Metaphenotypes associated with recurrent genomic lineages of Campylobacter jejuni responsible for human infections in Luxembourg

Abstract

Campylobacter jejuni is a leading cause of foodborne illnesses worldwide. Although considered fragile, this microaerophilic bacterium is able to survive in various challenging environments, which subsequently constitutes multiple sources of transmission for human infection. To test the assumption of acquiring specific features for adaptation and survival, we established a workflow of phenotypic tests related to the survival and the persistence of recurrent and sporadic strains. A representative collection of 83 strains isolated over 13 years from human, mammal, poultry, and environmental sources in Luxembourg, representing different spreading patterns (endemic, epidemic, and sporadic), was screened for survival to oxidative stresses, for acclimating to aerobic conditions (AC), and for persistence on abiotic surfaces. Using the cgMLST Oxford typing scheme for WGS data, the collection was classified into genomic lineages corresponding to host-generalist strains (lineages A and D, CC ST-21), host-specific strains (lineage B, CC ST-257 and lineage C, CC ST-464) and sporadic strains. We established that when a strain survives concentrations beyond 0.25 mM superoxide stress, it is six times more likely to survive hyperoxide stress and that a highly adherent strain is 14 times more likely to develop a biofilm. Surprisingly, more than half of the strains could acclimate to AC but this capacity does not explain the difference between recurrent genomic lineages and sporadic strains and the survival to oxidative stresses, while recurrent strains have a significantly higher adhesion/biofilm formation capacity than sporadic ones. From this work, the genomic lineages with more stable genomes could be characterized by a specific combination of phenotypes, called metaphenotypes. From the functional genomic analyses, the presence of a potentially functional T6SS in the strains of lineage D might explain the propensity of these strains to be strong biofilm producers. Our findings support the hypothesis that phenotypical abilities contribute to the spatio-temporal adaptation and survival of stable genomic lineages. It suggests a selection of better-adapted and persistent strains in challenging stress environments, which could explain the prevalence of these lineages in human infections.

Observations supporting hypothetical commensalism and competition between two Campylobacter jejuni strains colonizing the broiler chicken gut

“…This increase in the optic density could also be due to an increased overall bacterial death of D2008b. Another hypothesis would be based on a different susceptibility of both strains to oxidative stress resulting from bacterial growth (Nennig et al, 2022). Moreover, both strains might not be able to use the same nutrients as the culture media is becoming depleted, therefore giving an advantage to one strain over the other.…”

Environmental dynamics of Campylobacter jejuni genotypes circulating in Luxembourg: what is the role of wild birds?

“…Nevertheless, one isolate from birds corresponds to an endemic lineage that has been occurring in human infections for the past 15 years in Luxembourg and more generally in Europe [4]. This lineage is characterized by acclimation to aerobic conditions [41]. Even though Campylobacter is generally believed to survive poorly outside the animal host [42], this acclimatation capacity to aerobic environments might improve the environmental survival of this lineage.…”

“…Our research has illustrated that some persistent genotypes are multi-host, overlapping human, wild birds and livestock. As previously noted, these recurring genotypes have higher adhesion/ biofilm formation capacity than sporadic genotypes, contributing to the survival and spread of these stable genomic lineage [41]. The monitoring of C. jejuni genotypes in different environments and a better understanding of the contamination cycle can not only shed light on the epidemiology of campylobacteriosis in Luxembourg but also on diffuse outbreaks of this high-priority foodborne pathogen around the world.…”

“…The concordance of the typing systems in classifying these strains corroborated the spread of these lineages in these different hosts and in humans (Table S4). Several genotypes, potentially with specific metaphenotypes [41], could be multi-host and present in different environments/reservoirs/vectors (Fig. 4).…”

Genomic insights into zoonotic transmission and antimicrobial resistance in Campylobacter jejuni from farm to fork: a one health perspective

“…Among the resistance mechanisms to environmental stressors are the transformation into a viable non culturable state (VBNC), biofilm formation, and mutations specific to certain lineages [ 33 , 34 ]. Some of the host-generalist and host-specific strains of C. jejuni were proved to survive in aerobic conditions and under oxidative stress [ 35 ].…”