Genomic diversity and recombination in Xylella fastidiosa

Authors: VANHOVE, MATHIEU - University Of California; RETCHLESS, ADAM - Centers For Disease Control And Prevention (CDC) - United States; SICARD, ANNE - University Of California; RIEUX, ADRIEN - Cirad-La Recherche Agronomique Pour Le Developpe; COLETTA-FILHO, HELVECIO - Centro De Citricultura; DE LA FUENTE, LEONARDO - Auburn University; Stenger, Drake; ALEMIDA, RODRIGO - University Of California

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/19/2019
Publication Date: 4/26/2019
Citation: Vanhove, M., Retchless, A., Sicard, A., Rieux, A., Coletta-Filho, H., De La Fuente, L., Stenger, D.C., Alemida, R. 2019. Genomic diversity and recombination in Xylella fastidiosa. Applied and Environmental Microbiology. 85:e02972-18. https://doi.org/10.1128/AEM.02972-18.
DOI: https://doi.org/10.1128/AEM.02972-18

Interpretive Summary: The bacterium Xylella fastidiosa is an emergent plant pathogen responsible for diseases in a wide range of high value horticultural crops, including grapevine, almond, olives, stone fruits, citrus, and coffee. Genome sequence analyses indicate X. fastidiosa exhibits genetic diversity, both within and among five subspecies, correlated with differences in host range. Here, genome sequences of 72 X. fastidiosa strains were compared to define degree of genetic diversity within each subspecies and to define the extent of homologous recombination among subspecies. The analyses permitted improved estimates of time of divergence among X. fastidiosa subspecies, revealed that different subspecies are under different selective pressures, and determined that homologous recombination events have occurred recently among subspecies after human caused introductions brought previously isolated subspecies into close proximity. Further, the analyses support the contention that subspecies of X. fastidiosa are host adapted and that genetic exchange among subspecies may lead to emergence of new strains with novel pathogenicity characteristics. These results further indicate continued vigilance is needed to prevent additional introduction events, even in regions where X. fastidiosa is already established and prevalent.

Technical Abstract: Xylella fastidiosa is an economically important bacterial plant pathogen. With insights gained from 72 genomes, this study investigated differences among the three main X. fastidiosa subspecies, which have allopatric origins: fastidiosa, multiplex, and pauca. The origin of recombinogenic subspecies morus and sandyi also was assessed. A tip-calibrated phylogenetic approach allowed estimation of the evolutionary rate of X. fastidiosa (7.6204x10-7 mutation per site per year), which was subsequently used to estimate time of divergence for the main subspecies and introduction events. Content of the core/soft-core genome varied among subspecies with subsp. pauca displaying the highest genetic diversity (73,906 SNPs, p = 1.29x10-2). The three subspecies were found to be under different selective pressures, and recombination was recognized as a major driver of diversity in X. fastidiosa (r/m = 2.259), potentially facilitating shifts to novel plant hosts. Evidence of recombination was uncovered in the core genome alignment; subsp. fastidiosa was less prone to recombination (0.49% of the core genome), whereas a specific clade of subsp. multiplex was found to have multiple recombining segments, originating primarily from subsp. fastidiosa (93.2%). Interestingly for subsp. morus, which was initially thought to be the outcome of genome-wide recombination between fastidiosa and multiplex, inter-subspecies heterogeneous recombination levels reached 14.90% in the core genome. Finally, time to the most common recent ancestor for subsp. pauca strains infecting Citrus sinensis and strains affecting Coffea arabica in Brazil was estimated to be 792 (CI: 389 BC - 1909), with evidence of citrus strains containing genetic elements acquired from strains infecting coffee plants. In summary, our data indicate that X. fastidiosa subspecies are under distinct selective pressures, which have shaped genomic diversity in each clade.