Transmission of Staphylococcus aureus from Humans to Green Monkeys in The Gambia as Revealed by Whole-Genome Sequencing

Abstract

Staphylococcus aureus is an important pathogen of humans and animals. We genome sequenced 90 S. aureus isolates from The Gambia: 46 isolates from invasive disease in humans, 13 human carriage isolates, and 31 monkey carriage isolates. We inferred multiple anthroponotic transmissions of S. aureus from humans to green monkeys (Chlorocebus sabaeus) in The Gambia over different time scales. We report a novel monkey-associated clade of S. aureus that emerged from a human-to-monkey switch estimated to have occurred 2,700 years ago. Adaptation of this lineage to the monkey host is accompanied by the loss of phagecarrying genes that are known to play an important role in human colonization. We also report recent anthroponotic transmission of the well-characterized human lineages sequence type 6 (ST6) and ST15 to monkeys, probably because of steadily increasing encroachment of humans into the monkeys' habitat. Although we have found no evidence of transmission of S. aureus from monkeys to humans, as the two species come into ever-closer contact, there might be an increased risk of additional interspecies exchanges of potential pathogens. IMPORTANCEThe population structures of Staphylococcus aureus in humans and monkeys in sub-Saharan Africa have been previously described using multilocus sequence typing (MLST). However, these data lack the power to accurately infer details regarding the origin and maintenance of new adaptive lineages. Here, we describe the use of whole-genome sequencing to detect transmission of S. aureus between humans and nonhuman primates and to document the genetic changes accompanying host adaptation. We note that human-to-monkey switches tend to be more common than the reverse and that a novel monkey-associated clade is likely to have emerged from such a switch approximately 2,700 years ago. Moreover, analysis of the accessory genome provides important clues as to the genetic changes underpinning host adaptation and, in particular, shows that human-to-monkey switches tend to be associated with the loss of genes known to confer adaptation to the human host.

The Impact of the Staphylococcus aureus Virulome on Infection in a Developing Country: A Cohort Study

“…In future studies, both PVL and Hlb should be taken into account when assessing the mechanism of SSTI in Africa. Hlb was mainly detected in ST152 isolates, consistent with findings from the Gambia ( Senghore et al, 2016 ). The clonal complex CC152 is wide spread in Africa (8–21% of all MSSA) ( Ruimy et al, 2008 ; Breurec et al, 2011 ).…”

Association of antimicrobial resistance and gut microbiota composition in human and non-human primates at an urban ecotourism site

“…This might suggest that there is a higher risk of human to primate transfer of resistance S. aureus than a zoonotic transfer. In line with this, anthropozoonosis transmission of S. aureus was reported from Gambia [22]. Nonetheless, the isolation of unique S. aureus ST type in primate suggested that the animal can also be an unappreciated source of MRSA transmission [23].…”

Genomic diversity ofEscherichia coliisolates from non-human primates in the Gambia

“…Accumulating data shows that ExPEC strains are frequently isolated from diseased companion animals and livestock—highlighting the potential for zoonotic as well as anthroponotic transmission (65–70). In a previous study, green monkeys from Bijilo Park were found to carry lineages of Staphylococcus aureus thought to be acquired from humans (31). Our analyses suggest similar exchange of E. coli strains between humans and wild non-human primates.…”

“…We sampled all four of the diurnal non-human primate species indigenous to the Gambia. Monkeys in Abuko and Bijilo are frequently hand-fed by visiting tourists, despite prohibiting guidelines (31).…”