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Surfaceome and Proteosurfaceome in Parietal Monoderm Bacteria: Focus on Protein Cell-Surface Display Mickael Desvaux, Thomas Candela, Pascale Serror

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Surfaceome and Proteosurfaceome in Parietal Monoderm Bacteria: Focus on Protein Cell-Surface Display Mickael Desvaux, Thomas Candela, Pascale Serror Surfaceome and Proteosurfaceome in Parietal Monoderm Bacteria: Focus on Protein Cell-Surface Display Mickael Desvaux, Thomas Candela, Pascale Serror To cite this version: Mickael Desvaux, Thomas Candela, Pascale Serror. Surfaceome and Proteosurfaceome in Parietal Monoderm Bacteria: Focus on Protein Cell-Surface Display. Frontiers in Microbiology, Frontiers Media, 2018, 9, 10.3389/fmicb.2018.00100. hal-01727158 HAL Id: hal-01727158 https://hal.archives-ouvertes.fr/hal-01727158 Submitted on 8 Mar 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License fmicb-09-00100 February 12, 2018 Time: 14:24 # 1 REVIEW published: 14 February 2018 doi: 10.3389/fmicb.2018.00100 Surfaceome and Proteosurfaceome in Parietal Monoderm Bacteria: Focus on Protein Cell-Surface Display Mickaël Desvaux1*, Thomas Candela2 and Pascale Serror3 1 Université Clermont Auvergne, INRA, UMR454 MEDiS, Clermont-Ferrand, France, 2 EA4043 Unité Bactéries Pathogènes et Santé, Châtenay-Malabry, France, 3 Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France The cell envelope of parietal monoderm bacteria (archetypal Gram-positive bacteria) is formed of a cytoplasmic membrane (CM) and a cell wall (CW). While the CM is composed of phospholipids, the CW is composed at least of peptidoglycan (PG) covalently linked to other biopolymers, such as teichoic acids, polysaccharides, and/or polyglutamate. Considering the CW is a porous structure with low selective permeability contrary to the CM, the bacterial cell surface hugs the molecular figure of the CW components as a well of the external side of the CM. While the surfaceome corresponds to the totality of the molecules found at the bacterial cell surface, Edited by: Awdhesh Kalia, the proteinaceous complement of the surfaceome is the proteosurfaceome. Once University of Texas MD Anderson translocated across the CM, secreted proteins can either be released in the extracellular Cancer Center, United States milieu or exposed at the cell surface by associating to the CM or the CW. Following Reviewed by: the gene ontology (GO) for cellular components, cell-surface proteins at the CM can Konstantin V. Korotkov, University of Kentucky, United States either be integral (GO: 0031226), i.e., the integral membrane proteins, or anchored Chenggang Wu, to the membrane (GO: 0046658), i.e., the lipoproteins. At the CW (GO: 0009275), McGovern Medical School, United States cell-surface proteins can be covalently bound, i.e., the LPXTG-proteins, or bound *Correspondence: through weak interactions to the PG or wall polysaccharides, i.e., the cell wall binding Mickaël Desvaux proteins. Besides monopolypeptides, some proteins can associate to each other to [email protected] form supramolecular protein structures of high molecular weight, namely the S-layer, Specialty section: pili, flagella, and cellulosomes. After reviewing the cell envelope components and the This article was submitted to different molecular mechanisms involved in protein attachment to the cell envelope, Infectious Diseases, a section of the journal perspectives in investigating the proteosurfaceome in parietal monoderm bacteria are Frontiers in Microbiology further discussed. Received: 29 June 2017 Keywords: Gram-positive bacteria, cell-surface protein, surface proteome, subcellular localization, Accepted: 16 January 2018 pili/fimbriae/curli, lipoproteins, LPXTG sortase-dependent proteins, membrane proteins Published: 14 February 2018 Citation: Desvaux M, Candela T and Serror P INTRODUCTION (2018) Surfaceome and Proteosurfaceome in Parietal As the interface of the cell with its surrounding, the bacterial cell surface plays a crucial role Monoderm Bacteria: Focus on Protein Cell-Surface Display. in all types of interactions. In the first instance, the diversity of the bacterial cell envelope is Front. Microbiol. 9:100. generally viewed as dichotomic, on the one hand, the Gram-positive bacteria, and on the other doi: 10.3389/fmicb.2018.00100 hand, the Gram-negative bacteria (Desvaux et al., 2004, 2009). This difference is based on the result Frontiers in Microbiology | www.frontiersin.org 1 February 2018 | Volume 9 | Article 100 fmicb-09-00100 February 12, 2018 Time: 14:24 # 2 Desvaux et al. Protein Cell-Surface Display in Gram-Positive Bacteria of the Gram staining method originally developed by the cell envelope of parietal monoderm bacteria, the CW is not Danish pharmacologist and physician Hans Christian Joachim impermeable but on the contrary a porous and penetrable Gram (Gram, 1884) and still routinely used worldwide to structure. As such, cell envelope proteins are in contact with the differentiate bacteria (Beveridge, 2001). With the development external environment without ever having a domain protruding of microscopic techniques, it first appeared the difference in out the confines of the CW. Like for the fractal dimension staining was the result of profound divergence in structural of the protein surface (Richards, 1977; Banerji and Navare, organisation of the bacterial cell envelope, where Gram- 2013), the nature and definition of the bacterial cell surface positive bacteria have a thick cell wall (CW) sitting atop of strictly depends on the molecule considered, e.g., a water a cytoplasmic membrane (CM) (Silhavy et al., 2010). Later molecule or a globular protein, which can enter in contact, on, molecular analyses further revealed that Gram-positive access, diffuse or penetrate differently the CW (Figure 2). bacteria corresponded to a phylogenetically coherent group To be exposed at the cell surface of parietal monoderm within the domain Bacteria and belonged to only two phyla, bacteria, proteins need to be first secreted across the CM. namely the low GCC% Gram-positive bacteria of the phylum Several secretion systems allow protein translocation in parietal Firmicutes and the high GCC% Gram-positive bacteria of monoderm bacteria (Tjalsma et al., 2004; Desvaux et al., 2005; the phylum Actinobacteria (Woese, 1987; Woese et al., 1990). Desvaux and Hébraud, 2006; Sibbald et al., 2006; Chagnot Over the years, though, it appears this terminology presents et al., 2013), namely (i) the Sec (secretion), (ii) the Tat (twin- some ambiguity when considering the diversity of the domain arginine translocation), (iii) ABC protein exporter, (iv) the Bacteria (Desvaux et al., 2009). Considering the term “Gram- FPE (fimbrilin-protein exporter), (v) the FEA (flagella export positive bacteria,” it can refer to three distinct, and sometimes apparatus), and (vi) the ESX (ESAT-6 system), also called incompatible elements, i.e., a Gram staining result, a cell envelope Wss (WXG100 secretion system). Of note, the status of the architecture and/or a taxonomic group. For instance, bacteria holins (hole forming) as protein secretion systems per se of the class Mollicutes, comprising the genus Mycoplasma, remain controversial (Desvaux, 2012). Proteins secreted via the cannot retain the Gram stain because they naturally lack Sec translocon generally possess a targeting signal called the a CW although the low GCC% content of their genomes signal peptide (SP) of type I (SP I), which is composed of and other molecular markers resemble those of Gram-positive three non-conserved domains, namely the n-domain (positively bacteria of the phylum Firmicutes (Razin et al., 1998). Species charged and at the N-terminus), the h-domain (a-helical of the genus Mycobacterium possess a peculiar cell envelope hydrophobic core region), and the c-domain (cleavage site with a mycomembrane preventing Gram staining and thus processed by a membrane-bound signal peptidase) (Fekkes require alternative staining methods called acid-fast (Somoskovi and Driessen, 1999). While proteins secreted via Sec, Tat et al., 2001) but nonetheless belong to the high GCC% Gram- ABC exporter and FPE possess N-terminal SPs with some positive bacteria of the phylum Actinobacteria (Draper, 1998). specificities, the signal targeting proteins to the FEA or ESX In some deep branches of the phylum Firmicutes, some bacteria remain elusive. Besides transport across the CM, the transport clearly exhibit Gram-negative cell envelope for which a new and maturation of secreted proteins across the CW can be class was proposed, i.e., the Negativicutes (Marchandin et al., regulated by different mechanisms, such as the proteolytic 2010). maturation of secreted proenzymes, the requirement of divalent Inspired by the research work of Gupta (1998a,b, 2000), cations for activation or the post-translocational intervention the description of the bacterial cell envelope respective to the of peptidyl-prolyl isomerase chaperones (Forster and Marquis, number of biological membranes appeared much more definite 2012). and was first reintroduced in the field of bacterial protein To explicitly describe the subcellular localization of proteins, secretion (Desvaux et al., 2009). While monoderm bacteria refer the gene ontology (GO) respective to the cellular component to species exhibiting
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