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Published June 7, 2011 | Supplemental Material + Published
Journal Article Open

Nanopods: A New Bacterial Structure and Mechanism for Deployment of Outer Membrane Vesicles

Abstract

Background: Bacterial 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 Findings: We 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/Significance: Nanopods 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.

Additional Information

© 2011 Shetty et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received December 21, 2010; Accepted May 10, 2011; Published June 7, 2011. Editor: Michael Hensel, University of Osnabrueck, Germany. Funding: These studies were funded by grants to WJH (NSF MCB0920664) and to GJJ (NIH R01 AI067548); EIT was supported by a Natural Sciences and Engineering Research Council of Canada Postdoctorate Fellowship. Sequencing and annotation of the Delftia sp. Cs1-4 genome was done by the U.S. Department of Energy Joint Genome Institute, through the Community Sequencing Project (CSP795673 to WJH). The work conducted by the U.S. Department of Energy Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under contract No. DE-AC02-05CH11231. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors thank the following colleagues for supplying cultures: Jullian Davies (Delftia acidovorans SPH1), Eric Roden (Acidovorax delafieldii), David Stahl (Verminephrobacter eiseniae EF01-2) and Ronald Walcott (Acidovorax avenae subsp. citrulli AAC00-1). Author Contributions: Conceived and designed the experiments: WJH GJJ. Performed the experiments: AS SC EIT. Analyzed the data: WJH EIT GJJ AS. Contributed reagents/materials/analysis tools: WJH GJJ. Wrote the paper: WJH.

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