Abstract

Xanthomonas albilineans is the bacterium responsible for leaf scald, a lethal disease of sugarcane. Within the Xanthomonas genus, X. albilineans exhibits distinctive genomic characteristics including the presence of significant genome erosion, a non-ribosomal peptide synthesis (NRPS) locus involved in albicidin biosynthesis, and a type 3 secretion system (T3SS) of the Salmonella pathogenicity island-1 (SPI-1) family. We sequenced two X. albilineans-like strains isolated from unusual environments, i.e., from dew droplets on sugarcane leaves and from the wild grass Paspalum dilatatum, and compared these genomes sequences with those of two strains of X. albilineans and three of Xanthomonas sacchari. Average nucleotide identity (ANI) and multi-locus sequence analysis (MLSA) showed that both X. albilineans-like strains belong to a new species close to X. albilineans that we have named “Xanthomonas pseudalbilineans”. X. albilineans and “X. pseudalbilineans” share many genomic features including (i) the lack of genes encoding a hypersensitive response and pathogenicity type 3 secretion system (Hrp-T3SS), and (ii) genome erosion that probably occurred in a common progenitor of both species. Our comparative analyses also revealed specific genomic features that may help X. albilineans interact with sugarcane, e.g., a PglA endoglucanase, three TonB-dependent transporters and a glycogen metabolism gene cluster. Other specific genomic features found in the “X. pseudalbilineans” genome may contribute to its fitness and specific ecological niche.

Highlights

  • Leaf scald disease of sugarcane (Saccharum spp.) is caused by Xanthomonas albilineans (Ashby)Dowson—a xylem-invading pathogen

  • Between X. albilineans strains and MUS 060 or GPE 39 strains, and 98.6% when comparing X. albilineans strains to X. sacchari strains (Supplementary File S1)

  • Most taxonomists consider that a 16S rRNA gene nucleotide sequence identity below 97% means that the compared sequences belong to different species; the meaning of identity greater than 97% remains unclear, partly due to the variable evolutionary histories of bacterial species [29,30]

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Summary

Introduction

Leaf scald disease of sugarcane (Saccharum spp.) is caused by Xanthomonas albilineans (Ashby). Serotyping of 215 strains from 28 worldwide locations affected by sugarcane leaf scald disease distributed strains into three groups according to serotype: (i) serotype 1 represents the largest group, with strains from various geographic locations; (ii) serotype 2 consists of strains from tropical African countries; and (iii) serotype 3 contains strains from Caribbean islands (Guadeloupe, Martinique, Saint-Kitts) as well as from Asia (Sri Lanka) and Oceania (Fiji) [14,15] This serological characterization of X. albilineans strains has been corroborated using a combination of monoclonal antibodies on 38 strains from different locations worldwide [16]. The comparative phylogenetic and genomic analyses described in the present study refines the taxonomic classification of strains MUS 060 and GPE 39 and provides additional data that shed light on the evolutionary history of the sugarcane pathogen X. albilineans

Taxonomic Characterization of MUS 060 and GPE 39 Isolates
Orthology Analysis
Serotypes and Variability of LPS Loci
The Albicidin Locus and other NRPS Loci
Variability of the Locus Encoding the Type IV Pilus
CRISPR and Restriction-Modification System Loci
2.10. Genome Erosion
Bacterial Strains and DNA Preparation
DNA Sequencing and Assembly
Genotyping with 16S–23S rRNA ITS and 16S rRNA Gene Sequence
Phylogenetic Core Genome Analysis
Whole-Genome Sequences Analyses
OrthoMCL Analyses
Conclusions
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