title: Acute oral toxicity of Yersinia pseudotuberculosis to fleas: implications for the evolution of vector-borne transmission of plague.
abstract: Yersinia pestis diverged from Yersinia pseudotuberculosis</= 20 000 years ago, during which time it evolved to be transmitted by fleas. In comparing the ability of these closely related species to infect the rat flea Xenopsylla cheopis, we found that Y. pseudotuberculosis, unlike Y. pestis, is orally toxic to fleas. Fleas showed signs of acute toxicity, including diarrhoea, immediately after feeding on blood containing Y. pseudotuberculosis in response to protein toxin(s) produced by the bacteria. Adherence of Y. pseudotuberculosis to the midgut and large intracellular vacuoles in midgut epithelial cells were detected during the first 24 h after infection. The insect pathogen Photorhabdus luminescens and its TcdA1 and TcdB1-TccC1 insecticidal toxin complexes were similarly toxic to fleas, implicating the toxin complex (tc) genes also present in Yersinia species. However, the Y. pestis and Y. pseudotuberculosis TcaAB and TcaC-TccC proteins were non-toxic to fleas, and Y. pseudotuberculosis mutants deleted of tc genes retained acute toxicity. Our results indicate that loss of one or more insect gut toxins was a critical step in the recent evolution of flea-borne transmission in the genus Yersinia. Changes in the tc insecticidal genes do not appear to have been responsible, but may have had other effects on Yersinia-flea interactions.
authors.affiliation: Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, NIH, NIAID, Hamilton, MT 59840, USA.
authors.forename: David L
authors.initials: DL
authors.lastname: Erickson
authors.forename: Nicholas R
authors.initials: NR
authors.lastname: Waterfield
authors.forename: Viveka
authors.initials: V
authors.lastname: Vadyvaloo
authors.forename: Daniel
authors.initials: D
authors.lastname: Long
authors.forename: Elizabeth R
authors.initials: ER
authors.lastname: Fischer
authors.forename: Richard
authors.initials: R
authors.lastname: Ffrench-Constant
authors.forename: B Joseph
authors.initials: BJ
authors.lastname: Hinnebusch
mesh_terms: D000818:Animals; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D004064:Digestive System / Q000382:microbiology; D005247:Feeding Behavior; D015964:Gene Expression Regulation, Bacterial; D007303:Insect Vectors / Q000382:microbiology*; D016296:Mutagenesis; D009154:Mutation; D010930:Plague / Q000382:microbiology / Q000635:transmission; D016133:Polymerase Chain Reaction; D051381:Rats; D005423:Siphonaptera / Q000382:microbiology*; D015009:Yersinia Infections / Q000382:microbiology; D015010:Yersinia pestis / Q000235:genetics / Q000378:metabolism / Q000472:pathogenicity; D015011:Yersinia pseudotuberculosis / Q000235:genetics / Q000378:metabolism* / Q000472:pathogenicity; D015012:Yersinia pseudotuberculosis Infections / Q000378:metabolism / Q000382:microbiology
chemical_list: D001426:Bacterial Proteins