Genomic data reveal international lineages of critical priority Escherichia coli harbouring wide resistome in Andean condors (Vultur gryphus Linnaeus, 1758)

Abstract

Critical priority pathogens have globally disseminated beyond clinical settings, thereby threatening wildlife. Andean Condors (Vultur gryphus) are essential for ecosystem health and functioning, but their populations are globally near threatened and declining due to anthropogenic activities. During a microbiological and genomic surveillance study of critical priority antibiotic‐resistant pathogens, we identified pandemic lineages of multidrug‐resistant extended‐spectrum β‐lactamase (ESBL)‐producing Escherichia coli colonizing Andean Condors admitted at two wildlife rehabilitation centres in South America. Genomic analysis revealed the presence of genes encoding resistance to hospital and healthcare agents among international E. coli clones belonging to sequence types (STs) ST162, ST602, ST1196 and ST1485. In this regard, the resistome included genes conferring resistance to clinically important cephalosporins (i.e., CTX‐M‐14, CTX‐M‐55 and CTX‐M‐65 ESBL genes), heavy metals (arsenic, mercury, lead, cadmium, copper, silver), pesticides (glyphosate) and domestic/hospital disinfectants, suggesting a link with anthropogenic environmental pollution. On the other hand, the presence of virulence factors, including the astA gene associated with outbreak of childhood diarrhoea and extra‐intestinal disease in animals, was identified, whereas virulent behaviour was confirmed using the Galleria mellonella infection model. E. coli ST162, ST602, ST1196 and ST1485 have been previously identified in humans and food‐producing animals worldwide, indicating that a wide resistome could contribute to rapid adaptation and dissemination of these clones at the human–animal–environment interface. Therefore, these results highlight that Andean Condors have been colonized by critical priority pathogens, becoming potential environmental reservoirs and/or vectors for dissemination of virulent and antimicrobial‐resistant bacteria and/or their genes, in associated ecosystems and wildlife.

Antimicrobial Resistance Glides in the Sky—Free-Living Birds as a Reservoir of Resistant Escherichia coli With Zoonotic Potential

“…This finding indicates that ubiquitous birds might be exposed to the anthropogenic impact and acquisition of resistant bacteria through contact with the waste of human or livestock origin. Resistance toward antimicrobial classes that we found prevailing (beta-lactams, tetracyclines, quinolones, aminoglycosides, folate path inhibitors) was also reported in bird communities from distinct geographical areas worldwide, from the Americas through Africa, Europe, Asia to Australia (Nascimento et al, 2003;Guenther et al, 2010b;Literak et al, 2010;Poirel et al, 2012;Veldman et al, 2013;Mohsin et al, 2016;Guenther et al, 2017;Ahlstrom et al, 2018;Marcelino et al, 2019;Zurfluh et al, 2019;Cao et al, 2020;Fuentes-Castillo et al, 2020;Nabil et al, 2020). Moreover, AMR toward those substances was commonly found in E. coli from farm animals and reported from other wildlife species (Navarro-Gonzalez et al, 2013;Wasyl et al, 2013Wasyl et al, , 2018Ceccarelli et al, 2020).…”

ESBL-Producing Escherichia coli Carrying CTX-M Genes Circulating among Livestock, Dogs, and Wild Mammals in Small-Scale Farms of Central Chile

“…For example, a previous study estimated a 4% prevalence of ESBL- E. coli among vampire bats ( Desmodus rotundus ) in Peru using a similar methodology for screening [ 12 ]. Previous studies conducted in Chile and Latin America have detected the presence of ESBL- E. coli on wild birds including gulls [ 36 ], Andean condors [ 43 ], and three species of owls [ 42 ]. Likewise, bla CTX-M genes have been previously detected using qPCR methods from feces in Andean foxes [ 52 ] and the guiña ( Leopardus guigna ) [ 74 ], although the bacteria species carrying the genes, and whether it was expressed or not, remains unknown.…”

“…Chile, considered a high income economy but with an agricultural production more similar to LMICs, launched the ‘National plan to combat antimicrobial resistance’ in 2017, but no national surveillance has been implemented yet in the agricultural sector. ESBL- E. coli have not been detected in Chilean cattle herds [ 39 , 40 ], but have been isolated in feces from dogs [ 41 ], owls in rehabilitation centers [ 42 ], wild Andean condors ( Vultur gryphus ) [ 43 ] and gulls ( Leucophaeus pipixcan ) [ 36 ]. To our knowledge, no study has investigated the ESBL- E. coli fecal carriage of livestock nor simultaneously focused on dogs and wild mammals living closely to livestock.…”

Exposure to Anthropogenic Areas May Influence Colonization by Zoonotic Microorganisms in Scavenging Birds

“…It is important to note that we did not study strict anaerobic bacteria, however, our findings are relevant since this is the first study addressing and comparing aerobic bacteria from oropharynx and cloaca in a large number of wild and captive Andean condors (but see [ 64 ] for Escherichia coli ). Our study should serve as a starting point for further investigations that deepen and complement the knowledge of the microbiota of vultures using different environments.…”