A substrate-fusion protein is trapped inside the Type III Secretion System channel in Shigella flexneri

PLoS Pathog. 2014 Jan;10(1):e1003881. doi: 10.1371/journal.ppat.1003881. Epub 2014 Jan 16.

Abstract

The Type III Secretion System (T3SS) is a macromolecular complex used by Gram-negative bacteria to secrete effector proteins from the cytoplasm across the bacterial envelope in a single step. For many pathogens, the T3SS is an essential virulence factor that enables the bacteria to interact with and manipulate their respective host. A characteristic structural feature of the T3SS is the needle complex (NC). The NC resembles a syringe with a basal body spanning both bacterial membranes and a long needle-like structure that protrudes from the bacterium. Based on the paradigm of a syringe-like mechanism, it is generally assumed that effectors and translocators are unfolded and secreted from the bacterial cytoplasm through the basal body and needle channel. Despite extensive research on T3SS, this hypothesis lacks experimental evidence and the mechanism of secretion is not fully understood. In order to elucidate details of the T3SS secretion mechanism, we generated fusion proteins consisting of a T3SS substrate and a bulky protein containing a knotted motif. Because the knot cannot be unfolded, these fusions are accepted as T3SS substrates but remain inside the NC channel and obstruct the T3SS. To our knowledge, this is the first time substrate fusions have been visualized together with isolated NCs and we demonstrate that substrate proteins are secreted directly through the channel with their N-terminus first. The channel physically encloses the fusion protein and shields it from a protease and chemical modifications. Our results corroborate an elementary understanding of how the T3SS works and provide a powerful tool for in situ-structural investigations in the future. This approach might also be applicable to other protein secretion systems that require unfolding of their substrates prior to secretion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Bacterial Secretion Systems / physiology*
  • Cytoplasm / genetics
  • Cytoplasm / metabolism*
  • Protein Transport / physiology
  • Shigella flexneri / genetics
  • Shigella flexneri / metabolism*
  • Shigella flexneri / ultrastructure

Substances

  • Bacterial Proteins
  • Bacterial Secretion Systems

Grants and funding

KD was supported by a Boehringer Ingelheim Fonds PhD scholarship and the International Max Planck Research School for Infectious Diseases and Immunology. The European Research Council has provided financial support to MK under the European Community's Seventh Framework Programme (FP7/2007-2013). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.