Chicken‐source Escherichia coli within phylogroup F shares virulence genotypes and is closely related to extraintestinal pathogenic E. coli causing human infections

Abstract

ExPEC is an important pathogen that causes diverse infection in the human extraintestinal sites. Although avian-source phylogroup F Escherichia coli isolates hold a high level of virulence traits, few studies have systematically assessed the pathogenicity and zoonotic potential of E. coli isolates within phylogroup F. A total of 1,332 E. coli strains were recovered from chicken colibacillosis in China from 2012 to 2017. About 21.7% of chicken-source E. coli isolates were presented in phylogroup F. We characterized phylogroup F E. coli isolates both genotypically and phenotypically. There was a widespread prevalence of ExPEC virulence-related genes among chicken-source E. coli isolates within phylogroup F. ColV/BM plasmid-related genes (i.e. hlyF, mig-14p, ompTp, iutA and tsh) occurred in the nearly 65% of phylogroup F E. coli isolates. Population structure of chicken-source E. coli isolates within phylogroup F was revealed and contained several dominant STs (such as ST59, ST354, ST362, ST405, ST457 and ST648). Most chicken-source phylogroup F E. coli held the property to produce biofilm and exhibited strongly swimming and swarming motilities.Our result showed that the complement resistance of phylogroup F E. coli isolates was closely associated with its virulence genotype. Our research further demonstrated the zoonotic potential of chicken-source phylogroup F E. coli isolates. The phylogroup F E. coli isolates were able to cause multiple diseases in animal models of avian colibacillosis and human infections (sepsis, meningitis and UTI). The chickensource phylogroup F isolates, especially dominant ST types, might be recognized as a high-risk food-borne pathogen. This was the first study to identify that chickensource E. coli isolates within phylogroup F were associated with human ExPEC pathotypes and exhibited zoonotic potential. K E Y W O R D S chicken-source E. coli, ExPEC pathotypes, phylogroup F, population structure, zoonotic potential | 881 ZHUGE Et al. | INTRODUC TI ONBased on the disease syndrome, pathogenic Escherichia coli is classified as intestinal pathogenic E. coli (InPEC) and ExPEC (Rodriguez-

Avian Pathogenic Escherichia coli (APEC): An Overview of Virulence and Pathogenesis Factors, Zoonotic Potential, and Control Strategies

“…Adherence in APEC is facilitated primarily by type 1 fimbriae, P fimbriae, and S fimbriae [ 2 , 31 ]. Several genes encoding these fimbriae and additional adhesins, fim H, fim C (type 1 fimbriae), pap A, pap C, pap EF, pap G I, pap G II, pap GIII, fel A (P fimbriae), sfa / sfa S (S fimbriae), foc GE (F1C fimbriae), afa IBC (afimbriae), lpf A, lpf 0141, lpf 0154 (long polar fimbriae), mat / ecp A (fimbrillin), flg E (flagellar hook), crl , csg (curli), tsh (temperature-sensitive haemagglutinin), bma E (M hemagglutinin), hra / hrl A/ hek (heat-resistant agglutinin), iha (IrgA homologue adhesin), yqi G (putative outer membrane usher protein), and kii (K capsule encoding genes) have been reported in APEC [ 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 ]. These adhesins also mediate motility, biofilm formation, and APEC survival in macrophages [ 31 ].…”

“…In particular, protectins include bacterial capsules, outer membrane proteins, and lipopolysaccharide (LPS) components, and they provide protection against phagocytic engulfment by macrophages and complement-mediated bactericidal effect in the host serum [ 2 , 31 ]. Several genes encoding multiple protectins, iss (increased serum survival), tra T (complement resistance protein), omp T (outer membrane protease), kps MT(K1), kps MT(II), kps MT(III), neu C, neu S, neu D (capsule), kfi C-K5 (glycosyl transferase), and bet A (choline dehydrogenase) have been reported in APEC [ 36 , 41 , 51 , 53 , 61 ]. These protectins also mediate APEC adhesion, invasion, intracellular survival, colonization, and proliferation in the host, in addition to protection from host defense [ 61 ].…”

“…Toxins are biological poisons that assist in the bacterial ability to invade and cause damage to the tissues [ 2 , 31 ]. Several genes encoding multiple types of toxins, hly F, hly A, hly E (putative avian hemolysin), vat (vacuolating autotransporter toxin), sat (secreted autotransporter toxin), cdt B, cdt S (cytolethal distending factor), ast A, EAST-1 (heat-stable enterotoxin), stx2f (shiga toxin variant), pic (serine protease autotransporter), espC (serine protease), and ace 4/35 (acetylcholine esterase) have been reported in APEC [ 35 , 38 , 39 , 40 , 41 , 51 , 53 , 69 , 70 , 71 , 72 , 73 ]. These toxins also facilitate the colonization, motility, biofilm formation, agglutination, induction of vacuolization, and formation of outer membrane vesicles [ 69 ].…”

“…eil A is a component of a type III secretion system, whereas cel B and pab B are involved in sugar transport and tetrahydrofolate biosynthesis, respectively. In addition, genes such as cap U (cap locus protein), cif (cell cycle inhibiting factor), tir (translocated intimin receptor), tccp (tir cytoskeleton coupling protein), nle B (non-LEE encoded effector B) [ 57 ], ia L (invasion-associated locus), cjr C (putative siderophore receptor) [ 108 ], and mig-14p (antimicrobial resistance protein) [ 41 ] have been also reported in APEC. cap U is putative hexosyltransferase with uncharacterized function, whereas cif belongs to bacterial toxins that arrest host cell division.…”

“…coli , similar to UPEC and NMEC [ 4 ]. Multiple studies have reported APEC as a potential foodborne zoonotic pathogen as well as a source or reservoir of extra-intestinal infections in humans [ 21 , 22 , 41 , 116 , 117 , 118 , 119 , 120 , 121 , 122 , 123 , 124 , 125 , 126 , 127 , 128 , 129 , 130 , 131 , 132 , 133 , 134 , 135 , 136 , 137 , 138 , 139 , 140 , 141 , 142 , 143 ]. This is in particular due to its shared genetic similarity with human ExPECs, the presence of common or human ExPEC-defining virulence genes, and the ability to cause UTI and meningitis in rodent models, similar to UPEC and NMEC.…”