Staphylococcus aureus Carriage in the Nasotracheal Cavities of White Stork Nestlings (Ciconia ciconia) in Spain: Genetic Diversity, Resistomes and Virulence Factors

Abstract

The molecular ecology of Staphylococcus aureus in migratory birds (such as white storks) is necessary to understand their relevance in the “One Health” ecosystems. This study determined the nasotracheal carriage rates of S. aureus from white storks in Southern Spain and genetically characterized the within-host diversity. A collection of 67 S. aureus strains, previously obtained from 87 white stork nestlings (52 nasal and 85 tracheal samples) fed by their parents with food foraged in natural and landfill habitats, were tested for their antimicrobial resistance (AMR) phenotypes. Moreover, the AMR genotypes, immune evasion cluster (IEC), virulence genes and the detection of CC398 lineage were studied by PCR. The spa types and multilocus-sequencing-typing (MLST) were also determined by PCR and sequencing. Staphylococcus aureus carriage was found in 31% of storks (36.5%/11.9% in nasal/tracheal samples). All isolates were methicillin-susceptible (MSSA) and 8.8% of them were also susceptible to all tested antibiotics. The AMR phenotype/percentage/genes detected were as follows: penicillin/79.1%/blaZ; erythromycin-clindamycin-inducible/19.1%/ermA, ermT; tetracycline/11.9%/tetK; clindamycin/4.5%/lnuA and ciprofloxacin/4.5%. Twenty-one different spa types, including 2 new ones (t7778-ST15-CC15 and t18009-ST26-CC25), were detected and ascribed to 11 clonal complexes (CCs). MSSA-CC398 (8.2%), MSSA-CC15 (7.1%) and MSSA-ST291 (5.9%) were the most prevalent lineages in storks. Moreover, tst-positive (MSSA-CC22-t223 and MSSA-CC30-t1654), eta-positive (MSSA-CC9-t209) and etb-positive strains (MSSA-CC45-t015) were detected in four storks. The 18.5% of storks harboured distinct MSSA strains (with different lineages and/or AMR genes). Nestlings of storks foraging in landfills (10 CCs) had more diverse S. aureus strains than those of parents foraging in natural habitats (3 CCs). Low level of AMR was demonstrated among S. aureus strains. The predominance of MSSA-CC398 (an emergent clade) and toxigenic MSSA strains in stork nestlings highlight the need for continuous surveillance of S. aureus in wild birds.

High clonal diversity of Staphylococcus aureus isolates from children’s playgrounds in Hungary

“…Methicillin resistant strains of ST398 are important livestock associated pathogens of worldwide distribution, whereas methicillin susceptible ST398 isolates are adapted to humans, are primarily transmitted from human to human, with the majority of the infections reported from Europe and China 39 . However, wild animals, including the migratory white storks have also been described to carry MSSA-CC398 40 .…”

Molecular Characterization of Chimeric Staphylococcus aureus Strains from Waterfowl

“…These might be acquired by consumption of meat, carcasses or offal, or by transmission due to contact with contaminated offal. Examples include the presence of CC97- and CC425-MSSA in cinereous vultures ( Aegypius monachus ) in Spain, of a CC97 in a Swedish golden eagle ( Aquila chrysaetos ), of CC130 mecC -MRSA and CC398-MRSA in cinereous vultures, storks ( Ciconia ciconia ) and magpies ( Pica pica ) in Spain, of CC5, CC7, CC22, CC25, CC30, CC45, CC59, CC133, CC291 and CC398 (MSSA and MRSA) in Spanish storks, of (presumably rodent-associated) CC49- and CC1956-MSSA as well as of CC130 mecC- MRSA in Portuguese owls and of CC22-MRSA-IV (PVL+) and CC1-MRSA-IV in Austrian rooks ( Corvus frugilegus ) [ 1 , 2 , 3 , 4 , 5 , 6 ].…”

Anatomical, pathological, and histological features of experimental respiratory infection of birds by biofilm-forming bacteria Staphylococcus aureus

“…MRSA was isolated from a swab of a non-healing wound on the lateral thigh of a 4-year-old male canary, Serinus canaria domestica [15]. The following phenotypic/percentage/gene indicators were detected in S. aureus from nasal and tracheal washings of Ciconia storks: penicillin/79.1%/blaZ; erythromycin-clindamycin-inducible/19.1%/ermA; ermT; tetracycline/11.9%/tetK; clindamycin/4.5%/ lnuA; and ciprofloxacin/4.5% [16].…”