Impact of human created environments in the pathogenic potential and antimicrobial resistance of staphylococci from wild neotropical primates in Brazil

Abstract

The non-human primate (NHP) Leontopithecus rosalia is an endangered species native of Brazil and lives in forest fragments with different levels of contact with humans (natural, private and urban). Other NHPs – Callithrix spp. - were introduced by humans and co-exist and interact with the native species in these forests. To evaluate if living in or close to human-modified environments could constitute a risk for L. rosalia, we compared the prevalence, genetic background, antibiotic susceptibility and virulence gene content of staphylococci collected from the native and the introduced species from different forest fragments. We found that presence in human-dominated environments increased the colonization rate of L. rosalia with Mammaliicoccus sciuri (former Staphylococcus sciuri) from 18 % to 85 % (p = 0.0001) and of Callithrix spp with Staphylococcus aureus from 6 % to 100 % (p = 0.0001). According to molecular typing data obtained differences probably resulted from dissemination of these bacterial species from the invader NHP species and from humans. Changes in microbiota were paralleled by an increase in the prevalence of Panton-Valentine Leukocidin gene and in resistance to beta-lactams, macrolides and/or lincosamides as exposure to human environment increased. In particular, erythromycin resistance in S. aureus from Callithrix spp. increased from 0 % to 50 % and resistance rate to at least one antibiotic in coagulase-negative staphylococci species from L. rosalia increased from 13 % to 56 % (p = 0.0003). Our results showed that contact of native animal species with human-created environments increased the content of antimicrobial resistant and pathogenic bacteria on their commensal microbiota, which ultimately can impact on their health. Importance: Endangered animal species are vulnerable to environmental alterations and human activities have been repeatedly identified as factors driving drastic changes in the natural landscape. It is extremely important to monitor changes in the environment surrounding protected species, because this could lead to early detection of any potential threats. In this study, we found that the contact of L. rosalia - a protected non-human primate from Brazil - with human environments is related to changes in their commensal microbiota. These included an increase in the number of pathogenic and antibiotic resistant bacteria, which have a higher potential to cause infections that are more difficult to treat. We provided evidence for the harmful impact human contact has on L. rosalia. Also, our results suggest that monitoring of commensal microbiota of protected animal species might be a useful way of sensing the risks of protected species to human exposure.