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Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis Mickael Desvaux, Michel Hébraud

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Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis Mickael Desvaux, Michel Hébraud Bacterial secreted proteins: secretory mechanisms and role in pathogenesis Mickael Desvaux, Michel Hébraud To cite this version: Mickael Desvaux, Michel Hébraud. Bacterial secreted proteins: secretory mechanisms and role in pathogenesis. Karl Wooldridge - Caister Academic Press, Norwich UK. Listeria monocytogenes, Chap- ter 14, 2009. hal-02910864 HAL Id: hal-02910864 https://hal.inrae.fr/hal-02910864 Submitted on 18 Sep 2020 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. Listeria monocytogenes Mickaël Desvaux and Michel Hébraud 14 Abstract noting that the previously distinct species L. mur- As a monoderm prokaryote, protein secretion rayi is now assigned to the single species L. grayi systems in Listeria monocytogenes are distinct (Rocourt et al., 1992). L. ivanovii is comprised from those encounter in diderm bacteria, still of two subspecies, i.e. ivanovii and londiniensis, they remain the gates for expressing protein whereas the subspecies of L. grayi are subsp. functions outside the intracellular bacterial cell grayi and subsp. murrayi. These Low G+C% compartment. Despite the fact that protein se- Gram-positive bacteria belong to phylum BXIII cretion is a key factor in virulence of a pathogen, Firmicutes, class III Bacilli, order I Bacillales, fam- fewer studies have been dedicated to pathogenic ily IV Listeriaceae (Garrity, 2001). While it shares Gram-positive bacteria compared to Gram-neg- the same family with the closely related genus II ative bacteria and L. monocytogenes is no excep- Brochothrix, taxonomic analyses further revealed tion. Among the six protein secretion systems that the genus Listeria occupies an intermediary identified in L. monocytogenes, only proteins position in class III Bacilli between genus Bacillus putatively translocated via the Sec pathway are (order I Bacillales, family I Bacillaceae) and genus indisputably involved in bacterial virulence. The Lactobacillus (order II Lactobacillales, family I 16 secreted virulence effectors characterized to Lactobacillaceae) (Jones, 1988). Phylogenetic date are either (i) associated with the cytoplasmic analyses also suggest that the different Listeria membrane, i.e. as integral membrane proteins or species would have diverged only very recently lipoproteins, (ii) associated with the cell wall, (Collins et al., 1991; Sallen et al., 1996). L. grayi i.e. covalently in a sortase-dependent manner or represents the deepest branch within the genus via cell-wall binding domains, or (iii) released in and the remaining species split into (i) a first the extracellular milieu. Identification of several lineage composed of L. monocytogenes and L. candidates as putative secreted virulence factors innocua and (ii) a second lineage composed of L. as well as the availability in the near future of a welshimeri, L. ivanovii and L. seeligeri (Schmid et large amount of Listeria genomic data from dif- al., 2005). L. monocytogenes is the etiologic agent ferent sequencing projects promise a very excit- of listeriosis in human and animals, whereas L. ing time in the field of listerial protein secretion ivanovii is almost only associated with infections and should provide further insights into how L. in animals (Vazquez-Boland et al., 2001b). The monocytogenes interacts with its biotic or abiotic remaining Listeria species are apparently apatho- surroundings. genic, which would have resulted in the course of evolution from two independent deletion events Introduction of the virulence gene cluster as represented by L. The genus Listeria is hitherto circumscribed to innocua and L. welshimeri, respectively (Schmid only six species namely L. monocytogenes, L. in- et al., 2005). Listerial strains were early serotyped nocua, L. seeligeri, L. welshimeri, L. ivanovii and according to variation of 15 somatic O (subtyped L. grayi (Vaneechoutte et al., 1998); it is worth from I to XV) and five flagellar H (subtyped UNCORRECTED FIRST PROOFS 302 | Desvaux and Hébraud from A to E) antigens derived from methods coined by Pirie in 1940 and named after Lord employed on Gram-negative pathogen Salmo- Lister, a British surgeon, and the fact that an nella (Seeliger and Hohne, 1979; Seeliger and increase in the number of circulating monocytes, Jones, 1986). Though, due to differences in cell i.e. a monocytosis, was found in infected rabbits envelope structure between Gram-negative and and guinea pigs (Gray and Killinger, 1966; Farber Gram-positive bacteria, O antigens could not and Peterkin, 1991). The first case of human lis- be of lipopolysaccharidic nature in Listeria and teriosis dates back to 1929 in Denmark (Nyfelt, serological identification could only result from 1929). From an epidemiological point a view, cross-reactivity of antisera. Indeed, it appeared human listeriosis must be considered as a rare later on that the somatic component of the se- disease as indicated by a low incidence with only rotypic designation in Listeria resides primarily 2–10 reported cases per million populations per in teichoic acids, structurally and antigenically as year (Schuchat et al., 1991; Ramaswamy et al., a result of glycosidic substitutions of the ribitol 2007). In France and the USA, however, listerio- phosphate units (Fiedler et al., 1983; Uchikawa sis is one of most frequent food-borne causes of et al., 1986). Concerning H antigens, it is worth death since it ranks only second after salmonel- noting that variation of flagella expression in losis with a high mortality rate ranging between different growth conditions can result in discrep- 20% and 30% (Mead et al., 1999; Vaillant et al., ant serological results (Peel et al., 1988a; Peel 2005). While overall case fatality rate is not as et al., 1988b). Altogether, 17 distinct serotypes high in other European countries, listeriosis in- (or serovars) have been established in Listeria cidence has significantly increased between 2001 spp. including 13 for L. monocytogenes, i.e. 1/2a, and 2005 in Germany as it increased from 0.26 1/2b, 1/2c, 3a, 3b, 3c, 4a, 4ab, 4b, 4c, 4d, 4e and per 100 000 inhabitants, i.e. 217 cases, to 0.62 7. Molecular subtyping analyses further divided per 100 000 inhabitants, i.e. 519 cases (Koch & L. monocytogenes into three major phylogenetic Stark, 2006). Listeriosis essentially breaks out divisions, with prevalent distribution of sero- in weakened patients namely immunodepressed types (i) 1/2b, 3b, 3c, 4b, 4d and 4e in lineage I, individuals, pregnant women, neonates and eld- (ii) 1/2a, 1/2c, and 3a in lineage II, and (iii) 4a, erly (Vazquez-Boland et al., 2001b). In healthy 4b and 4c in lineage III (Rasmussen et al., 1995; individuals, listerial infection can manifest as a Wiedmann et al., 1997; Nadon et al., 2001; Ward more or less severe gastroenteritis (Swaminathan et al., 2004; Chen et al., 2007). Importantly, while and Gerner-Smidt, 2007). Nonetheless, human good correlation (though not absolute) between listeriosis is a serious food-borne illness caused these three monophyletic lineages and most com- essentially by consumption of contaminated mon serotypes could be ascertained, serotype 4b processed food such as soft cheeses, diary prod- could be found in both lineages I and III, indicat- ucts, smoked fish, processed meats and delicates- ing this serotype could not be used for lineage sen (Farber and Peterkin, 1991; Vazquez-Boland attribution since such L. monocytogenes do not et al., 2001b). The presence of L. monocytogenes represent a distinct evolutionary group (Ward et in foodstuffs mainly results from its ability to al., 2004). Determining irrefutably the serotype survive and multiply under conditions frequently of some Listeria isolates can be very challenging used for food preservation, i.e. low pH, low tem- as phenotypic characteristics may vary in func- perature, low Aw and high salt concentrations tion of environmental conditions. Therefore, (Roberts and Wiedmann, 2003). In addition, these serological methods have now been largely L. monocytogenes also forms biofilms, which overtaken by molecular methods in order to increases its persistence and resistance within clearly identify and differentiate listerial strains industrial production chain lines (Chavant et (Liu, 2006), nonetheless serotyping information al., 2002, 2004) and might facilitate infection is still widely used in everyday practice. (Roberts and Wiedmann, 2003). It is worth Following an epidemic in animal care houses stressing that L. monocytogenes, like other Listeria in Cambridge (UK), Listeria monocytogenes was spp., is a chemoorganoheterotroph, ubiquitous discovered in 1924 by Murray et al. (1926); how- in the environment where it lives as a saprophyte. ever, the final name of this bacterial species was The level of virulence is highly variable from UNCORRECTED FIRST PROOFS Listeria monocytogenes | 303 one bacterial strain to another and there is no tions in only one model bacterium, i.e. Escherichia direct correlation between clinical isolates and coli (Salmond and Reeves, 1993; Wandersman, those originating from the food chain. Indeed, 1993). In the following
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