Impacts of local population history and ecology on the evolution of a globally dispersed pathogen

Abstract

Background: Pathogens with a global distribution face diverse biotic and abiotic conditions across populations. Moreover, the ecological and evolutionary history of each population is unique. Xylella fastidiosa is a xylem-dwelling bacterium infecting multiple plant hosts, often with detrimental effects. As a group, X. fastidiosa is divided into distinct subspecies with allopatric historical distributions and patterns of multiple introductions from numerous source populations. The capacity of X. fastidiosa to successfully colonize and cause disease in naïve plant hosts varies among subspecies, and potentially, among populations. Within Central America (i.e. Costa Rica) two X. fastidiosa subspecies coexist: the native subsp. fastidiosa and the introduced subsp. pauca. Using whole genome sequences, the patterns of gene gain/loss, genomic introgression, and genetic diversity were characterized within Costa Rica and contrasted to other X. fastidiosa populations. Results: Within Costa Rica, accessory and core genome analyses showed a highly malleable genome with numerous intra-and inter-subspecific gain/loss events. Likewise, variable levels of inter-subspecific introgression were found within and between both coexisting subspecies; nonetheless, the direction of donor/recipient subspecies to the recombinant segments varied. Some strains appeared to recombine more frequently than others; however, no group of genes or gene functions were overrepresented within recombinant segments. Finally, the patterns of genetic diversity of subsp. fastidiosa in Costa Rica were consistent with those of other native populations (i.e. subsp. pauca in Brazil). Conclusions: Overall, this study shows the importance of characterizing local evolutionary and ecological history in the context of worldwide pathogen distribution.

Genetic differentiation of Xylella fastidiosa following the introduction into Taiwan

“…pauca and subsp. fastidiosa have lower genetic diversity than native ones (Castillo et al 2020). Yet, with time, nucleotide differences accumulate as a product of ecological and environmentally mediated pressures as well as the result of non-adaptive evolution (Castillo et al 2021).…”

“…fastidiosa strains (N = 206). Three Costa Rican isolates (non-grapevine infecting) were used as an outgroup (Castillo et al 2020). The core genome alignment was used to build a Maximum Likelihood (ML) tree with RAxML (Stamatakis 2014).…”

“…The bacterium X. fastidiosa is taxonomically divided into three main monophyletic subspecies with allopatric origins: X. fastidiosa subsp. fastidiosa , native to Central America (Castillo et al 2020; Nunney et al 2019; Vanhove et al 2020); X. fastidiosa subsp. multiplex , native to temperate and subtropical North America (Nunney et al 2012, 2014); and X. fastidiosa subsp.…”

Bacterial Vector-Borne Plant Diseases: Unanswered Questions and Future Directions

“…Because X. fastidiosa studies have focused on diseased crops, we do not understand what diversity may exist within X. taiwanensis or X. fastidiosa in natural ecosystems or whether there are other species of Xylella ( Almeida and Nunney, 2015 ). It is unreasonable to assume that the only Xylella not considered to be endemic to the Americas is found in an island in Asia; even within the Americas, there is evidence of unsampled clades of X. fastidiosa ( Castillo et al, 2020 ). Similarly, in the Americas, and more recently in Europe, the vast majority of X. fastidiosa for which there are genetic data are linked to crops of economic importance.…”

Orthology-Based Estimate of the Contribution of Horizontal Gene Transfer from Distantly Related Bacteria to the Intraspecific Diversity and Differentiation of Xylella fastidiosa

“…Despite the occurrence of recombination events between strains, Xylella fastidiosa shows a low ratio of recombination to point mutation on a per housekeeping gene basis when compared to other bacterial species [ 12 ]. Genome-wide approaches also revealed recombination events among strains, so that ancestral and more recent recombination was detected for all subspecies, with some strains showing a high recombination rate [ 16 , 17 ]⁠.…”