Antibiotic Resistance Genes in Lemur Gut and Soil Microbiota Along a Gradient of Anthropogenic Disturbance

Abstract

The overuse of man-made antibiotics has facilitated the global propagation of antibiotic resistance genes in animals, across natural and anthropogenically disturbed environments. Although antibiotic treatment is the most well-studied route by which resistance genes can develop and spread within host-associated microbiota, resistomes also can be acquired or enriched via more indirect routes, such as via transmission between hosts or via contact with antibiotic-contaminated matter within the environment. Relatively little is known about the impacts of anthropogenic disturbance on reservoirs of resistance genes in wildlife and their environments. We therefore tested for (a) antibiotic resistance genes in primate hosts experiencing different severities and types of anthropogenic disturbance (i.e., non-wildlife animal presence, human presence, direct human contact, and antibiotic treatment), and (b) covariation between host-associated and environmental resistomes. We used shotgun metagenomic sequencing of ring-tailed lemur (Lemur catta) gut resistomes and associated soil resistomes sampled from up to 10 sites: seven in the wilderness of Madagascar and three in captivity in Madagascar or the United States. We found that, compared to wild lemurs, captive lemurs harbored greater abundances of resistance genes, but not necessarily more diverse resistomes. Abundances of resistance genes were positively correlated with our assessments of anthropogenic disturbance, a pattern that was robust across all ten lemur populations. The composition of lemur resistomes was site-specific and the types of resistance genes reflected antibiotic usage in the country of origin, such as vancomycin use in Madagascar. We found support for multiple routes of ARG enrichment (e.g., via human contact, antibiotic treatment, and environmental acquisition) that differed across lemur populations, but could result in similar degrees of enrichment. Soil resistomes varied across natural habitats in Madagascar and, at sites with greater anthropogenic disturbance, lemurs and soil resistomes covaried. As one of the broadest, single-species investigations of wildlife resistomes to date, we show that the transmission and enrichment of antibiotic resistance genes varies across environments, thereby adding to the mounting evidence that the resistance crisis extends outside of traditional clinical settings.

Comparing Antibiotic Resistance in Free-Ranging vs. Captive African Wild Herbivores

“…Other factors that may contribute to this difference in AMR include movement and access to shared water points, but these could not be investigated in this study. Another study found a larger number of β-lactam–resistant Enterobacteriaceae in plains zebra in Tanzania and provided a behavioral explanation: plains zebras are frequently found near human dwellings and may come into contact with human waste and be exposed to contamination by resistant bacteria (Katakweba et al 2015; Bornbusch and Drea 2021).…”

A comparison of rectal and oral cultivable microbiota in wild and captive black lion tamarins (Leontopithecus chrysopygus, Mikan 1823)

“…More information is needed to understand the microbial composition of healthy gut microbiota in wild and captive nonhuman primates. For example, studies of antimicrobial resistance and social environment are crucial to connect microbiotal information to animal health (Barelli et al, 2021; Bornbusch & Drea, 2021; García et al, 2020; Kuthyar et al, 2019; Perofsky et al, 2017; Sarkar et al, 2020; Tsukayama et al, 2018; Tung et al, 2015; Zhu et al, 2021; Zvoboda, 2017). A decrease in the diversity of intestinal microbiome species may be associated with diseases and inflammation thus aiding pathogenic microorganisms (Battaglioli et al, 2018; Cho & Blaser, 2012; Hale et al, 2019; Petersen & Round, 2014).…”

Gut microbiota of skywalker hoolock gibbons (Hoolock tianxing) from different habitats and in captivity: Implications for gibbon health

“…For example, the gut microbiota of nonhuman primates (NHPs) is observably affected by captive rearing (Campbell et al, 2020; Littleford‐Colquhoun et al, 2019), with lower bacterial alpha‐diversity and humanlike microbes (Clayton et al, 2016; Kohl et al, 2014; Metcalf et al, 2017; Uenishi et al, 2007). These changes in gut microbiota profiles may be linked to reduced reproduction and a greater risk of disease infection in captive animals (Amato, Metcalf, et al, 2016; Baros Jorquera et al, 2021; Bornbusch & Drea, 2021; Schluter et al, 2020). Previous research on captive baboons (Papio kindae) found that the relative abundance of drug‐resistant bacteria significantly increased in their gut compared to wild baboons (Tsukayama et al, 2018).…”