Variation suggestive of horizontal gene transfer at a lipopolysaccharide (lps) biosynthetic locus in Xanthomonas oryzae pv. oryzae, the bacterial leaf blight pathogen of rice

BMC Microbiol. 2004 Oct 9:4:40. doi: 10.1186/1471-2180-4-40.

Abstract

Background: In animal pathogenic bacteria, horizontal gene transfer events (HGT) have been frequently observed in genomic regions that encode functions involved in biosynthesis of the outer membrane located lipopolysaccharide (LPS). As a result, different strains of the same pathogen can have substantially different lps biosynthetic gene clusters. Since LPS is highly antigenic, the variation at lps loci is attributed to be of advantage in evading the host immune system. Although LPS has been suggested as a potentiator of plant defense responses, interstrain variation at lps biosynthetic gene clusters has not been reported for any plant pathogenic bacterium.

Results: We report here the complete sequence of a 12.2 kb virulence locus of Xanthomonas oryzae pv. oryzae (Xoo) encoding six genes whose products are homologous to functions involved in LPS biosynthesis and transport. All six open reading frames (ORFs) have atypical G+C content and altered codon usage, which are the hallmarks of genomic islands that are acquired by horizontal gene transfer. The lps locus is flanked by highly conserved genes, metB and etfA, respectively encoding cystathionine gamma lyase and electron transport flavoprotein. Interestingly, two different sets of lps genes are present at this locus in the plant pathogens, Xanthomonas campestris pv. campestris (Xcc) and Xanthomonas axonopodis pv. citri (Xac). The genomic island is present in a number of Xoo strains from India and other Asian countries but is not present in two strains, one from India (BXO8) and another from Nepal (Nepal624) as well as the closely related rice pathogen, Xanthomonas oryzae pv. oryzicola (Xoor). TAIL-PCR analysis indicates that sequences related to Xac are present at the lps locus in both BXO8 and Nepal624. The Xoor strain has a hybrid lps gene cluster, with sequences at the metB and etfA ends, being most closely related to sequences from Xac and the tomato pathogen, Pseudomonas syringae pv. tomato respectively.

Conclusion: This is the first report of hypervariation at an lps locus between different strains of a plant pathogenic bacterium. Our results indicate that multiple HGT events have occurred at this locus in the xanthomonad group of plant pathogens.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Base Sequence
  • Codon
  • DNA, Bacterial / chemistry
  • Gene Transfer, Horizontal*
  • Genes, Bacterial*
  • Genetic Variation*
  • Genome, Bacterial
  • Lipopolysaccharides / biosynthesis*
  • Molecular Sequence Data
  • Oryza / microbiology
  • Repetitive Sequences, Nucleic Acid
  • Virulence Factors / genetics
  • Xanthomonas / genetics*
  • Xanthomonas / metabolism
  • Xanthomonas / pathogenicity

Substances

  • Codon
  • DNA, Bacterial
  • Lipopolysaccharides
  • Virulence Factors

Associated data

  • GENBANK/AF337647
  • GENBANK/AY319936
  • GENBANK/AY319937
  • GENBANK/AY319938
  • GENBANK/AY319939
  • GENBANK/AY319940
  • GENBANK/AY319941