The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae

Abstract : The Xanthomonadaceae includes two xylem-limited plant pathogenic bacteria, Xanthomonas albilineans and Xylella fastidiosa. The complete genome of X. albilineans was sequenced, providing not only strong clues to identify new pathogenicity factors in this pathogen causing sugarcane leaf scald disease, but also new insights into the evolution of Xanthomonadaceae. Previous phylogenetic analysis suggested that the Xanthomonas and Stenotrophomonas genera of Xanthomonadaceae form a coherent group excluding X. fastidiosa. Surprisingly, phylogenetic analysis using X. albilineans genomic sequences resulted in a different tree in which X. fastidiosa belongs to the Xanthomonas group. Based on this latter tree, X. albilineans and X. fastidiosa are derived from the progenitor of the Xanthomonas genus which itself is derived from the progenitor of Stenotrophomonas. Comparative genomic analysis identified 551 ancestral genes which are present in both Xanthomonas axonopodis pv. vesicatoria and Stenotrophomonas but absent in both X. fastidiosa and X. albilineans, revealing that these two latter species experienced a similar reductive genome evolution during their descent from the progenitor of the Xanthomonas genus. This degenerative evolution is probably driven by adaptation to the nutrient-poor xylem elements and to the cloistered environmental niche of xylem vessels. Comparable genomic erosion is observed among intracellular animal bacteria and is associated with a mutualistic life style. Adaptation of X. albilineans and X. fastidiosa to a xylem-limited life style is also illustrated by the unique characteristics of the enzymes involved in cellulose degradation, and the absence of a type III secretion system of the Hrp1 and Hrp2 injectisome families.