Seagulls and Superbugs: Role of genomics in understanding the spread of antimicrobial resistance
Antimicrobial resistance is regarded as one of the greatest threats to human and animal health. Resistance to critically important antimicrobials (CIAs) or drugs of last resort such as extended-spectrum cephalosporins (ESCs), fluoroquinolones (FQs), colistin and carbapenems amongst Enterobacteriaceae and other Gram-negative bacteria is a major public health concern. This is attributed to co-associated resistance to other classes of antimicrobials and limited therapeutic options to treat infections with CIA-resistant bacteria in both humans and animals. Globally, emergence and dissemination of CIA-resistance in livestock, wild birds and companion animals are a major concern due to the potential for direct or indirect transfer of such resistant bacteria to humans Our recent study  investigated the ecology, epidemiology and origins of CIA-resistant Escherichia coli carried by Australian Silver Gulls (Chroicocephalus novaehollandiae), a gregarious avian wildlife species that is a common inhabitant of coastal areas with high levels of human contact. Sampling locations were widely dispersed around the perimeter of Australian continent, with sites separated by up to 3,500 km. Whole-genome sequencing was used to study the diversity and molecular characteristics of resistant isolates to ascertain their epidemiological origin. Investigation of 562 fecal samples revealed wide spread occurrence of extended-spectrum cephalosporin (21.7%) and fluoroquinolone (23.8%) resistant E. coli. Genome sequencing revealed CIA-resistant E. coli isolates (n=284) from gulls predominantly belonged to human-associated extra-intestinal pathogenic E. coli (ExPEC) clones responsible for causing urinary tract infections and sepsis in humans. This included globally disseminated clones such as ST131 (17%), ST10 (8%), ST1193 (6%), ST69 (5%), ST38 (4%). Comparative genomic analysis revealed that pathogenic and resistant E. coli clones isolated from gulls overlapped extensively with human clinical isolates from Australia and overseas. One isolate from Victoria was resistant to carbapenems and another isolate from Western Australia was resistant to colistin. Carbapenems and colistin are last resort antimicrobials used to treat multidrug-resistant bacterial infections. This study uniquely establishes that Australian Silver Gulls are carriers of virulent and CIA-resistant human-associated pathogenic E. coli clones. The carriage of diverse CIA-resistant E. coli clones that strongly resemble pathogenic clones from humans, suggests that seagulls can act as ecological sponges indiscriminately accumulating and disseminating CIA-resistant bacteria over vast distances. The study illustrates the broader community risk entailed in transmission of CIA-resistant pathogenic E. coli in a cycle that encompasses humans, seagulls and the environment.