Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus

doi:10.1073/pnas.0909285106

Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus

^aThe Roslin Institute and Centre for Infectious Diseases, Royal (Dick) School of Veterinary Studies,
^bInstitute of Evolutionary Biology, and
^cCentre for Inflammation Research, Queens Medical Research Institute, University of Edinburgh, Edinburgh EH8 9YL, Scotland, United Kingdom; and
^dRobert Koch Institut, 38855 Wernigerode, Germany

Edited by Richard P. Novick, New York University School of Medicine, New York, NY, and approved September 18, 2009 (received for review August 14, 2009)

Abstract

The impact of globalization on the emergence and spread of pathogens is an important veterinary and public health issue. Staphylococcus aureus is a notorious human pathogen associated with serious nosocomial and community-acquired infections. In addition, S. aureus is a major cause of animal diseases including skeletal infections of poultry, which are a large economic burden on the global broiler chicken industry. Here, we provide evidence that the majority of S. aureus isolates from broiler chickens are the descendants of a single human-to-poultry host jump that occurred approximately 38 years ago (range, 30 to 63 years ago) by a subtype of the worldwide human ST5 clonal lineage unique to Poland. In contrast to human subtypes of the ST5 radiation, which demonstrate strong geographic clustering, the poultry ST5 clade was distributed in different continents, consistent with wide dissemination via the global poultry industry distribution network. The poultry ST5 clade has undergone genetic diversification from its human progenitor strain by acquisition of novel mobile genetic elements from an avian-specific accessory gene pool, and by the inactivation of several proteins important for human disease pathogenesis. These genetic events have resulted in enhanced resistance to killing by chicken heterophils, reflecting avian host-adaptive evolution. Taken together, we have determined the evolutionary history of a major new animal pathogen that has undergone rapid avian host adaptation and intercontinental dissemination. These data provide a new paradigm for the impact of human activities on the emergence of animal pathogens.

Footnotes

¹To whom correspondence should be addressed. E-mail: ross.fitzgerald{at}ed.ac.uk
Author contributions: B.V.L., A.J.S., U.N., and J.R.F. designed research; B.V.L., C.M.G., N.L.B.Z., L.A.W., A.C.-M., R.A.C., A.R., and U.N. performed research; N.L.B.Z. contributed new reagents/analytic tools; B.V.L., C.M.G., N.L.B.Z., L.A.W., A.C.-M., A.J.S., A.R., U.N., and J.R.F. analyzed data; and B.V.L. and J.R.F. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. CP001781, CP001782, CP001783, and CP001784 (ED98 genome sequence, chromosome and plasmids, respectively); and ACZQ00000000 (MR1 Whole Genome Shotgun Project)].
This article contains supporting information online at www.pnas.org/cgi/content/full/0909285106/DCSupplemental.