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Electron Cryotomography of Bacterial Secretion Systems

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  • Authors: Catherine M. Oikonomou1, Grant J. Jensen2,3
  • Editors: Maria Sandkvist4, Eric Cascales5, Peter J. Christie6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125; 2: Department of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125; 3: Howard Hughes Medical Institute, Pasadena, CA 91125; 4: Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan; 5: CNRS Aix-Marseille Université, Mediterranean Institute of Microbiology, Marseille, France; 6: Department of Microbiology and Molecular Genetics, McGovern Medical School, Houston, Texas
  • Source: microbiolspec April 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0019-2018
  • Received 19 October 2018 Accepted 11 February 2019 Published 05 April 2019
  • Grant J. Jensen, [email protected]
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  • Abstract:

    In biology, function arises from form. For bacterial secretion systems, which often span two membranes, avidly bind to the cell wall, and contain hundreds of individual proteins, studying form is a daunting task, made possible by electron cryotomography (ECT). ECT is the highest-resolution imaging technique currently available to visualize unique objects inside cells, providing a three-dimensional view of the shapes and locations of large macromolecular complexes in their native environment. Over the past 15 years, ECT has contributed to the study of bacterial secretion systems in two main ways: by revealing intact forms for the first time and by mapping components into these forms. Here we highlight some of these contributions, revealing structural convergence in type II secretion systems, structural divergence in type III secretion systems, unexpected structures in type IV secretion systems, and unexpected mechanisms in types V and VI secretion systems. Together, they offer a glimpse into a world of fantastic forms—nanoscale rotors, needles, pumps, and dart guns—much of which remains to be explored.

  • Citation: Oikonomou C, Jensen G. 2019. Electron Cryotomography of Bacterial Secretion Systems. Microbiol Spectrum 7(2):PSIB-0019-2018. doi:10.1128/microbiolspec.PSIB-0019-2018.

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/content/journal/microbiolspec/10.1128/microbiolspec.PSIB-0019-2018
2019-04-05
2019-09-20

Abstract:

In biology, function arises from form. For bacterial secretion systems, which often span two membranes, avidly bind to the cell wall, and contain hundreds of individual proteins, studying form is a daunting task, made possible by electron cryotomography (ECT). ECT is the highest-resolution imaging technique currently available to visualize unique objects inside cells, providing a three-dimensional view of the shapes and locations of large macromolecular complexes in their native environment. Over the past 15 years, ECT has contributed to the study of bacterial secretion systems in two main ways: by revealing intact forms for the first time and by mapping components into these forms. Here we highlight some of these contributions, revealing structural convergence in type II secretion systems, structural divergence in type III secretion systems, unexpected structures in type IV secretion systems, and unexpected mechanisms in types V and VI secretion systems. Together, they offer a glimpse into a world of fantastic forms—nanoscale rotors, needles, pumps, and dart guns—much of which remains to be explored.

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Image of FIGURE 1
FIGURE 1

T2SS. ECT revealed the structures of the T4aP in and , enabling high-resolution structures to be placed into the map to produce a hypothetical model of the machine. Further studies revealed structural convergence of the related T4bP in and T2SS in , with a similar periplasmic ring (arrows) formed by nonhomologous proteins in each system. Note in this and subsequent figures how bacterial secretion systems often locally distort the cell envelope . Images are reprinted from the following with permission: panel A left and middle, reference 6 ; panel A right, reference 5 ; panel B, reference 29 ; and panel C, reference 31 .

Source: microbiolspec April 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0019-2018
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Image of FIGURE 2
FIGURE 2

T3SS. ECT and subtomogram averaging revealed the structures of diverse T3SSs, including the flagellar motors of many bacteria (three examples, from , , and ) and the injectisome from Typhimurium . Structures shown from left to right: EMD-3154, EMD-3155, and EBD-3150 from reference 45 and EMD-2667 from reference 52 .

Source: microbiolspec April 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0019-2018
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Image of FIGURE 3
FIGURE 3

T4SS. ECT revealed the structure of the Dot/Icm T4SS, including a central channel extending from the inner membrane, and enabled components to be placed in the map. It also revealed the similar structure of the T4SS (inset), as well as novel, related OM tubes. Images are reprinted from the following with permission: panel A, reference 60 (but see also reference 59 ); panel B, reference 61 .

Source: microbiolspec April 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0019-2018
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Image of FIGURE 4
FIGURE 4

T5SS. ECT revealed the stick-like form of the CDI T5SS (arrows) and helped elucidate its mechanism, in which half of CdiA extends out from the cell surface . Upon target binding, the remaining half of CdiA is exported to deliver the toxin to the target cell. Images reprinted with permission from reference 66 .

Source: microbiolspec April 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.PSIB-0019-2018
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Image of FIGURE 5
FIGURE 5

T6SS. ECT revealed the contractile mechanism of the T6SS and its structure in . It also revealed higher-order arrays of T6SS in and a T6SS-related metamorphosis-associated contractile structure (MAC) in . Images are reprinted from the following with permission: panels A and B, reference 70 ; panel D, reference 72 .

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