Deep phylo-taxono genomics reveals Xylella as a variant lineage of plant associated Xanthomonas with Stenotrophomonas and Pseudoxanthomonas as misclassified relatives

Abstract

AbstractGenus Xanthomonas is a group of phytopathogens which is phylogenetically related to Xylella, Stenotrophomonas and Pseudoxanthomonas following diverse lifestyles. Xylella is a lethal plant pathogen with highly reduced genome, atypical GC content and is taxonomically related to these three genera. Deep phylo-taxono-genomics reveals that Xylella is a variant Xanthomonas lineage that is sandwiched between Xanthomonas species. Comparative studies suggest the role of unique pigment and exopolysaccharide gene clusters in the emergence of Xanthomonas and Xylella clades. Pan genome analysis identified set of unique genes associated with sub-lineages representing plant associated Xanthomonas clade and nosocomial origin Stenotrophomonas. Overall, our study reveals importance to reconcile classical phenotypic data and genomic findings in reconstituting taxonomic status of these four genera.Significance StatementXylella fastidiosa is a devastating pathogen of perennial dicots such as grapes, citrus, coffee, and olives. The pathogen is transmitted by an insect vector to its specific host wherein the infection leads to complete wilting of the plants. The genome of X. fastidiosa is extremely reduced both in terms of size (2Mb) and GC content (50%) when compared with its relatives such as Xanthomonas, Stenotrophomonas, and Pseudoxanthomonas that have higher GC content (65%) and larger genomes (5Mb). In this study, using systematic and in-depth genome-based taxonomic and phylogenetic criteria along with comparative studies, we assert the need of unification of Xanthomonas with its misclassified relatives (Xylella, Stenotrophomonas and Pseudoxanthomonas). Interestingly, Xylella revealed itself as a minor lineage embedded within two major Xanthomonas lineages comprising member species of different hosts.