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000468384900002.Pdf UNIVERSIDADE ESTADUAL DE CAMPINAS SISTEMA DE BIBLIOTECAS DA UNICAMP REPOSITÓRIO DA PRODUÇÃO CIENTIFICA E INTELECTUAL DA UNICAMP Versão do arquivo anexado / Version of attached file: Versão do Editor / Published Version Mais informações no site da editora / Further information on publisher's website: https://www.frontiersin.org/articles/10.3389/fmicb.2019.01078/full DOI: 10.3389/fmicb.2019.01078 Direitos autorais / Publisher's copyright statement: ©2019 by Frontiers Research Foundation. All rights reserved. DIRETORIA DE TRATAMENTO DA INFORMAÇÃO Cidade Universitária Zeferino Vaz Barão Geraldo CEP 13083-970 – Campinas SP Fone: (19) 3521-6493 http://www.repositorio.unicamp.br fmicb-10-01078 May 18, 2019 Time: 16:6 # 1 REVIEW published: 21 May 2019 doi: 10.3389/fmicb.2019.01078 Bacteria-Killing Type IV Secretion Systems Germán G. Sgro1†, Gabriel U. Oka1†, Diorge P. Souza1‡, William Cenens1, Ethel Bayer-Santos1‡, Bruno Y. Matsuyama1, Natalia F. Bueno1, Thiago Rodrigo dos Santos1, Cristina E. Alvarez-Martinez2, Roberto K. Salinas1 and Chuck S. Farah1* 1 Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, São Paulo, Brazil, 2 Departamento de Genética, Evolução, Microbiologia e Imunologia, Instituto de Biologia, University of Campinas (UNICAMP), Edited by: Campinas, Brazil Ignacio Arechaga, University of Cantabria, Spain Reviewed by: Bacteria have been constantly competing for nutrients and space for billions of years. Elisabeth Grohmann, During this time, they have evolved many different molecular mechanisms by which Beuth Hochschule für Technik Berlin, to secrete proteinaceous effectors in order to manipulate and often kill rival bacterial Germany Xiancai Rao, and eukaryotic cells. These processes often employ large multimeric transmembrane Army Medical University, China nanomachines that have been classified as types I–IX secretion systems. One of the *Correspondence: most evolutionarily versatile are the Type IV secretion systems (T4SSs), which have Chuck S. Farah [email protected] been shown to be able to secrete macromolecules directly into both eukaryotic and †These authors have contributed prokaryotic cells. Until recently, examples of T4SS-mediated macromolecule transfer equally to this work from one bacterium to another was restricted to protein-DNA complexes during ‡ Present address: bacterial conjugation. This view changed when it was shown by our group that many Diorge P. Souza, MRC Laboratory for Molecular Cell Xanthomonas species carry a T4SS that is specialized to transfer toxic bacterial effectors Biology, University College London, into rival bacterial cells, resulting in cell death. This review will focus on this special London, United Kingdom subtype of T4SS by describing its distinguishing features, similar systems in other Ethel Bayer-Santos, Departamento de Microbiologia, proteobacterial genomes, and the nature of the effectors secreted by these systems Instituto de Ciências Biomédicas, and their cognate inhibitors. Universidade de São Paulo, São Paulo, Brazil Keywords: bacterial competition, Xanthomonadales, type IV immunity protein, type IV secretion effector, type IV secretion system, X-Tfe, X-Tfi, X-T4SS Specialty section: This article was submitted to Microbial Physiology and Metabolism, INTRODUCTION a section of the journal Frontiers in Microbiology Type IV secretion systems (T4SSs) have been studied since the birth of modern molecular biology, Received: 15 March 2019 starting with the description of bacterial conjugation over 70 years ago (Lederberg and Tatum, Accepted: 29 April 2019 1946). It quickly became evident that the T4SS-mediated horizontal transfer of genetic material Published: 21 May 2019 is a major contributor to bacterial evolution, making it necessary to consider lateral connections Citation: between lineages for a complete description of the bacterial tree of life (de la Cruz and Davies, 2000). Sgro GG, Oka GU, Souza DP, Horizontal gene transfer is also one of the principal mechanisms for the spread of genes conferring Cenens W, Bayer-Santos E, resistance to antibiotics (Cabezon et al., 2015). Moreover, many pathogenic bacteria use T4SSs to Matsuyama BY, Bueno NF, facilitate their proliferation and survival inside eukaryotic hosts, typically by the secretion of protein dos Santos TR, Alvarez-Martinez CE, Salinas RK and Farah CS (2019) effectors or protein-DNA complexes (Gonzalez-Rivera et al., 2016). T4SSs are thus important Bacteria-Killing Type IV Secretion virulence factors in a variety of human diseases, including whooping cough (Bordetella pertussis; Systems. Front. Microbiol. 10:1078. Locht et al., 2011; Carbonetti, 2015), cat-scratch fever (Bartonella henselae; Siamer and Dehio, doi: 10.3389/fmicb.2019.01078 2015), brucellosis (Brucella spp.; Ke et al., 2015), Legionnaire’s pneumonia (Legionella pneumophila; Frontiers in Microbiology | www.frontiersin.org 1 May 2019 | Volume 10 | Article 1078 fmicb-10-01078 May 18, 2019 Time: 16:6 # 2 Sgro et al. Bacteria-Killing Type IV Secretion Systems Finsel and Hilbi, 2015), Q fever (Coxiella burnetii; Moffatt et al., and size diversity has been observed for many of the subunits 2015) and peptic ulcer and gastric cancer (Helicobacter pylori; in different species. This is perhaps most starkly exemplified Naumann et al., 2017). One of the most well-characterized when considering the H. pylori Cag T4SS which, in addition to T4SSs is that of Agrobacterium tumefaciens which injects orthologs of the basic set of canonical class A subunits, possesses nucleoprotein complexes and protein factors into plant cells another five subunits that are required for proper function (Alvarez-Martinez and Christie, 2009; Li and Christie, 2018). (Backert et al., 2015; Frick-Cheng et al., 2016). Furthermore, specialized T4SSs from Neisseria gonorrhoeae or The even more distantly related class B includes T4SSs found H. pylori secrete DNA to the extracellular milieu or uptake DNA in the pathogens L. pneumophila, C. burnetii, and Rickettsiella from the environment to the bacterial cytoplasm, respectively grylli as well as in the IncI conjugative plasmids R64 and ColIb- (Hofreuter et al., 2001; Hamilton et al., 2005; Callaghan et al., P9 (Sexton and Vogel, 2002). L. pneumophila causes Legionnaire’s 2017). Finally, the plant pathogen Xanthomonas citri (Oliveira disease in humans by infecting alveolar macrophages where et al., 2016; Sgro et al., 2018; Souza et al., 2015) and, more it replicates within a specialized vacuole (Backert and Meyer, recently, the opportunistic human pathogen Stenotrophomonas 2006; Ensminger and Isberg, 2009). Its Dot/Icm T4SS is made maltophilia (preprint: Bayer-Santos et al., 2019), have been shown up of 27 components and secretes more than 300 effector to use a T4SS to inject toxic effectors into target bacteria, thus proteins that manipulate signal transduction pathways in the inducing the death of rival cells (Figure 1). host cell, primarily affecting organelle trafficking (Hilbi et al., T4SSs are structurally very diverse. For example, the 2017; Qiu and Luo, 2017). The bacteria-killing T4SSs, which is related pKM101 and R388 plasmid-encoded conjugation systems the topic of this review, belong to the canonical class A T4SSs, (Chandran et al., 2009; Fronzes et al., 2009; Rivera-Calzada et al., although they do have some structurally distinguishing features 2013) and the pathogenic Legionella Dot/Icm (Ghosal et al., 2017; as described below. Chetrit et al., 2018) and H. pylori Cag (Frick-Cheng et al., 2016; The Xanthomonadales order of Gammaproteobacteria Chang et al., 2018) effector-secreting systems, while all exhibiting (Saddler and Bradbury, 2007), recently divided into two an outer membrane-associated core complex with 14-fold or 13- orders, Xanthomonadales (families Xanthomonadaceae and fold symmetry, present significantly different features in terms of Rhodanobacteraceae) and Nevskiales (Naushad et al., 2015), their overall size. These systems also display a varied set of both include several hundred phytopathogenic species of the functional and structural subunits, and even the homologous genera Xanthomonas and Xylella as well as important and subunits have very low sequence similarity and frequently present ubiquitous soil, water and plant-associated bacteria of the genera modified domain architectures (Alvarez-Martinez and Christie, Stenotrophomonas, Lysobacter, Luteimonas, Pseudoxanthomonas, 2009; Christie et al., 2014; Guglielmini et al., 2014; Christie, Rhodanobacter, Luteibacter, Dyella, Frateuria, Aquimonas, 2016; Grohmann et al., 2017). For these reasons, the T4SSs from and others (Van Sluys et al., 2002; Saddler and Bradbury, Gram-negative bacteria have been divided into two major classes, 2007; Looney et al., 2009; Mansfield et al., 2012). Some denoted A and B (Christie and Vogel, 2000), and classification Stenotrophomonas strains are opportunistic pathogens of systems based on detailed phylogenetic analysis have divided immunosuppressed human patients (Chang et al., 2015) and Gram-negative and Gram-positive T4SSs into up to 8 classes some Stenotrophomonas and Lysobacter strains have been (Guglielmini et al., 2014). recognized as potential biological control agents in combating The canonical class A, best represented by the A. tumefaciens plant diseases caused by fungi or other bacteria (Hayward vir system and those coded by conjugative plasmids pKM101, et al., 2010; Mukherjee and Roy, 2016; Panthee et al., 2016). R388, and RP4, have the basic set of 12 conserved subunits, Other species from the genera Lysobacter
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