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Role of Wall Teichoic Acid L-Rhamnosylation in Listeria Monocytogenes Resistance to Antimicrobial Peptides and Surface Protein Anchoring

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Role of Wall Teichoic Acid L-Rhamnosylation in Listeria Monocytogenes Resistance to Antimicrobial Peptides and Surface Protein Anchoring FILIPE FREITAS COELHO HENRIQUES DE CARVALHO ROLE OF WALL TEICHOIC ACID L-RHAMNOSYLATION IN LISTERIA MONOCYTOGENES RESISTANCE TO ANTIMICROBIAL PEPTIDES AND SURFACE PROTEIN ANCHORING Tese de Candidatura ao grau de Doutor em Ciências Biomédicas, submetida ao Instituto de Ciências Biomédicas Abel Salazar da Universidade do Porto. Orientador – Doutor Didier Jacques Christian Cabanes Categoria – Investigador principal Afiliação – Instituto de Biologia Molecular e Celular Coorientador – Professor Doutor Rui Appelberg Gaio Lima Categoria – Professor catedrático Afiliação – Instituto de Ciências Biomédicas Abel Salazar da Universidade do Porto De acordo com o disposto no ponto n.º 2 do Art.º 31º do Decreto-Lei n.º 74/2006, de 24 de Março, aditado pelo Decreto-Lei n.º 230/2009, de 14 de Setembro, o autor esclarece que na elaboração desta tese foram incluídos dados das publicações abaixo indicadas, e declara ter participado activamente na concepção e execução das experiências que estiveram na origem dos mesmos, assim como na sua interpretação, discussão e redacção. According to the relevant national legislation, the author clarifies that this thesis includes data from the publications listed below, and declares that he participated actively in the conception and execution of the experiments that produced such data, as well as in their interpretation, discussion and writing. PUBLICAÇÕES / PUBLICATIONS Carvalho F, Atilano ML, Pombinho R, Covas G, Gallo R, Filipe SR, Sousa S, Cabanes D (2015) L-rhamnosylation of Listeria monocytogenes wall teichoic acids promotes resistance to antimicrobial peptides by delaying interaction with the membrane. PLoS Pathog 11(5):e1004919 Carvalho F, Sousa S, Cabanes D (2014) How Listeria monocytogenes organizes its surface for virulence. Front Cell Infect Microbiol 4(48). FUNDING The author was supported by national funds through a grant (SFRH/BD/61825/2009) from Fundação para a Ciência e a Tecnologia (FCT). The work here presented was funded by the Fundo Europeu de Desenvolvimento Regional (FEDER) through the Programa Operacional Factores de Competitividade (COMPETE), and by national funds through FCT, under projects PTDC/SAU-IMU/111806/2009, PTDC/SAU-MIC/111581/2009FCOMP-01-0124- FEDER-015844, ERA-Net PathoGenoMics LISTRESS ERA-PTG/0003/2010, Infect-ERA/0001/2013PROANTILIS; and by project “NORTE-07-0124-FEDER- 000002-Host-Pathogen Interactions”, co-funded by the Programa Operacional Regional do Norte (ON.2 – O Novo Norte), under the Quadro de Referência Estratégico Nacional (QREN), through FEDER and FCT. TABLE OF CONTENTS ABSTRACT ........................................................................................................... 11 RESUMO............................................................................................................... 13 LIST OF ABBREVIATIONS .................................................................................. 15 CHAPTER I – INTRODUCTION ........................................................................... 19 A. Listeria monocytogenes ................................................................................ 21 A.1. History ................................................................................................ 21 A.2. Taxonomy, phylogeny and classification ............................................ 21 A.3. General features ................................................................................. 23 A.4. Listeriosis ........................................................................................... 25 A.4.1. Epidemiology ........................................................................ 25 A.4.2. Pathophysiology .................................................................... 25 A.4.3. Clinical manifestations and treatment ................................... 26 A.5. Cellular infection cycle ........................................................................ 28 A.5.1. Major virulence factors .......................................................... 29 B. Gram-positive cell envelope ......................................................................... 35 B.1. Peptidoglycan ..................................................................................... 35 B.1.1. Peptidoglycan metabolism .................................................... 36 B.1.1.1. Peptidoglycan assembly .......................................... 37 B.1.1.2. Peptidoglycan turnover ............................................ 39 B.2. Surface proteins and anchoring mechanisms .................................... 41 B.2.1. Cell wall-associated proteins ................................................ 42 B.2.1.1. LPXTG and NXXTX proteins ................................... 42 B.2.1.2. LysM proteins .......................................................... 45 B.2.1.3. GW proteins ............................................................ 45 B.2.2. Membrane-associated proteins ............................................ 47 B.2.2.1. Lipoproteins ............................................................. 47 B.2.2.2. Hydrophobic tail proteins ......................................... 48 B.2.3. Proteins with unknown association mechanism .................... 49 B.3. Teichoic acids ..................................................................................... 49 B.3.1. Lipoteichoic acids (LTAs) ...................................................... 50 B.3.1.1. LTA structure and biogenesis ................................. 50 B.3.1.2. LTA modifications and functions ............................. 51 B.3.2. Wall teichoic acids (WTAs) .................................................. 53 B.3.2.1. WTA structure and biogenesis ................................ 53 B.3.2.2. WTA modifications and functions ........................... 55 B.3.2.3. WTA diversity in Listeria monocytogenes ............... 57 C. Antimicrobial peptides .................................................................................. 59 C.1. General features and properties ........................................................ 59 C.2. Classes ............................................................................................. 61 C.2.1. Bacteriocins ......................................................................... 62 C.2.1.1. Gram-negative bacteriocins .................................... 62 C.2.1.2. Gram-positive bacteriocins ..................................... 64 C.2.2. Defensins ............................................................................. 69 C.2.3. Cathelicidins ........................................................................ 73 C.3. Mechanisms of action ........................................................................ 77 C.3.1. Cytoplasmic membrane disruption ...................................... 77 C.3.2. Inhibition of intracellular targets ........................................... 79 C.4. Bacterial mechanisms of resistance .................................................. 81 C.4.1. Modification of cell envelope components ........................... 81 CHAPTER II – PROJECT PRESENTATION ...................................................... 85 CHAPTER III – RESULTS ................................................................................... 89 Part I – L-Rhamnosylation of Listeria monocytogenes wall teichoic acids promotes resistance to antimicrobial peptides by delaying interaction with the membrane .................................................................................................... 93 I.1. Abstract ............................................................................................... 97 I.2. Author Summary ................................................................................. 99 I.3. Introduction ........................................................................................ 101 I.4. Results .............................................................................................. 105 I.4.1. The rmlACBD locus is required for the presence of L-rhamnose in Lm WTAs .................................................................................. 105 I.4.2. RmlT is required for the incorporation of L-rhamnose into Lm WTAs ............................................................................................ 108 I.4.3. WTA L-rhamnosylation promotes Lm resistance to AMPs .... 110 I.4.4. WTA L-rhamnosylation interferes with Lm cell wall crossing by AMPs ............................................................................................. 112 I.4.5. WTA L-rhamnosylation delays AMP interaction with the Lm plasma membrane ......................................................................... 114 I.4.6. WTA L-rhamnosylation is crucial for AMP resistance in vivo and Lm virulence .................................................................................. 117 I.5. Discussion ......................................................................................... 121 I.6. Materials and methods ....................................................................... 127 I.6.1. Bacterial strains and growth conditions ................................ 127 I.6.2. Construction and complementation of mutant strains ........... 127 I.6.3. Gene expression analyses ................................................... 126 I.6.4. WTA PAGE analysis ............................................................ 129 I.6.5. Purification of cell wall components ...................................... 129 I.6.6. Extraction of bacterial cytoplasmic
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