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. 2009 Nov 17;106(46):19545-50.
doi: 10.1073/pnas.0909285106. Epub 2009 Nov 2.

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

Bethan V Lowder  1 , Caitriona M Guinane, Nouri L Ben Zakour, Lucy A Weinert, Andrew Conway-Morris, Robyn A Cartwright, A John Simpson, Andrew Rambaut, Ulrich Nübel, J Ross Fitzgerald
Affiliations

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

Bethan V Lowder et al. Proc Natl Acad Sci U S A. .

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.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
The majority of poultry S. aureus isolates evolved by a single host jump from humans followed by wide dissemination. (A) Geographical distribution of poultry and other avian S. aureus STs identified in countries from 4 different continents. Pie chart diameter is proportional to the number of isolates from each location. (B) Neighbor joining tree with bootstrapping consensus inferred from 500 replicates was constructed using concatenated sequences of S. aureus STs from birds (green branches) and representatives of the major clonal complexes of human and animal origin in the S. aureus species (black branches). The 2 major avian-associated clonal complexes, CC5 and CC385, are indicated in blue and red, respectively. (C) Minimum spanning tree based on 185 BiPs in 19 representative poultry ST5 isolates compared with 135 S. aureus ST5 human isolates of global origin analyzed in a previous study (9). Circle size is proportional to haplotype frequency and line length is proportional to the number of mutational steps between haplotypes. Colored nodes indicate the geographical origin of the poultry isolates, closely-related human isolates from Poland, and the human strain N315.
Fig. 2.
Fig. 2.
S. aureus avian isolates of distinct clonal lineage share a common accessory gene pool. (A) Novel MGEs identified in the whole-genome sequence of the ST5 poultry isolate ED98. The ED98 genome and plasmid maps represent ORFs (blue arrows on outer circle), GC content (middle circle), and GC skew (inner circle; GC+ and GC- skew in green and purple, respectively). Prophage and SaPI ORFs are represented by arrows, and red arrows denote genes putatively involved in virulence and/or host specificity. (B) The distribution of novel MGEs identified in the ED98 genome sequence among a panel of diverse isolates of avian, human, bovine, and ovine origin. Neighbor joining tree with bootstrapping consensus inferred from 500 replicates was constructed using concatenated sequences of S. aureus STs from different host species, including representatives of the major clonal complexes identified in the S. aureus species. Labels at branch tips denote STs of strains. A filled box indicates presence of an MGE and an empty box its absence as determined by MGE-specific PCR. A crossed box indicates the presence of a related but non-identical genetic element (determined by successful amplification in 1 of 2 PCRs). Red, blue, and green boxes denote strains of avian, human, and ruminant (bovine or ovine) origin, respectively. Strain prefixes denote the host species origin of the strains including ch, broiler chicken; ph, farmed pheasant; tu, farmed turkey; pa, farmed partridge; cl, poultry layer; bu, wild buzzard; hu, human; bo, cattle; and ov, sheep, respectively.
Fig. 3.
Fig. 3.
Poultry S. aureus strain ED98 exhibits increased resistance to killing by avian neutrophils (heterophils) in comparison with the human basal S. aureus strain MR1. Survival of poultry strain ED98 and human strain MR1 after opsonization with avian or human plasma followed by incubation with avian heterophil samples (n = 17) or human neutrophils (n = 13), measured by percentage reduction in colony count in the coculture compared with the colony count of the bacteria alone. Error bars indicate SE.
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