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Potential Pathogenicity of Aeromonas Hydrophila Complex Strains Isolated from Clinical, Food and Environmental Sources

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Potential Pathogenicity of Aeromonas Hydrophila Complex Strains Isolated from Clinical, Food and Environmental Sources Canadian Journal of Microbiology Potential pathogenicity of Aeromonas hydrophila complex strains isolated from clinical, food and environmental sources Journal: Canadian Journal of Microbiology Manuscript ID cjm-2015-0466.R1 Manuscript Type: Article Date Submitted by the Author: 03-Dec-2015 Complete List of Authors: Albarral, Vicenta; Universitat de Barcelona, Microbiologia i Parasitologia Sanitàries Draft Sanglas, Ariadna; Universitat de Barcelona, Microbiologia i Parasitologia Sanitàries Palau, Montserrat; Universitat de Barcelona, Microbiologia i Parasitologia Sanitàries Miñana-Galbis, David; Universitat de Barcelona, Microbiologia i Parasitologia Sanitàries Fusté, M. Carmen; Universitat de Barcelona, Microbiologia i Parasitologia Sanitàries; Universitat de Barcelona, Institut de Recerca de la Biodiversitat (IRBio) <i>Aeromonas hydrophila</i> complex, virulence factors, enterotoxins, Keyword: Caco-2 https://mc06.manuscriptcentral.com/cjm-pubs Page 1 of 29 Canadian Journal of Microbiology 1 RESEARCH ARTICLE 2 3 Potential pathogenicity of Aeromonas hydrophila complex strains isolated from clinical, 4 food and environmental sources 5 Vicenta Albarral 1, Ariadna Sanglas 1, Montserrat Palau 1, David Miñana-Galbis 1*, and M. Carmen Fusté 1,2 6 7 1Departament de Microbiologia i Parasitologia Sanitàries, Facultat de Farmàcia, Universitat de 8 Barcelona. Av. Joan XXIII s/n, 08028 Barcelona, Spain. 9 2Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona. Av. Diagonal 643, 08028 10 Barcelona, Spain. 11 12 13 *Corresponding author: Draft 14 David Miñana-Galbis 15 Mailing address: Departament de Microbiologia i Parasitologia Sanitàries, Facultat de Farmàcia, 16 Universitat de Barcelona, Av. Joan XXIII s/n, 08028. Barcelona, Spain 17 Phone: +34 93 402 44 97 18 Fax: +34 93 402 44 98 19 Email: [email protected] 20 21 Email address: 22 Vicenta Albarral, [email protected] 23 Ariadna Sanglas, [email protected] 24 Montserrat Palau, [email protected] 25 M. Carmen Fusté, [email protected] 26 27 Running title 28 Potential pathogenicity of the A. hydrophila complex 29 1 https://mc06.manuscriptcentral.com/cjm-pubs Canadian Journal of Microbiology Page 2 of 29 30 Abstract 31 Aeromonas are autochthonous inhabitants of aquatic environments including chlorinated and polluted 32 waters, although they can also be isolated from a wide variety of environmental and clinical sources. 33 They cause infections in vertebrates and invertebrates and are considered to be an emerging 34 pathogen in humans, producing intestinal and extra-intestinal diseases. Most of the clinical isolates 35 correspond to A. hydrophila , A. caviae , and A. veronii bv. Sobria, which are described as the causative 36 agents of wound infections, septicaemia and meningitis in immunocompromised people, and diarrhoea 37 and dysenteric infections in the elderly and children. The pathogenic factors associated with 38 Aeromona s are multifactorial and involve structural components, siderophores, quorum sensing 39 mechanisms, secretion systems, extracellular enzymes and exotoxins. 40 41 In this study, we analysed a representative number of clinical and environmental strains belonging to 42 the A. hydrophila species complex to evaluateDraft their potential pathogenicity. We thereby detected their 43 enzymatic activities and antibiotic susceptibility pattern, and the presence of virulence genes ( aer , alt , 44 ast and ascV ). The notably high prevalence of these virulence factors, even in environmental strains, 45 indicated a potential pathogenic capacity. Additionally, we determined the adhesion capacity and 46 cytopathic effects of this group of strains in Caco-2 cells, most strains exhibiting adherence and 47 causing complete lysis. 48 49 Keywords Aeromonas hydrophila complex, virulence factors, enterotoxins, Caco-2. 50 2 https://mc06.manuscriptcentral.com/cjm-pubs Page 3 of 29 Canadian Journal of Microbiology 51 52 Introduction 53 The genus Aeromonas Stanier 1943 belongs to the family Aeromonadaceae within the class 54 Gammaproteobacteria (Martin-Carnahan and Joseph 2005). Aeromonas are autochthonous inhabitants 55 of aquatic environments, including chlorinated and polluted waters, although they can also be isolated 56 from a wide variety of environmental and clinical sources. They cause infections in vertebrates and 57 invertebrates, such as frogs, birds, various fish species and domestic animals. Aeromonas is 58 considered to be an emerging pathogen in humans (Janda and Abbott 1998), producing intestinal and 59 extra-intestinal diseases. Most of the clinical isolates correspond to A. hydrophila , A. caviae , and A. 60 veronii bv. Sobria, which are described as the causative agents of wound infections, septicaemia and 61 meningitis in immunocompromised people, and diarrhoea and dysenteric infections in the elderly and 62 children (Kirov et al. 2004). 63 Draft 64 The pathogenic factors associated with Aeromona s are multifactorial and involve structural 65 components (flagella, fimbriae, capsule, S-layers, lipopolysaccharide, and outer membrane proteins), 66 siderophores, quorum sensing mechanisms, secretion systems (T2SS, T3SS, T4SS, and T6SS), 67 extracellular enzymes (proteases with caseinase and elastase activities, lipases such as phospholipases 68 and cholesterol acyltransferase) and exotoxins (Tomás 2012; Beaz-Hidalgo and Figueras 2013; Grim 69 et al. 2013). 70 71 Two main types of enterotoxins have been described in this genus, cytotonic and cytotoxic. Cytotoxic 72 enterotoxins produce severe damage in the small intestine mucous membrane. Aer toxin (also named 73 aerolysin or Act), the main enterotoxin described in Aeromonas , shows haemolytic, cytotoxic and 74 enterotoxic activities, is thermolabile, inhibits phagocytosis and increases the TNF-α and interleukin IL- 75 1β intracellular levels in macrophages. The Aeromonas cytotonic enterotoxins, such as Alt 76 (thermolabile) and Ast (thermostable), do not destroy the intestinal mucous membrane. Instead, they 77 increase the prostaglandin intracellular levels in the enterocytes and activate the adenylate cyclase, 78 thereby increasing cAMP synthesis and triggering a fluid secretion, which causes liquid diarrhoea 79 (Aguilera-Arreola et al . 2007; Chang et al. 2008; Janda and Abbott 2010; Ottaviani et al. 2011). Some 3 https://mc06.manuscriptcentral.com/cjm-pubs Canadian Journal of Microbiology Page 4 of 29 80 strains possess a type III secretion system (T3SS), which enables many pathogenic gram-negative 81 bacteria to secrete and inject pathogenicity proteins (effectors) into the cytosol of eukaryotic cells via 82 needle-like structures called needle complexes or injectisomes. T3SS was first identified in pathogenic 83 strains of Yersinia spp. (Michiels et al. 1990). In Aeromonas T3SS has been identified in A. 84 salmonicida , A. caviae , A. veronii bv. Sobria and A. hydrophila (Vilches et al. 2004; Krzymińska et al. 85 2012). Since this mechanism correlates with bacterial pathogenicity, its presence is used as a general 86 indicator of bacterial virulence. 87 88 Potential pathogenicity of Aeromonas strains has also been associated with adherence and 89 cytopathogenic effects in Hep-2 (derived from a human laryngeal carcinoma), Vero (derived from 90 normal kidneys of the African green monkey), and HT29 and Caco-2 cell lines (both derived from 91 human colorectal adenocarcinoma) (Snowden et al. 2006; Couto et al. 2007; Janda and Abbott 2010; 92 Ottaviani et al. 2011). Draft 93 94 The A. hydrophila species complex (AHC) consists of a group of genetically closely related species that 95 are phenotypically difficult to discriminate (Miñana-Galbis et al. 2002), which includes: A. hydrophila , 96 with three subspecies (A. hydrophila subsp. hydrophila, A. hydrophila subsp. dhakensis and A. 97 hydrophila subsp. ranae ) and A. bestiarum , A. popoffii and A. salmonicida, divided in five subspecies 98 (A. salmonicida subsp. salmonicida , A. salmonicida subsp. achromogenes , A. salmonicida subsp. 99 masoucida , A. salmonicida subsp. pectinolytica and A. salmonicida subsp. smithia ) (Miñana-Galbis et 100 al. 2002; Martin-Carnahan and Joseph 2005; Fusté et al . 2012). Two additional species have been 101 recently described in this group, A. aquariorum and A. piscicola (Martínez-Murcia et al. 2008; Beaz- 102 Hidalgo et al. 2009), while A. hydrophila subsp. dhakensis and A. aquariorum have been reclassified in 103 A. dhakensis (Beaz-Hidalgo et al. 2013). 104 105 In this study, we analysed a representative number of clinical, food and environmental strains 106 belonging to the AHC to evaluate their potential pathogenicity. We thereby detected their enzymatic 107 activities and antibiotic susceptibility pattern, the presence of virulence genes ( aer , alt , ast and ascV ), 108 and their adhesion capacity and cytopathic effects in Caco-2 cells. 4 https://mc06.manuscriptcentral.com/cjm-pubs Page 5 of 29 Canadian Journal of Microbiology 109 110 Materials and methods 111 Bacterial strains 112 A total of 127 strains belonging to the “ Aeromonas hydrophila complex" (26 A. bestiarum , 15 A. 113 dhakensis , 29 A. hydrophila , 11 A. piscicola , 6 A. popoffii and 40 A. salmonicida ), isolated from fresh 114 waters, marine bivalve molluscs and clinical samples, were analysed in this study (Table S1). Strains 115 were obtained from different culture collections, our own collection or donated by different 116 researchers. These strains were previously identified in a taxonomic study based on multilocus 117 sequence analysis of
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