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EcoSal Plus

Domain 4:

Synthesis and Processing of Macromolecules

Lipoproteins and Their Trafficking to the Outer Membrane

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  • Author: Marcin Grabowicz1,2,3
  • Editors: Maria Sandkvist4, Eric Cascales5, Peter J. Christie6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Emory Antibiotic Resistance Center, Emory University School of Medicine, Atlanta, GA 30322; 2: Department of Microbiology & Immunology, Emory University School of Medicine, Atlanta, GA 30322; 3: Division of Infectious Diseases, Department of Medicine, Emory University School of Medicine, Atlanta, GA 30322; 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
  • Received 27 August 2018 Accepted 01 February 2019 Published 22 March 2019
  • Address correspondence to Marcin Grabowicz, [email protected]
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  • Abstract:

    Lipoproteins are produced by both Gram-positive and Gram-negative bacteria. Once secreted, lipoproteins are quickly acylated, anchoring them into the plasma membrane. Recent work has shown that Gram-positive bacteria are able to generate considerable diversity in the acylation of their lipoproteins, though the mechanisms involved are only just beginning to emerge. In Gram-negative organisms, most lipoproteins are subsequently trafficked to the outer membrane (OM). Lipoprotein trafficking is an essential pathway in these bacteria. At least one OM lipoprotein component is required by each of the essential machines that assemble the OM (such as the Bam and Lpt machines) and build the peptidoglycan cell wall (Lpo-penicillin-binding protein complexes). The Lol pathway has been the paradigm for OM lipoprotein trafficking: a complex of LolCDE extracts lipoproteins from the plasma membrane, LolA shuttles them through the periplasmic space, and LolB anchors them into the OM. The peptide signals responsible for OM-targeting via LolCDE have long been known for . Remarkably, production of novel lipoprotein acyl forms in has reinforced the idea that lipid signals also contribute to OM targeting via LolCDE. Moreover, recent work has shown that lipoprotein trafficking can occur in without either LolA or LolB. Therefore, current evidence suggests that at least one additional, LolAB-independent route for OM lipoprotein trafficking exists. This chapter reviews the posttranslocation modifications of all lipoproteins, with a focus on the trafficking of lipoproteins to the OM of Gram-negative bacteria.

  • Citation: Grabowicz M. 2019. Lipoproteins and Their Trafficking to the Outer Membrane, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0038-2018

Article Version

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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0038-2018
2019-03-22
2019-12-07

Abstract:

Lipoproteins are produced by both Gram-positive and Gram-negative bacteria. Once secreted, lipoproteins are quickly acylated, anchoring them into the plasma membrane. Recent work has shown that Gram-positive bacteria are able to generate considerable diversity in the acylation of their lipoproteins, though the mechanisms involved are only just beginning to emerge. In Gram-negative organisms, most lipoproteins are subsequently trafficked to the outer membrane (OM). Lipoprotein trafficking is an essential pathway in these bacteria. At least one OM lipoprotein component is required by each of the essential machines that assemble the OM (such as the Bam and Lpt machines) and build the peptidoglycan cell wall (Lpo-penicillin-binding protein complexes). The Lol pathway has been the paradigm for OM lipoprotein trafficking: a complex of LolCDE extracts lipoproteins from the plasma membrane, LolA shuttles them through the periplasmic space, and LolB anchors them into the OM. The peptide signals responsible for OM-targeting via LolCDE have long been known for . Remarkably, production of novel lipoprotein acyl forms in has reinforced the idea that lipid signals also contribute to OM targeting via LolCDE. Moreover, recent work has shown that lipoprotein trafficking can occur in without either LolA or LolB. Therefore, current evidence suggests that at least one additional, LolAB-independent route for OM lipoprotein trafficking exists. This chapter reviews the posttranslocation modifications of all lipoproteins, with a focus on the trafficking of lipoproteins to the OM of Gram-negative bacteria.

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Figures

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Figure 1

Secreted lipoproteins are first diacylated at an invariant Cys residue by Lgt using resident phospholipids as acyl donors. The signal sequence is then cleaved by the peptidase Lsp to yield diacyl-form lipoproteins. In almost all Gram-negative bacteria, Lnt attaches another acyl chain to the amino group of Cys to yield triacyl-form lipoproteins. Low-GC Gram-negative bacteria can also produce peptidyl forms (likely due to an Lsp-type enzyme that yields Cys), as well as -acetyl and lyso forms that are derived from diacyl lipoproteins. Triacyl- and lyso-lipoproteins can efficiently interact with LolCDE for trafficking to the OM in Gram-negative organisms. Diacyl-form lipoproteins can be trafficked to the OM via LolDF.

Citation: Grabowicz M. 2019. Lipoproteins and Their Trafficking to the Outer Membrane, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0038-2018
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Image of Figure 2
Figure 2

The OM lipoprotein trafficking routes of are shown. Once mature, OM-targeted lipoproteins engage with the LolCDE transporter in the IM. LolE interacts with lipoproteins and LolC recruits the periplasmic chaperone protein LolA. At the expense of ATP hydrolysis by LolD, the LolCDE complex extracts lipoproteins from the IM bilayer and transfers them to LolA. Lipoproteins are shuttled through the periplasm in a LolA-bound complex. At the OM, the lipoprotein LolB receives LolA-bound client lipoproteins and anchors them into the OM bilayer. Since Δ mutants are viable, an alternate trafficking route must exist that can traffic essential OM lipoproteins to support cell viability. LolCDE remains essential in such Δ mutants, suggesting that lipoproteins originate from this complex and are then trafficked to the OM via an unknown mechanism.

Citation: Grabowicz M. 2019. Lipoproteins and Their Trafficking to the Outer Membrane, EcoSal Plus 2019; doi:10.1128/ecosalplus.ESP-0038-2018
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