Proximity to urbanization is associated with antimicrobial-resistant enteric pathogens in wild bird microbiomes

Authors: MOURKAS, EVANGELOS - Oxford University; VALDEBENITO, JOSE - Universidad De Chile; MARSH, HANNAH - Oxford University; HITCHINGS, MATTHEW - Swansea University; COOPER, KERRY - University Of Arizona; Parker, Craig; SZÉKELY, TAMAS - University Of Debrecen; JOHANSSON, HÅKAN - Linnaeus University; ELLSTRÖM, PATRIK - Uppsala University; PASCOE, BEN - Oxford University; WALDENSTRÖM, JONAS - Linnaeus University; SHEPPARD, SAMUEL - Oxford University

Submitted to: Nature Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/16/2024
Publication Date: 8/13/2024
Citation: Mourkas, E., Valdebenito, J.O., Marsh, H., Hitchings, M.D., Cooper, K.K., Parker, C.T., Székely, T., Johansson, H., Ellström, P., Pascoe, B., Waldenström, J., Sheppard, S.K. 2024. Proximity to urbanization is associated with antimicrobial-resistant enteric pathogens in wild bird microbiomes. Nature Ecology and Evolution. 34:1-11. https://doi.org/10.1016/j.cub.2024.07.059.
DOI: https://doi.org/10.1016/j.cub.2024.07.059

Interpretive Summary: Urbanization is dramatically changing Earth’s ecosystems. Today, more than half of all people live in urban areas, with the proportion expected to rise to 70% by 2050. Accommodating the ever-growing human population requires the expansion of densely populated areas, but this has serious consequences. Shrinking of natural habitats forces wild animals into urbanized areas but only species with behavioral plasticity successfully adapt to these new environments. Because of the potential for large home-ranges, birds that tolerate urbanization, such as crows and gulls, could transmit zoonotic pathogens, including AMR bacteria. Here, we analyze the impact of urbanization on zoonotic transmission and AMR spread in wild birds using Campylobacter jejuni as a sentinel pathogen species. Our analysis of multiple behavioural and ecological traits confirmed a positive correlation between proximity to urbanization and the number of C. jejuni genotypes and AMR genes in wild bird hosts. Specifically, wild birds from highly urban areas harboured up to four times more C. jejuni genotypes and six times more antimicrobial resistance genetic determinants on average. This is consistent with increased frequency of transition events. Quantifying zoonotic transmission and gene pool spread in this way is essential in guiding surveillance and control measures against future zoonosis emergences.

Technical Abstract: Human behaviour is dramatically changing global ecology. Nowhere is this more apparent than in urbanization, where novel high human density habitats are disrupting long established ecotones. Resultant changes to the transitional areas between organisms, especially enhanced contact between humans and wild animals, provides new opportunities for the spread of zoonotic pathogens, posing a serious threat to global public health. Here, by studying the multi-host enteric pathogen Campylobacter jejuni isolated from the gut of 30 bird species in 8 countries, we investigated how proximity to urbanization influenced the spread of antimicrobial resistant (AMR) strains. Generalized linear models compared multiple behavioural and ecological traits and confirmed a positive correlation between proximity to urbanization and the number of C. jejuni genotypes and AMR genes in wild bird hosts. Specifically, wild birds from highly urban areas harboured approximately up to four times more C. jejuni genotypes and six times more antimicrobial resistance genetic determinants on average. This is consistent with increased frequency of transition events. Quantifying zoonotic transmission and gene pool spread in this way is essential in guiding surveillance and control measures against future zoonosis emergences.