Retracing the evolutionary path that led to flea-borne transmission of Yersinia pestis.
Yersinia pestis is an arthropod-borne bacterial pathogen that evolved recently from Yersinia pseudotuberculosis, an enteric pathogen transmitted via the fecal-oral route. This radical ecological transition can be attributed to a few discrete genetic changes from a still-extant recent ancestor, thus providing a tractable case study in pathogen evolution and emergence. Here, we determined the genetic and mechanistic basis of the evolutionary adaptation of Y. pestis to flea-borne transmission. Remarkably, only four minor changes in the bacterial progenitor, representing one gene gain and three gene losses, enabled transmission by flea vectors. All three loss-of-function mutations enhanced cyclic-di-GMP-mediated bacterial biofilm formation in the flea foregut, which greatly increased transmissibility. Our results suggest a step-wise evolutionary model in which Y. pestis emerged as a flea-borne clone, with each genetic change incrementally reinforcing the transmission cycle. The model conforms well to the ecological theory of adaptive radiation.
Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 903 South 4(th) Street, Hamilton, MT 59840, USA.
Yi-Cheng
YC
Sun
Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 903 South 4(th) Street, Hamilton, MT 59840, USA.
Clayton O
CO
Jarrett
Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 903 South 4(th) Street, Hamilton, MT 59840, USA.
Christopher F
CF
Bosio
Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 903 South 4(th) Street, Hamilton, MT 59840, USA. Electronic address: jhinnebusch@niaid.nih.gov.
B Joseph
BJ
Hinnebusch
D000818:Animals; D001426:Bacterial Proteins / Q000235:genetics; D018441:Biofilms; D005075:Biological Evolution; D005260:Female; D006801:Humans; D007303:Insect Vectors / Q000382:microbiology*; D008297:Male; D051379:Mice; D008969:Molecular Sequence Data; D009154:Mutation; D010802:Phylogeny; D005423:Siphonaptera / Q000382:microbiology*; D015009:Yersinia Infections / Q000382:microbiology / Q000635:transmission*; D015010:Yersinia pestis / Q000145:classification / Q000235:genetics* / Q000502:physiology; D015011:Yersinia pseudotuberculosis / Q000145:classification / Q000235:genetics / Q000502:physiology
D001426:Bacterial Proteins