Comparative genomics of Xylella fastidiosa suggests determinants of host-specificity and expands its mobile genetic elements repertoire

Abstract

The Gram-negative bacterium Xylella fastidiosa colonizes plant xylem vessels and is obligately vectored by xylem sap-feeding hemipteran insects. X. fastidiosa causes diseases in many plant species but in a variety of its plant hosts this bacterium behaves as a commensal endophyte. Originally confined to the Americas, infecting mainly grapevine, citrus and coffee plants, X. fastidiosa has spread to several plant species in Europe, causing devastating crop diseases. Although many pathogenicity and virulence factors have been identified in X. fastidiosa which enable the bacterium to successfully establish in the xylem tissue, the mechanisms by which distinct X. fastidiosa strains colonize and cause disease in specific plant hosts have not been fully elucidated. Here we present comparative analyses of 94 publicly available whole-genome sequences of X. fastidiosa strains with the goal of providing insights into plant host specificity determinants for this phytopathogen as well as of expanding the knowledge of its mobile genetic elements (MGE) content, mainly prophages. Our results revealed a pangenome of 4,549 protein coding sequences (CDSs) which is still open. The core- and accessory genomes comprise 954 and 2,219 CDSs, respectively. Phylogenetic tree construction using all core genome CDSs grouped the strains in three major clades of subspecies fastidiosa, multiplex and pauca, with subclades related to the strains sequence type (ST) obtained from multi-locus sequence typing (MLST). The geographic region where the strains were collected showed stronger association with the clades of X. fastidiosa strains rather than the plant species from which they were isolated. Among the CDSs related to virulence and pathogenicity found in the core genome, those related to lipopolysaccharide (LPS) synthesis and trimeric autotransporter adhesins (TAA) are somewhat related with the plant host of a given strain according to phylogenetic inference. The X. fastidiosa accessory genome is represented by an abundant and heterogeneous mobilome, which includes a diversity of prophage regions. In summary, the genome comparisons reported here will enable a better understanding of the diversity of phylogenetically close genomes and warrant further investigation of LPS and TAAs as potential X. fastidiosa host-specificity determinants.

Using genomes and evolutionary analyses to screen for host-specificity and positive selection in the plant pathogen Xylella fastidiosa

“…After building a phylogeny, they tested coevolutionary relationships between host species and X. fastidiosa MLST types but found no significant evidence of coevolution, implying a lack of host specialization. This topic was recently revisited with full genome data (26,27), but the results were inconsistent between studies. Uceda-Campos et al ( 2022) found no evidence that plant host species clustered on their X. fastidiosa phylogeny, but the samples did cluster by geography.…”

“…For example, two recent papers have used phylogenies to explore the question of host specificity. In one, Uceda-Campos et al (2022) found that X. fastidiosa isolates grouped on the phylogeny by geography, but not by plant host species, suggesting host specificity is not correlated with phylogenetic relationships and genetic divergence (26). In contrast, Kahn and Almeida (2022) used the phylogeny to infer the ancestral character states of plant hosts and found that the ancestral host plant could be inferred for most ancestral nodes (27).…”