Recombination‐prone bacterial strains form a reservoir from which epidemic clones emerge in agroecosystems

Abstract

The acquisition of virulence-related genes through horizontal gene transfer can modify the pathogenic profiles of strains and lead to the emergence of new diseases. Xanthomonas arboricola is a bacterial species largely known for the damage it causes to stone and nut fruit trees worldwide. In addition to these host-specific populations called pathovars, many nonpathogenic strains have been identified in this species. Their evolutionary significance in the context of pathogen emergence is unknown. We looked at seven housekeeping genes amplified from 187 pathogenic and nonpathogenic strains isolated from various plants worldwide to analyze population genetics and recombination dynamics. We also examined the dynamics of the gains and losses of genes associated with life history traits (LHTs) during X. arboricola evolution. We discovered that X. arboricola presents an epidemic population structure. Successful pathovars of trees (i.e. pruni, corylina and juglandis) are epidemic clones whose emergence appears to be linked to the acquisition of eight genes coding for Type III effectors. The other strains of this species are part of a recombinant network, within which LHT-associated genes might have been lost. We suggest that nonpathogenic strains, because of their high genetic diversity and propensity for recombination, may promote the emergence of pathogenic strains.

Using Ecology, Physiology, and Genomics to Understand Host Specificity inXanthomonas

“…Heterogeneous populations of yellow-pigmented nonpathogenic strains from different plants and identified as Xanthomonas by various serological, protein profile, or sequence-based methods could not be assigned to existing pathovars, including those grouping strains from the same host species (42,95,131,133). These strains do not cluster with the pathogenic strains of the host from which they were isolated.…”

“…These strains do not cluster with the pathogenic strains of the host from which they were isolated. Interestingly, it was noticed that most of these strains belong to the Xanthomonas arboricola species (95). Some represent new separate lineages in known species (42,47) and others form new clades such as the Xanthomonas maliensis species proposed to group the nonpathogenic strains isolated from disinfected rice leaves (131).…”

“…The acquisition of a T3SS and core T3Es as a second step could lead to the emergence of generalist pathogenic strains (70,97). The extensive acquisition of novel T3Es and subsequent shaping of T3E repertoires through HGT events was hypothesized to account for specialization of strains on specific hosts (70,95,97). On top of HGT, selection of advantageous alleles seems to contribute to host adaptation (153).…”

Genotyping and epidemiological metadata provides new insights into population structure of Xanthomonas isolated from walnut trees

“…Interestingly, some Xaj lineages appeared strongly associated, as in the case of Lin1 frequently isolated with Lin12, and Lin6 recovered simultaneously with Lin11 in all leaf samples. Although, further investigations are important to determine if the xanthomonads diversity within the same walnut host plant and even within the same plant organ, is a mix of bacterial populations colonizing evenly the same host plant and organ, or if it results from the co-colonization of dominant versus lessened xanthomonads populations, it was recently proposed that sympatric populations, as pathogenic and nonpathogenic strains found together on walnut buds, may have important effects on genetic dynamics of new strains emergence (16, 20).…”

“…Genotyping studies have found a considerable genetic diversity in Xaj , which is reportedly high when compared with the diversity described for other X. arboricola pathovars (5, 11-14). This feature, together with evidence of genomic trade-offs within the species (5, 13, 15, 16), evokes an opportunistic pathogen, even though evidence for environmental reservoirs of Xaj remains poorly characterized (11, 17-19). These data are further supported by the isolation of nonpathogenic strains of X. arboricola , described as phylogenetically heterogeneous, and grouping separately from the well-defined clusters of pathogenic Xaj strains (20).…”