A Virulent Trueperella pyogenes Isolate, Which Causes Severe Bronchoconstriction in Porcine Precision-Cut Lung Slices.

Lei Qin,Yong-Bo Yang,Yan-Dong Tang,Fandan Meng,Gang Wang,Xuehui Cai,Mingxia Sun,Haijuan He,Wenlong Zhang,Shujie Wang

doi:10.3389/fvets.2021.824349

Abstract

Trueperella pyogenes causes disease in cattle, sheep, goats and swine, and is involved occasionally in human disease worldwide. Most reports implicating T. pyogenes have been associated with clinical cases, whereas no report has focused on pathogenicity of T. pyogenes in mouse models or precision-cut lung slice (PCLS) cultures from swine. Here, we isolated and identified a virulent, β-hemolytic, multidrug-resistant T. pyogenes strain named 20121, which harbors the virulence marker genes fimA, fimE, nanH, nanP and plo. It was found to be highly resistant to erythromycin, azithromycin and medemycin. Strain 20121 was pathogenic in mouse infection models, displaying pulmonary congestion and inflammatory cell infiltration, partial degeneration in epithelial cells of the tracheal and bronchiolar mucosa, a small amount of inflammatory cell infiltration in the submucosa, and bacteria (>104 CFU/g) in the lung. Importantly, we used T. pyogenes 20121 to infect porcine precision-cut lung slices (PCLS) cultures for the first time, where it caused severe bronchoconstriction. Furthermore, dexamethasone showed its ability to relieve bronchoconstriction in PCLS caused by T. pyogenes 20121, highlighting dexamethasone may assist antibiotic treatment for clinical T. pyogenes infection. This is the first report of T. pyogenes used to infect and cause bronchoconstriction in porcine PCLS. Our results suggest that porcine PCLS cultures as a valuable 3D organ model for the study of T. pyogenes infection and treatment in vitro.

Highlights

Trueperella pyogenes is a Gram-positive, non-motile, non-spore-forming, short, rod- to coccobacillus-shaped bacterium that occurs singly, in pairs or in clusters
This study demonstrates that porcine precision-cut lung slices (PCLS) is a suitable 3D organ model for the study of pathogenicity of T. pyogenes in vitro
Electron micrographs of ultrathin sections showed the strain was most likely encapsulated with 10–25 nm cell wall thickness (Figure 1C). 16S rRNA sequencing indicated that the isolate was T. pyogenes, which harbored virulence factor genes plo, fimA, fimE, nanH and nanP

Summary

Introduction

Trueperella pyogenes is a Gram-positive, non-motile, non-spore-forming, short, rod- to coccobacillus-shaped bacterium that occurs singly, in pairs or in clusters. T. pyogenes was previously called Corynebacterium pyogenes, Actinomyces pyogenes and Arcanobacterium pyogenes, in chronological order [1, 2]. In 2011, according to Yassin et al, Arcanobacterium pyogenes was renamed as T. pyogenes based on phylogenetic and chemotaxonomic observations [2]. T. pyogenes expresses several established and putative virulence factors. Known virulence factors mainly include exotoxin pyolysin (PLO), and others promote adhesion factors such as fimbriae (Fim), neuraminidase (NanH, NanP) and collagen-binding protein (CbpA) [3, 4]. The cytolysin PLO is considered to be a major virulence factor, associated with cell damage induced by T. pyogenes infection [5]. Adhesion factors may be associated with mucosal adherence and colonization of host tissues, thereby contributing to the pathogenicity of T. pyogenes [3]

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