Evidence of land‐sea transfer of the zoonotic pathogen Campylobacter to a wildlife marine sentinel species

Abstract

Environmental pollution often accompanies the expansion and urbanisation of human populations where sewage and wastewaters commonly have an impact on the marine environments. Here we explored the potential for faecal bacterial pathogens, of anthropic origin, to spread to marine wildlife in coastal areas. The common zoonotic bacterium Campylobacter was isolated from grey seals (Halichoerus grypus), an important sentinel species for environmental pollution, and compared to isolates from wild birds, agricultural sources and clinical samples to characterize possible transmission routes. Campylobacter jejuni was present in half of all grey seal pups sampled (24/50 dead and 46/90 live pups) in the breeding colony on the Isle of May (Scotland), where it was frequently associated with histological evidence of disease. Returning yearling animals (19/19) were negative for C. jejuni suggesting clearance of infection whilst away from the localised colony infection source. The genomes of 90 isolates from seals were sequenced and characterized using a whole-genome multilocus sequence typing (MLST) approach, and compared to 192 published genomes from multiple sources using population genetic approaches and a probabilistic genetic attribution model to infer the source of infection from MLST data. The strong genotype-host association has enabled the application of source attribution models in epidemiological studies of human campylobacteriosis, and here assignment analyses consistently grouped seal isolates with those from human clinical samples. These findings are consistent with either a common infection source or direct transmission of human campylobacter to grey seals, raising concerns about the spread of human pathogens to wildlife marine sentinel species in coastal areas.

Global Epidemiology of Campylobacter Infection

“…As expected, Campylobacter infections are mainly attributed to poultry products by using these techniques (303,304). More recently, however, molecular techniques, such as multilocus sequence typing, porA/flaA typing, and gyrase subunit A typing, have played a more significant role in source attribution (305)(306)(307)(308)(309)(310), allowing further insights into the contributions of the different reservoirs to the burden of campylobacteriosis in humans and the subsequent transfer of Campylobacter species to wildlife through environmental contamination.…”

The Kraken in the Aquarium: Questions that Urgently Need to be Addressed in Order to Advance Marine Conservation

“…From acidification (Harvey et al, 2013;Gaylord et al, 2015) to zoonotic pathogens (Baily et al, 2015), the integrity and resilience of marine ecosystems are being threatened (Duarte, 1995;Neubauer et al, 2013). People who rely on the oceans for ecosystem services such as carbon sequestration, food, and cultural security are also being affected ( Millennium Ecosystem Assessment, 2005;Worm et al, 2009).…”

Investigation of a mouse and a sheep model to study pathogenic mechanisms of Campylobacter jejuni fetoplacental infection

“…IL6 is a pro-inflammatory cytokine with roles in Th 2 responses and antibody production. 9 While IL6 can be found within the reproductive tract, 33 it did not appear to have a major role in the pathology of abortifacient C. jejuni IA3902 in BALB/c and CD-1 mice used in this study. This is in contrast to other work, which suggested roles for IL6 in the immunity and pathogenesis of Campylobacter; specifically that it enhanced local enteric and systemic antibodies to C. jejuni.…”

“…Anthropic transfer of C. jejuni to sentinel marine wildlife species, namely, grey seal pups with histologic evidence of disease underscores the inherently complicated environmental, microbial and host relationships that exist with this pathogen. 9 The fact that the same organism can cause disease in different systems in different hosts definitely adds more complexity to the mix. The tetracycline resistant C. jejuni capable of causing abortion in sheep is genetically identical to isolates from human cases of gastroenteritis.…”

“…Mice have a hemochorial placenta similar to humans, a short gestation period, defined genetics and their immune system has been well characterized and is similar to that of humans. 10 The mouse model has proven useful for the study of the pathogenesis of reproductive disease due to Chlamydophila abortus and vaccine related investigations 9 and a pregnant mouse model has been characterized for the study of bovine Tritrichomonas fetus infection. 1 Murine models have been established for human reproductive research as a mouse model for preeclampsia has been described.…”