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 world-wide pathogen distribution.

Keywords: Genetic diversity; Inter-subspecific recombination; Pan genome; WGS; Xylella fastidiosa.

Fig. 1

Number of shared genes among Xylella fastidiosa isolates. a. ML phylogenetic tree shows the relationship between isolates X. fastidiosa subsp. fastidiosa (blue) and subsp. pauca (yellow) from Costa Rica plants. Isolates names are colored based in the plant in which they were isolated: Vinca spp. (purple), Psidium spp. (red), Coffea spp. (brown), and Nerium oleander (orange); b. A cladogram shows the core genome (up) and the number of unique at each node of the phylogeny (down, bolded). Numbers next to isolate name indicate number of genes in the genome

Fig. 2

Recent recombination of two X. fastidiosa subspecies in Costa Rica. Colors indicate phylogenetically distinct X. fastidiosa lineages: X. fastidiosa subsp. pauca (red), X. fastidiosa subsp. fastidiosa (group 1, blue), and X. fastidiosa subsp. fastidiosa (group 2, green). a. Circular plot of strain-specific recombination events. Each line represents a recombinant event, with the width and placement of the line indicating recombinant segment size and its alignment position, respectively; b. FastGEAR recombination plot showing donor/recipient sequences and the position of the recombinant event in the alignment; c. Heatmap showing the number of donor/recipient interactions among strains

Fig. 3

Brazil and Costa Rica lineage- and strain-specific recombination circular plots. Orange box includes isolates representing the two monophyletic clades/subspecies found within Costa Rica: X. fastidiosa subsp. fastidiosa (Psidium spp., Vinca spp. and Coffea spp.) and X. fastidiosa subsp. pauca (Nerium oleander and Coffea spp.). Green box includes isolates representing the phylogenetic diversity of X. fastidiosa subsp. pauca found in Brazil: the monophyletic citrus clade, the paraphyletic coffee clade, and the individual Hibiscus spp. and Prunus domestica isolates. Colors indicate isolates obtained from different host plant species. Costa Rica: Psidium spp. (red), Vinca spp. (purple), Coffea spp. (brown), Nerium oleander (orange). Brazil: Coffea spp. (brown), Citrus spp. (pale orange), Hibiscus spp. (pale pink), and Prunus domestica (dark pink). Circular plot shows recombination between strains and recombination between lineages. Each line represents a recombinant event, with the width and placement of the line indicating recombinant segment size and alignment position

Fig. 4

ML tree showing the relationship between worldwide X. fastidiosa subsp. fastidiosa and subsp. pauca isolates. a. Distribution map of X. fastidiosa subsp. fastidiosa (blue) and subsp. pauca (yellow) populations. Regions where both species coexist are marked in green. Arrows indicate source and destination populations for each introduction. Map was downloaded from Wikimedia Commons (https://commons.wikimedia.org/wiki/Maps_of_the_world#/media/File:Simplified_blank_world_map_without_Antartica_(no_borders).svg). b. ML tree shows the relationship of worldwide X. fastidiosa subsp. fastidiosa and subsp. pauca populations. Bootstrap values show support for each tree node