Role of long polar fimbriae type 1 and 2 in pathogenesis of mammary pathogenic Escherichia coli

Abstract

Escherichia coli is a leading cause of bovine mastitis worldwide. The bacteria can rapidly grow in milk and elicit a strong lipopolysaccharide (LPS)/toll-like receptor-4 (TLR4)-dependent inflammatory response. Recently, the long polar fimbriae (LPF) were identified as a promising virulence factor candidate widely distributed in mammary pathogenic E. coli (MPEC) strains. Mammary pathogenic E. coli possess 2 lpf loci encoding LPF1 and LPF2, respectively. By deleting the major fimbrial subunit gene, lpfA, we found that both LPF1 and LPF2 contribute to MPEC adhesion, invasion, and biofilm formation in vitro. The lpf1A and lpf2A mutants showed reduced cytotoxicity in our in vitro cell infection model. Furthermore, we observed that LPF2 induced a mild TLR4-independent proinflammatory response. The median lethal dose (LD 50 ) of both ∆lpf2A and ∆lpf1A∆lpf2A mutants to BALB/c mice increased by 0.38 and 0.15 logs, respectively, whereas that of wild-type strain MPJS13 was 8.69 logs. In contrast, LPF1 deficiency significantly enhanced the LPS/ TLR4-mediated inflammatory response in mammary epithelial cells, and the LD 50 of the mutant decreased to 8.18 logs. In conclusion, our data suggested that LPF are important in MPEC colonization of mammary cells and may provide a benefit to bacterial intracellular survival that induces persistent bovine mastitis.

Escherichia coli Mastitis in Dairy Cattle: Etiology, Diagnosis, and Treatment Challenges

“…These niches include competing microbes, soluble and cellular antimicrobials in milk, e.g., lactoferrin and lactoperoxidase ( Kawai et al, 2015 ; Koshiishi et al, 2017 ), and the innate response elicited by immune cells ( Wellnitz and Bruckmaier, 2012 ). Consequently, E. coli with specific VFs selected within the mammary gland are better suited to cause bovine mastitis ( Blum et al, 2015 ; Richards et al, 2015 ; Goldstone et al, 2016 ; Roussel et al, 2017 ; Sun et al, 2021 ; Zhou et al, 2021 ).…”

“…The mammary gland is not a natural or primary habitat for E. coli because of the milk-associated innate immunity components, such as antimicrobial peptides, lysozyme, lactoferrin, and complement ( Alamdari and Ehsani, 2017 ; Karav et al, 2017 ; Kuhi et al, 2021 ). However, some E. coli have acquired specific virulence factors (VFs) that might help the bacteria to invade the mammary gland, survive, and multiply in milk ( Blum et al, 2008 , 2015 , 2018 ; Olson et al, 2018 ; Salamon et al, 2020 ; Zhou et al, 2021 ), turning the mammary gland into an amenable opportunistic habitat for these bacteria. Given the relevance of mastitis caused by E. coli , this paper reviews the important aspects of the disease, the characteristic of the etiologic agent E. coli , diagnosis, and treatments.…”

Unveiling distinct genetic features in multidrug-resistant Escherichia coli isolated from mammary tissue and gut of mastitis induced mice

“…Virulence genes (VFGs) that code for toxins, hemolysins, adhesins, and lipopolysaccharides were identified in E. coli from bovine mastitis [ 27 , 28 ]. Although, mammary gland is not a natural or primary habitat for E. coli , some of the strains of this pathogen might acquire specific VFGs that help them to invade the mammary gland creating an amenable opportunistic habitat for survival, multiplication and subsequent pathogenesis [ 29 , 30 ]. So far, bovine mastitis associated E. coli are well investigated in different countries [ 29 , 30 ], only sporadic studies have been conducted on the molecular epidemiology, phylogenetic diversity, resistome, virulome, and metabolic potentials of E. coli from bovine mastitis cases in Bangladesh [ 4 ].…”

“…Although, mammary gland is not a natural or primary habitat for E. coli , some of the strains of this pathogen might acquire specific VFGs that help them to invade the mammary gland creating an amenable opportunistic habitat for survival, multiplication and subsequent pathogenesis [ 29 , 30 ]. So far, bovine mastitis associated E. coli are well investigated in different countries [ 29 , 30 ], only sporadic studies have been conducted on the molecular epidemiology, phylogenetic diversity, resistome, virulome, and metabolic potentials of E. coli from bovine mastitis cases in Bangladesh [ 4 ]. Moreover, no report has been published on the phylogenomic diversity, molecular typing and genomic potentials (resistome, virulome and metabolic functions) of E. coli isolated from mice with mastitis.…”

Genomic insights of mcr-1 harboring Escherichia coli by geographical region and a One-Health perspective

“…In the E. coli isolates from environmental and food/feed samples, the lpfA gene (long polar fimbriae associated with adherence) was detected with considerable frequency (71 and 86% of the analyzed genomes) in comparison with isolates from human and animal origin. lpfA was commonly associated with enteropathogenic E. coli ( Ross et al, 2015 ; Zhou et al, 2021 ). In a recent study carried out in Brazil, there was a statistically significant increased presence of the lpfA gene ( p < 0.05) in E. coli from agricultural soils in comparison with the isolates from non-agriculture origin ( Furlan and Stehling, 2021 ), highlighting the role of animal manure as potential source of virulence genes.…”