Gene Loss and Lineage-Specific Restriction-Modification Systems Associated with Niche Differentiation in the Campylobacter jejuni Sequence Type 403 Clonal Complex

Abstract

g Campylobacter jejuni is a highly diverse species of bacteria commonly associated with infectious intestinal disease of humans and zoonotic carriage in poultry, cattle, pigs, and other animals. The species contains a large number of distinct clonal complexes that vary from host generalist lineages commonly found in poultry, livestock, and human disease cases to host-adapted specialized lineages primarily associated with livestock or poultry. Here, we present novel data on the ST403 clonal complex of C. jejuni, a lineage that has not been reported in avian hosts. Our data show that the lineage exhibits a distinctive pattern of intralineage recombination that is accompanied by the presence of lineage-specific restriction-modification systems. Furthermore, we show that the ST403 complex has undergone gene decay at a number of loci. Our data provide a putative link between the lack of association with avian hosts of C. jejuni ST403 and both gene gain and gene loss through nonsense mutations in coding sequences of genes, resulting in pseudogene formation. Campylobacter is a common component of the gut microbiota of many avian and mammalian species, where it is often considered a commensal organism, as it is typically carried without obvious disease symptoms. While diarrheal infections are rarely recorded in animals (1, 2), they are extremely common in humans, where the majority of infections are caused by Campylobacter jejuni (3). Human C. jejuni infection can originate in multiple reservoirs, but it is known that a large proportion of human C. jejuni cases are attributed to chickens (4), typically through handling of raw meat, cross contamination, or direct consumption of undercooked meat. However, this does not account for all cases of campylobacteriosis, and it is clear that isolates from other sources and species can infect humans.The ubiquity of Campylobacter poses interesting questions about its ecology and infection biology (5). C. jejuni and C. coli have been isolated from numerous avian and mammalian species, including food production animals, such as poultry, pigs, and cattle (6, 7), as well as in companion animals, including cats and dogs (2). Wild birds, fecally contaminated ground and surface waters, and drinking water are also reservoirs for C. coli and C. jejuni (8, 9). While both species are widely distributed, disease-causing C. coli is most commonly associated with food production mammals, especially pigs, but improving knowledge of the population structure and evolution of these organisms is challenging some of the traditional ideas. It is now clear that both C. jejuni and C. coli are frequently isolated from multiple species (10, 11), and understanding lineage distribution across multiple hosts is an important current objective in Campylobacter research.Multilocus sequence typing (MLST) has been performed on a large number of C. jejuni isolates from clinical samples, veterinary sources, abattoir surveys, and environmental sources (4,9,10,12). These studies have revealed the existence of host-rest...

Lineage‐specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group

“…As in recent publications on other species (Meric, Hitchings, Pascoe, & Sheppard, 2016;Monteil et al, 2016;Morley et al, 2015;Murray et al, 2017;Yahara et al, 2017), a reference pan-genome approach was used with gene-by-gene alignment, consistent with whole-genome MLST (Jolley & Maiden, 2010;Maiden et al, 2013;Meric et al, 2014;Sheppard, Jolley, & Maiden, 2012), implemented in BIGSdb open-source software. Briefly, the reference pan-genome was constructed by combining the genomes of several reference strains (Bt strain YBT020 (Zhu et al, 2011), Bc strain ATCC 14579 (Ivanova et al, 2003) and Ba strain Ames (Read et al, 2003)) with whole-genome annotations from all the other genomes of this study to derive a single gene list.…”

Whole-Genome Sequencing in Epidemiology of Campylobacter jejuni Infections

“…Although source attribution models using WGS data as input have yet to be applied to campylobacteriosis cases, phylogenic and population structure analyses of C. jejuni isolates collected from different studies have been used to trace the sources of sporadic cases, as described above (16). Furthermore, major efforts have been devoted to detecting and elucidating the mechanisms of host adaptation in C. jejuni with the use of WGS, especially identifying host-specific traits (29,30). The discovery of such loci gained or lost makes these genetic elements possible targets for source tracking; the genetic make-up of a human isolate could theoretically help determine the source of that isolate.…”

Campylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay

“…It is therefore likely that a progressive process of pseudogene formation is responsible for degradation of autotransporter genes in specific lineages rather than phase variation mediated by poly-G tracts. Pseudogenisation of autotransporters suggests a functional redundancy of these genes in certain lineages, leading to inactivation once their respective functions are no longer required within a specialised niche [45,46]. This "adaptive loss" scenario has been observed in C. jejuni previously and is a proposed consequence of niche differentiation [45].…”