Recombination-Mediated Host Adaptation by Avian Staphylococcus aureus

Abstract

Staphylococcus aureus are globally disseminated among farmed chickens causing skeletal muscle infections, dermatitis, and septicaemia. The emergence of poultry-associated lineages has involved zoonotic transmission from humans to chickens but questions remain about the specific adaptations that promote proliferation of chicken pathogens. We characterized genetic variation in a population of genome-sequenced S. aureus isolates of poultry and human origin. Genealogical analysis identified a dominant poultry-associated sequence cluster within the CC5 clonal complex. Poultry and human CC5 isolates were significantly distinct from each other and more recombination events were detected in the poultry isolates. We identified 44 recombination events in 33 genes along the branch extending to the poultry-specific CC5 cluster, and 47 genes were found more often in CC5 poultry isolates compared with those from humans. Many of these gene sequences were common in chicken isolates from other clonal complexes suggesting horizontal gene transfer among poultry associated lineages. Consistent with functional predictions for putative poultry-associated genes, poultry isolates showed enhanced growth at 42 °C and greater erythrocyte lysis on chicken blood agar in comparison with human isolates. By combining phenotype information with evolutionary analyses of staphylococcal genomes, we provide evidence of adaptation, following a human-to-poultry host transition. This has important implications for the emergence and dissemination of new pathogenic clones associated with modern agriculture.

Lineage‐specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group

“…As in recent publications on other species (Meric, Hitchings, Pascoe, & Sheppard, 2016;Monteil et al, 2016;Morley et al, 2015;Murray et al, 2017;Yahara et al, 2017), a reference pan-genome approach was used with gene-by-gene alignment, consistent with whole-genome MLST (Jolley & Maiden, 2010;Maiden et al, 2013;Meric et al, 2014;Sheppard, Jolley, & Maiden, 2012), implemented in BIGSdb open-source software. Briefly, the reference pan-genome was constructed by combining the genomes of several reference strains (Bt strain YBT020 (Zhu et al, 2011), Bc strain ATCC 14579 (Ivanova et al, 2003) and Ba strain Ames (Read et al, 2003)) with whole-genome annotations from all the other genomes of this study to derive a single gene list.…”

Virulence Factors and Phylogeny of Staphylococcus aureus Associated With Bovine Mastitis in Russia Based on Genome Sequences

“…In recent years, the frequency of the confirmed transition of antibiotic-resistant strains from animal to human populations is rapidly growing. Therefore, the study of the microflora of animals in close contact with humans is relevant (4)(5)(6)(7).…”

Staphylococcus aureus in Animals

“…At least 44 recombination events in 33 genes have accumulated in poultry isolates and a further 47 genes were found to be more frequent in poultry compared to human isolates. Interestingly, many of these genes were common among chicken isolates from other clonal complexes indicating that horizontal transfer of these genes between CCs may have a potential role in host adaptation (102). On a phenotypic level, these genetic alterations contribute to S. aureus adaptation to their poultry host and poultry isolates show enhanced growth at 42°C (the core body temperature of the adult chicken (106)) and greater erythrocyte lysis on chicken blood agar for chicken compared to human isolates (102).…”

“…Interestingly, many of these genes were common among chicken isolates from other clonal complexes indicating that horizontal transfer of these genes between CCs may have a potential role in host adaptation (102). On a phenotypic level, these genetic alterations contribute to S. aureus adaptation to their poultry host and poultry isolates show enhanced growth at 42°C (the core body temperature of the adult chicken (106)) and greater erythrocyte lysis on chicken blood agar for chicken compared to human isolates (102). Conversely, most human isolates but only around half of the chicken isolates were able to lyse human erythrocytes (102).…”

“…On a phenotypic level, these genetic alterations contribute to S. aureus adaptation to their poultry host and poultry isolates show enhanced growth at 42°C (the core body temperature of the adult chicken (106)) and greater erythrocyte lysis on chicken blood agar for chicken compared to human isolates (102). Conversely, most human isolates but only around half of the chicken isolates were able to lyse human erythrocytes (102). The improved growth of chicken isolates at 42°C is thought to be related to two poultry-associated genes (SAAV_0062 and SAAV_0064) that share more than 85% nucleotide identity with genes important for growth at elevated temperatures, including dnaK and dnaE (102).…”