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Protein Secretion in Spirochetes

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  • Author: Wolfram R. Zückert1
  • Editors: Maria Sandkvist2, Eric Cascales3, Peter J. Christie4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology, Molecular Genetics and Immunology, University of Kansas School of Medicine, Kansas City, KS 66160; 2: Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan; 3: CNRS Aix-Marseille Université, Mediterranean Institute of Microbiology, Marseille, France; 4: Department of Microbiology and Molecular Genetics, McGovern Medical School, Houston, Texas
  • Source: microbiolspec June 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.PSIB-0026-2019
  • Received 14 January 2019 Accepted 18 April 2019 Published 14 June 2019
  • Wolfram R. Zückert, [email protected]
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  • Abstract:

    Spirochetes form a separate phylum of bacteria with two membranes but otherwise unusual morphologies and envelope structures. Distinctive common features of , , and include the sequestration of flagella to the periplasm and thin peptidoglycan cell walls that are more closely associated with the inner membrane. Outer membrane compositions differ significantly between the genera. most closely track Gram-negative bacteria due to the incorporation of lipopolysaccharides. and outer membranes lack lipopolysaccharide, with treponemes expressing only a few outer membrane proteins and displaying a dizzying diversity of abundant surface lipoproteins instead. Phylogenetic and experimental evidence indicates that spirochetes have adapted various modules of bacterial export and secretion pathways to build and maintain their envelopes. Export and insertion pathways in the inner membrane appear conserved, while spirochetal experimentation with various envelope architectures over time has led to variations in secretion pathways in the periplasm and outer membrane. Classical type I to III secretion systems have been identified, with demonstrated roles in drug efflux and export of flagellar proteins only. Unique activities of periplasmic proteases, including a C-terminal protease, are involved in maturation of some periplasmic proteins. Proper lipoprotein sorting within the periplasm appears to be dependent on functional Lol pathways that lack the outer membrane lipoprotein insertase LolB. The abundance of surface lipoproteins in and detailed protein sorting studies suggest a lipoprotein secretion pathway that either extends Lol through the outer membrane or bypasses it altogether. Proteins can be released from cells in outer membrane vesicles or, rarely, as soluble proteins.

  • Citation: Zückert W. 2019. Protein Secretion in Spirochetes. Microbiol Spectrum 7(3):PSIB-0026-2019. doi:10.1128/microbiolspec.PSIB-0026-2019.

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/content/journal/microbiolspec/10.1128/microbiolspec.PSIB-0026-2019
2019-06-14
2019-08-22

Abstract:

Spirochetes form a separate phylum of bacteria with two membranes but otherwise unusual morphologies and envelope structures. Distinctive common features of , , and include the sequestration of flagella to the periplasm and thin peptidoglycan cell walls that are more closely associated with the inner membrane. Outer membrane compositions differ significantly between the genera. most closely track Gram-negative bacteria due to the incorporation of lipopolysaccharides. and outer membranes lack lipopolysaccharide, with treponemes expressing only a few outer membrane proteins and displaying a dizzying diversity of abundant surface lipoproteins instead. Phylogenetic and experimental evidence indicates that spirochetes have adapted various modules of bacterial export and secretion pathways to build and maintain their envelopes. Export and insertion pathways in the inner membrane appear conserved, while spirochetal experimentation with various envelope architectures over time has led to variations in secretion pathways in the periplasm and outer membrane. Classical type I to III secretion systems have been identified, with demonstrated roles in drug efflux and export of flagellar proteins only. Unique activities of periplasmic proteases, including a C-terminal protease, are involved in maturation of some periplasmic proteins. Proper lipoprotein sorting within the periplasm appears to be dependent on functional Lol pathways that lack the outer membrane lipoprotein insertase LolB. The abundance of surface lipoproteins in and detailed protein sorting studies suggest a lipoprotein secretion pathway that either extends Lol through the outer membrane or bypasses it altogether. Proteins can be released from cells in outer membrane vesicles or, rarely, as soluble proteins.

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Figures

Image of FIGURE 1
FIGURE 1

Envelope structures of model spirochetes , , and . Spirochetes have a common diderm envelope structure with an inner membrane (IM) and outer membrane (OM) and a periplasmic space in between that contains a thin peptidoglycan cell wall and periplasmic flagella. A major difference between the three genera is seen in the OM: displays a limited set of integral OM proteins (OMPs), among them the unusual porin P13 with a predicted α-helical TM topology, but a large variable set of surface lipoproteins. The OM most closely resembles a Gram-negative OM, with lipopolysaccharide (LPS) being the major component of the surface leaflet, complemented by a large number of OMPs and a limited set of surface lipoproteins. expresses only rare OMPs with limited surface exposure. Some of the model proteins under study are labeled in italics. See text for details.

Source: microbiolspec June 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.PSIB-0026-2019
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Image of FIGURE 2
FIGURE 2

Generalized model of spirochetal protein secretion. The left half shows type I to III secretion systems (T1SS, T2SS, and T3SS) as well as the pathways involved in the secretion of nonlipidated membrane and periplasmic proteins. The right half shows the pathways for lipoprotein (LP) modification, sorting, and secretions. Pathway components or mechanisms that appear unique to a particular spirochetal genus are labeled by stippled red circles with the genus initial: , ; , ; and , . For example, a potential T2SS has been identified only for . The pathways in blue delineate the current alternative periplasmic and OM mechanisms that may be involved in the secretion of α-helical integral OMPs and surface lipoproteins in ; of note, could also take advantage of its T2SS to secrete surface lipoproteins ( 23 , 95 ). Release of outer membrane vesicles (OMVs) has been observed and studied in . See text for details.

Source: microbiolspec June 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.PSIB-0026-2019
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