Characterization of beta-lactam-resistant Escherichia coli from Australian fruit bats indicates anthropogenic origins

Abstract

Antimicrobial-resistant Escherichia coli , particularly those resistant to critically important antimicrobials, are increasingly reported in wildlife. The dissemination of antimicrobial-resistant bacteria to wildlife indicates the far-reaching impact of selective pressures imposed by humans on bacteria through misuse of antimicrobials. The grey-headed flying fox (GHFF; Pteropus poliocephalus), a fruit bat endemic to eastern Australia, commonly inhabits urban environments and encounters human microbial pollution. To determine if GHFF have acquired human-associated bacteria, faecal samples from wild GHFF (n=287) and captive GHFF undergoing rehabilitation following illness or injury (n=31) were cultured to detect beta-lactam-resistant E. coli . Antimicrobial susceptibility testing, PCR and whole genome sequencing were used to determine phenotypic and genotypic antimicrobial resistance profiles, strain type and virulence factor profiles. Overall, 3.8 % of GHFF carried amoxicillin-resistant E. coli (wild 3.5 % and captive 6.5 %), with 38.5 % of the 13 GHFF E. coli isolates exhibiting multidrug resistance. Carbapenem (bla NDM-5) and fluoroquinolone resistance were detected in one E. coli isolate, and two isolates were resistant to third-generation cephalosporins (bla CTX-M-27 and ampC). Resistance to tetracycline and trimethoprim plus sulfamethoxazole were detected in 69.2% and 30.8 % of isolates respectively. Class 1 integrons, a genetic determinant of resistance, were detected in 38.5 % of isolates. Nine of the GHFF isolates (69.2 %) harboured extraintestinal virulence factors. Phylogenetic analysis placed the 13 GHFF isolates in lineages associated with humans and/or domestic animals. Three isolates were human-associated extraintestinal pathogenic E. coli (ST10 O89:H9, ST73 and ST394) and seven isolates belonged to lineages associated with extraintestinal disease in both humans and domestic animals (ST88, ST117, ST131, ST155 complex, ST398 and ST1850). This study provides evidence of anthropogenic multidrug-resistant and pathogenic E. coli transmission to wildlife, further demonstrating the necessity for incorporating wildlife surveillance within the One Health approach to managing antimicrobial resistance.

Genomic Analysis of an I1 Plasmid Hosting a sul3-Class 1 Integron and blaSHV-12 within an Unusual Escherichia coli ST297 from Urban Wildlife

“…Nonetheless, investigations of urban gulls and pigeons repeatedly produced Escherichia coli and Salmonella enterica that carry genes encoding resistance to fluoroquinolones, carbapenems and extended spectrum β-lactams [ 27 , 28 , 29 , 30 , 31 ]. In Australia, MDR E. coli have also been recovered from penguins [ 32 ] and bats [ 33 ], indicating that enterobacterial flora carried by wildlife species that intersect with human populations readily harbor ARG combinations that mirror those circulating in veterinary and human clinical environments. The sul3 gene has been reported globally and often in association with E. coli sourced from intensive animal production but also frequently in humans [ 34 ].…”

Carriage of antibiotic resistant bacteria in endangered and declining Australian pinniped pups

“…are multiple reports of IS26 class 1 integron variants in E. coli from animals in Australia, including cows and pigs [18,51,52] and Grey-headed flying foxes (Pteropus poliocephalus) [53], as well as in human clinical cases [54]. The presence of class 1 integrons with IS26 variants in E. coli isolates from free-ranging A. p. doriferus pups provides further evidence to suggest that this colony is exposed to a marine environment that is contaminated by various sources of anthropogenic pollution.…”

Multidrug-Resistant High-Risk Escherichia coli and Klebsiella pneumoniae Clonal Lineages Occur in Black-Headed Gulls from Two Conservation Islands in Germany

“…The occurrence of five clinically relevant representatives belonging to international high-risk clonal lineages among only 12 ESBL-producing strains is remarkable. ST131 has not only been reported as the major E. coli clone in the clinical setting [ 32 ] but is often also found in veterinary, food, and environmental settings [ 52 , 53 ]. While previous studies have frequently found MDR ST58 strains in farm animals and, to a lesser extent, in wild birds [ 54 , 55 ] and as contaminants of retail meat [ 21 ], ST38 has been detected in several animal species, including broilers, rats, and black-headed gulls [ 12 , 56 ], with the latter matching our results.…”