Horizontal gene acquisition of Liberibacter plant pathogens from a bacteriome-confined endosymbiont of their psyllid vector

PLoS One. 2013 Dec 4;8(12):e82612. doi: 10.1371/journal.pone.0082612. eCollection 2013.

Abstract

he Asian citrus psyllid Diaphorina citri is a notorious agricultural pest that transmits the phloem-inhabiting alphaproteobacterial 'Candidatus Liberibacter asiaticus' and allied plant pathogens, which cause the devastating citrus disease called Huanglongbing or greening disease. D. citri harbors two distinct bacterial mutualists in the symbiotic organ called bacteriome: the betaproteobacterium 'Candidatus Profftella armatura' in the syncytial cytoplasm at the center of the bacteriome, and the gammaproteobacterium 'Candidatus Carsonella ruddii' in uninucleate bacteriocytes. Here we report that a putative amino acid transporter LysE of Profftella forms a highly supported clade with proteins of L. asiaticus, L. americanus, and L. solanacearum. L. crescens, the most basal Liberibacter lineage currently known, lacked the corresponding gene. The Profftella-Liberibacter subclade of LysE formed a clade with proteins from betaproteobacteria of the order Burkholderiales, to which Profftella belongs. This phylogenetic pattern favors the hypothesis that the Liberibacter lineage acquired the gene from the Profftella lineage via horizontal gene transfer (HGT) after L. crescens diverged from other Liberibacter lineages. K A/K S analyses further supported the hypothesis that the genes encoded in the Liberibacter genomes are functional. These findings highlight the possible evolutionary importance of HGT between plant pathogens and their insect vector's symbionts that are confined in the symbiotic organ and seemingly sequestered from external microbial populations.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Transport Systems / chemistry
  • Amino Acid Transport Systems / genetics
  • Animals
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Gene Order
  • Gene Transfer, Horizontal*
  • Genome, Bacterial
  • Hemiptera / microbiology*
  • Host-Pathogen Interactions*
  • Insect Vectors / microbiology*
  • Molecular Sequence Data
  • Phylogeny
  • Rhizobiaceae / classification
  • Rhizobiaceae / genetics*
  • Sequence Alignment

Substances

  • Amino Acid Transport Systems
  • Bacterial Proteins

Grants and funding

This work was supported by JSPS KAKENHI grant numbers 21687020 and 24117510 to AN. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.