is determined with greater precision, and (iii) this combination prevents contamination, which is possible when using an ex-situ AFM. Our results imply that the interconnects in extracted fiber sheaths are either damaged during extraction, or that their composition is different from fibers, or both. From a more general analytical perspective, the proposed methodology of ToF-SIMS in FI-DE-mode combined with in-situ AFM holds great promise for studying the chemical structure of other biological systems.

cell biology↗

Efficient long-range conduction in cable bacteria through nickel protein wires

Filamentous cable bacteria display unrivalled long-range electron transport, generating electrical currents over centimeter distances through a highly ordered network of fibers embedded in their cell envelope. The conductivity of these periplasmic wires is exceptionally high for a biological material, but their chemical structure and underlying electron transport mechanism remain unresolved. Here, we combine high-resolution microscopy, spectroscopy, and chemical imaging on individual cable bacterium filaments to demonstrate that the periplasmic wires consist of a conductive protein core surrounded by an insulating shell layer. The core proteins contain a sulfur-ligated nickel cofactor, and conductivity decreases when nickel is oxidized or selectively removed. The involvement of nickel as the active metal in biological conduction is remarkable, and suggests a hitherto unknown form of electron transport that enables efficient conduction in centimeter-long protein structures.

microbiology↗

A Highly-ordered and Fail-safe Electrical Network in Cable Bacteria

Cable Bacteria are an emerging class of electroactive organisms that sustain unprecedented long-range electron transport across centimeter-scale distances. The pathways of the electrical currents in these filamentous microorganisms remain unresolved. Here, the electrical circuitry in a single cable bacterium is visualized with nanoscopic resolution using Conductive Atomic Force Microscopy. Combined with perturbation experiments, it is demonstrated that electrical currents are conveyed through a parallel network of conductive fibers embedded in the cell envelope which are electrically interconnected between adjacent cells. This redundant structural organization of electrical pathways likely forms a crucial adaptive trait for organisms capable of long-distance electron transport. The observed electrical circuit architecture is unique in biology and could inspire future technological applications in bioelectronics.

biophysics↗