|TAN, YONGJUN - St Louis University
|WANG, CINDY - St Louis University
|SCHNEIDER, THERESA - St Louis University
|LI, HUAN - St Louis University
|DE SOUZA, ROBSON FRANCISC - University Of São Paulo
|TANG, XUEMING - Shanghai Jiaotong University
|Swisher Grimm, Kylie
|HSIEH, TZUNG-FU - North Carolina State University
|WANG, XU - Auburn University
|LI, XU - North Carolina State University
|ZHANG, DAPENG - St Louis University
Submitted to: Microbiology Spectrum
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/9/2021
Publication Date: 9/15/2021
Citation: Tan, Y., Wang, C., Schneider, T., Li, H., de Souza, R., Tang, X., Swisher Grimm, K.D., Hsieh, T., Wang, X., Li, X., Zhang, D. 2021. Comparative phylogenomic analysis reveals evolutionary genomic changes and novel toxin families in endophytic Liberibacter pathogens. Microbiology Spectrum. 9(2). Article e00509-21. https://doi.org/10.1128/Spectrum.00509-21.
Interpretive Summary: Liberibacter pathogens cause diseases to important crops including citrus Huanglongbing and potato Zebra Chip. To gain a better understanding of the biology and pathogenesis of Liberibacter bacteria, we performed an in-depth comparative analysis on twelve Liberibacter genomes. Using genome comparison, gene neighborhood analysis, ortholog clustering, and phylogenetic inference, we identified major genomic changes, including prophage loci diversity and gene-loss/gene-gain events, that are associated with the evolutionary transition of Liberibacter from the free-living nonpathogenic ancestral species to endophytic pathogens. Consistent with the habitat change, the lost genes were enriched for biosynthesis of cellular building blocks such as amino acids. Importantly, among the gained genes, we uncovered several previously unrecognized toxins, including a new type of polymorphic toxins, a YdjM phospholipase toxin, and a secreted EEP protein. These discoveries suggest a promising new direction for experimental approaches toward elucidating the mechanism of Liberibacter pathogenesis and finding cure for the devastating Huanglongbing disease.
Technical Abstract: Liberibacter pathogens cause economically devastating diseases in Rutaceae (citrus), Solanaceae (potato and tomato), and Apiaceae (carrots and celery) crops around the world. In collaboration with researchers at Saint Louis University, North Carolina University, Auburn University, Universidade de São Paulo, and Shanghai Jiao Tong University, researchers at the USDA-ARS assessed genomic differences between pathogenic and non-pathogenic species of Liberibacter to help elucidate mechanisms of pathogenesis that may enable future development of treatments for infected crops. Prophage regions and gene-loss or gene-gain events were identified in association with the evolutionary transition of Liberibacter from the non-pathogenic species to the pathogenic species. Genes gained in the pathogenic Liberibacter species included some previously unrecognized toxins, while those lost in the pathogenic, endophytic species included genes involved in synthesis and metabolism of cellular components. Liberibacters have caused millions of dollars in losses to major crops world-wide and identification of genomic factors that may be responsible for pathogenesis will help in our efforts to combat the various diseases.