Emerging Threats at the Intersection of Wildlife and Public Health: Investigating the Epidemiology of Chlamydia psittaci and Viral Coinfections in Australian Birds

Vasilli Kasimov

doi:10.25907/00796

The One Health approach recognises that the health of humans is intrinsically linked to the health of animals and our shared environment. Birds are central to One Health, serving as significant vectors and reservoirs for numerous zoonotic bacterial and viral pathogens. As such, our research aimed to investigate the role of birds within the One Health framework, resulting in comprehensive insights into the prevalence, genetic diversity, and potential biosecurity risks posed by avianborne pathogens, particularly those from the genus Chlamydia, within Australia’s avian population. Initially, we investigated the presence and genetic diversity of Chlamydiaceae, including the zoonotic Chlamydia psittaci and other emerging Chlamydia species, in wild birds across Australia, mainly focusing on samples collected from various avian species admitted to the Australia Zoo Wildlife Hospital. Our research revealed an overall Chlamydiaceae prevalence of 29.26% (165/564) and a 3.19% (18/564) prevalence for the zoonotic C. psittaci. Molecular characterisation identified genetically diverse Chlamydia species, including avian Chlamydia abortus, Ca. Chlamydia ibidis, Chlamydia pneumoniae and C, pecorum, all detected within novel avian host species in Australia for the first time, highlighting the expanded host range for these pathogens. In addition to Chlamydiaceae, our research also included the screening of Australian avian taxa for other pathogens such as beak and feather disease virus (BFDV), avipoxviruses, columbid alphaherpesvirus 1 (CoAHV1), and psittacid alphaherpesvirus 1 (PsAHV1). Our studies unveiled the first detection of the exotic PsAHV1 (the causative agent of Pacheco’s disease) in wild Australian birds. Furthermore, we discovered numerous non-parrot species are asymptomatically infected with BFDV strains that cause acute mortality in parrots. These findings draw attention to the high pathogen diversity in wild Australian birds and highlight the potential spillover of these pathogens into critically endangered bird species. Further, to overcome the challenges associated with isolation and culture of Chlamydia, we employed culture-independent probe-based whole-genome sequencing to expand the global C. psittaci genome catalogue, providing the first genomes from New Zealand. This allowed us to generate novel C. psittaci genomes from several avian species, providing new insights into its global phylogenomic diversity and multi-host generalist capacity of C. psittaci. Moreover, combining multilocus sequence typing (MLST) and major outer membrane protein (ompA) genotyping on additional avian samples provided a cost-efficient method for exploring the genetic diversity among various C. psittaci strains across Australasia. Finally, our research delivers new insights into the genetic diversity of avian C. abortus strains, particularly those detected from wild Australian Torresian crows (Corvus orru). Probe-based capture WGS allowed us to identify novel strains of avian C. abortus directly from DNA extracted from clinical swabs, revealing these strains are genetically similar to avian C. abortus strains detected in Polish wildfowl and corvid species. Furthermore, these strains carry virulence-associated genes, including the large chlamydial cytotoxin (toxB) gene and a chlamydial plasmid, similar to those identified in zoonotic C. psittaci strains. These results suggest that avian C. abortus may be pathogenic and have zoonotic potential, further exemplified by these strains being genetic intermediates of two pathogens of veterinary significance (zoonotic C. psittaci and livestock C. abortus strains). In summary, our studies underscore the prevalence and diversity of avian-borne pathogens in Australia, their potential to spillover into novel host species, and the implications for biosecurity. Our research also demonstrates the effectiveness of probe-capture WGS in producing high-quality chlamydial genomes from clinical samples. These findings reiterate the need for ongoing surveillance and further characterisation of these emerging pathogens and for understanding their ecology, genetic identity, potential reservoirs, and factors influencing infection spillover to ensure effective future strategies for the protection of Australian wildlife, livestock, and human health.

Emerging Threats at the Intersection of Wildlife and Public Health: Investigating the Epidemiology of Chlamydia psittaci and Viral Coinfections in Australian Birds

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