Deep Population Genomics Reveals Systematic and Parallel Evolution at a Lipopolysaccharide Biosynthetic Locus in Xanthomonas Pathogens That Infect Rice and Sugarcane.

The advent of high-throughput sequencing and population genomics has enabled researchers to investigate selection pressure at hypervariable genomic loci encoding pathogen-associated molecular pattern (PAMP) molecules like lipopolysaccharide (LPS). Xanthomonas is a model and a major group of phytopathogenic bacteria that infect hosts in tissue-specific manner. Our in-depth population-based genomic investigation revealed the emergence of major lineages in two Xanthomonas pathogens that infect xylem of rice and sugarcane is associated with the acquisition and later large-scale replacement by distinct type of LPS cassettes. In the population of the rice xylem pathogen, Xanthomonas oryzae pv. oryzae (Xoo) and sugarcane pathogens Xanthomonas sacchari (Xsac) and Xanthomonas vasicola (Xvv), the BXO8 type of LPS cassette is replaced by a BXO1 type of cassette in Xoo and by Xvv type LPS cassette in Xsac and Xvv. These findings suggest a wave of parallel evolution at an LPS locus mediated by horizontal gene transfer (HGT) events during its adaptation and emergence. Aside from xylem pathogens, two closely related lineages of Xoo that infect parenchyma of rice and Leersia hexandra grass have acquired an LPS cassette from Xanthomonas pathogens that infect parenchyma of citrus, walnut, and strawberries, indicating yet another instance of parallel evolution mediated by HGT at an LPS locus. Our targeted and megapopulation-based genome dynamic studies revealed the acquisition and dominance of specific types of LPS cassettes in adaptation and success of a major group of phytopathogenic bacteria. IMPORTANCE Lipopolysaccharide (LPS) is a major microbe associated molecular pattern and hence a major immunomodulator. As a major and outer member component, it is expected that LPS is a frontline defense mechanism to deal with different host responses. Limited studies have indicated that LPS loci are also highly variable at strain and species level in plant-pathogenic bacteria, suggesting strong selection pressure from plants and associated niches. The advent of high-throughput genomics has led to the availability of a large set of genomic resources at taxonomic and population levels. This provides an exciting and important opportunity to carryout megascale targeted and population-based comparative genomic/association studies at important loci like those encoding LPS biosynthesis to understand their role in the evolution of the host, tissue specificity, and also predominant lineages. Such studies will also fill major gap in understanding host and tissue specificity in pathogenic bacteria. Our pioneering study uses the Xanthomonas group of phytopathogens that are known for their characteristic host and tissue specificity. The present deep phylogenomics of diverse Xanthomonas species and its members revealed lineage association and dominance of distinct types of LPS in accordance with their origin, host, tissue specificity, and evolutionary success.