Campylobacter jejuni colonization and population structure in urban populations of ducks and starlings in New Zealand

Abstract

A repeated cross-sectional study was conducted to determine the prevalence of Campylobacter spp. and the population structure of C. jejuni in European starlings and ducks cohabiting multiple public access sites in an urban area of New Zealand. The country's geographical isolation and relatively recent history of introduction of wild bird species, including the European starling and mallard duck, create an ideal setting to explore the impact of geographical separation on the population biology of C. jejuni, as well as potential public health implications. A total of 716 starling and 720 duck fecal samples were collected and screened for C. jejuni over a 12 month period. This study combined molecular genotyping, population genetics and epidemiological modeling and revealed: (i) higher Campylobacter spp. isolation in starlings (46%) compared with ducks (30%), but similar isolation of C. jejuni in ducks (23%) and starlings (21%), (ii) significant associations between the isolation of Campylobacter spp. and host species, sampling location and time of year using logistic regression, (iii) evidence of population differentiation, as indicated by FST, and host-genotype association with clonal complexes CC ST-177 and CC ST-682 associated with starlings, and clonal complexes CC ST-1034, CC ST-692, and CC ST-1332 associated with ducks, and (iv) greater genetic diversity and genotype richness in ducks compared with starlings. These findings provide evidence that host-associated genotypes, such as the starling-associated ST-177 and ST-682, represent lineages that were introduced with the host species in the 19th century. The isolation of sequence types associated with human disease in New Zealand indicate that wild ducks and starlings need to be considered as a potential public health risk, particularly in urban areas.We applied molecular epidemiology and population genetics to obtain insights in to the population structure, host-species relationships, gene flow and evolution of Campylobacter jejuni in urban ducks and starlings.

Population Genetics and Characterization of Campylobacter jejuni Isolates from Western Jackdaws and Game Birds in Finland

“…In addition to western jackdaws, 76% (n ϭ 108) of the mallard ducks carried C. jejuni. An earlier study from New Zealand reported that 23% (n ϭ 702) of wild mallard ducks were positive for C. jejuni (5), and in a study from the United Kingdom, high frequencies (93.3 to 100%) of farmed mallard ducks carried Campylobacter, emphasizing their role as a risk for human health (22). The relatively high frequency and diversity of C. jejuni among mallard ducks in this study may at least partly be a consequence of mixing with natural C. jejuni populations from other waterfowl, since the farmed mallard ducks were raised in natural ponds, which were cohabited by wild birds.…”

“…MLST is, however, limited to the characterization and discrimination of isolates according to sequence type (ST) (11)(12)(13); thus, more accurate methods, such as whole-genome MLST (wgMLST), are increasingly being used (11,14) to compare genetically related isolates in more detail and to be able to identify clones potentially originating from the same source. In previous studies, most of the STs found among wild birds, including mallard ducks (5), barnacle geese (7), starlings (15), and several other bird species (16), have been considered to represent mainly hostassociated STs, differing from those STs reported in human patients or domestic animals. Thus, wild birds are commonly considered to have a minor role in human campylobacteriosis.…”

Local genes for local bacteria: Evidence of allopatry in the genomes of transatlantic Campylobacter populations

“…In simple attribution models using MLST data, C. jejuni and C. coli isolates from chickens in the Netherlands, Senegal and the United States have been more closely related to UK chicken isolate populations rather than to populations from other host species in the same country (Sheppard, Colles et al., ). While genomic signatures of host association can transcend geographical structuring within C. jejuni and C. coli populations, there can be differences in the genotypes that are isolated from different countries (Asakura et al., ; Islam et al., ; Kivisto et al., ; Mohan et al., ; Prachantasena et al., ). This presents challenges, not only for attributing the source of infections among travellers returning from foreign locations (Mughini‐Gras et al., ), but also for understanding disease epidemiology in the context of a global food industry.…”

Local genes for local bacteria: evidence of allopatry in the genomes of transatlantic Campylobacter populations

“…In simple attribution models using MLST data, C. jejuni and C. coli isolates from chickens in the Netherlands, Senegal and the United States have been more closely related to UK chicken isolate populations rather than to populations from other host species in the same country (Sheppard et al, 2010a). While genomic signatures of host association can transcend geographical structuring within C. jejuni and C. coli populations, there can be differences in the genotypes that are isolated from different countries (Mohan et al, 2013, Asakura et al, 2012, Kivisto et al, 2014, Islam et al, 2014, Prachantasena et al, 2016 As recombination introduces more nucleotide substitutions than during mutation in C. jejuni and C. coli (Webb and Blaser, 2002, Morelli et al, 2010, genes with evidence of elevated recombination rates, which share a gene pool, will more rapidly acquire local signals of sequence variation than genes with lower recombination rates. These genes represent potential targets for use as biogeographical epidemiological markers.…”