Abstract
BackgroundBacterial outer membrane vesicles (OMV) are packets of periplasmic material that, via the proteins and other molecules they contain, project metabolic function into the environment. While OMV production is widespread in proteobacteria, they have been extensively studied only in pathogens, which inhabit fully hydrated environments. However, many (arguably most) bacterial habitats, such as soil, are only partially hydrated. In the latter, water is characteristically distributed as films on soil particles that are, on average thinner, than are typical OMV (ca. ≤10 nm water film vs. 20 to >200 nm OMV;).Methodology/Principal FindingsWe have identified a new bacterial surface structure, termed a “nanopod”, that is a conduit for projecting OMV significant distances (e.g., ≥6 µm) from the cell. Electron cryotomography was used to determine nanopod three-dimensional structure, which revealed chains of vesicles within an undulating, tubular element. By using immunoelectron microscopy, proteomics, heterologous expression and mutagenesis, the tubes were determined to be an assembly of a surface layer protein (NpdA), and the interior structures identified as OMV. Specific metabolic function(s) for nanopods produced by Delftia sp. Cs1-4 are not yet known. However, a connection with phenanthrene degradation is a possibility since nanopod formation was induced by growth on phenanthrene. Orthologs of NpdA were identified in three other genera of the Comamonadaceae family, and all were experimentally verified to form nanopods.Conclusions/SignificanceNanopods are new bacterial organelles, and establish a new paradigm in the mechanisms by which bacteria effect long-distance interactions with their environment. Specifically, they create a pathway through which cells can effectively deploy OMV, and the biological activity these transmit, in a diffusion-independent manner. Nanopods would thus allow environmental bacteria to expand their metabolic sphere of influence in a manner previously unknown for these organisms.
Highlights
The ability of bacteria to extend their sphere of metabolic influence long distances from the cell is key to their activity and survival, and is achieved by secretion of small molecules, such as acyl homoserine lactones [1,2], which can have broad, regulatory effects on the metabolism of neighboring bacteria, as well as macromolecules, namely enzymes and outer membrane vesicles (OMV), which transmit specific function(s) [3]
Cs1-4, a polycyclic aromatic hydrocarbon (PAH)degrading bacterium that was isolated from PAH-contaminated soil in Wisconsin [16]
Imaging of phenanthrene-grown batch cultures of strain Cs1-4 by transmission electron microscopy (TEM) revealed an abundance of detached structures that had a crystalline-like outer surface, and contained interior structures that varied in morphology from spherical to spiral
Summary
The ability of bacteria to extend their sphere of metabolic influence long distances (ca. microns) from the cell is key to their activity and survival, and is achieved by secretion of small molecules, such as acyl homoserine lactones [1,2], which can have broad, regulatory effects on the metabolism of neighboring bacteria, as well as macromolecules, namely enzymes and outer membrane vesicles (OMV), which transmit specific function(s) [3]. Nanopods were discovered in phenanthrene-grown cultures of Delftia sp. TEM-Imaging of nanopods in thin sections showed interior vesicle-like structures, which were contained within an encasing structure
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