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.
Highlights
Antibiotic resistance genes (ARGs) occur naturally and are evolutionarily ancient (Aminov and Mackie, 2007; D’Costa et al, 2011), but the pervasive use of antibiotics has accelerated their global propagation and precipitated a resistance crisis (Ventola, 2015; Van Puyvelde et al, 2018)
Lemurs from the three captivity settings had significantly greater ARG relative abundances (Figure 1A and Supplementary Table 2); whether considering all of the environments surveyed (LMM; t = 7.081, p < 0.0001; Figure 1A) or only the wilderness sites (LMM; t = 2.248, p = 0.027; Figure 1B), disturbance rank significantly correlated with the relative abundance of ARGs in host guts
By assessing ARGs in multiple ring-tailed lemur populations living under variably disturbed conditions, we (a) shed light on the breadth of ARG presence and diversity outside of traditionally studied settings, (b) highlight the potentially different routes by which ARGs may be acquired by wild versus captive animals, and (c) demonstrate covariance between lemur and soil resistomes in a subset of wild populations
Summary
Antibiotic resistance genes (ARGs) occur naturally and are evolutionarily ancient (Aminov and Mackie, 2007; D’Costa et al, 2011), but the pervasive use of antibiotics has accelerated their global propagation and precipitated a resistance crisis (Ventola, 2015; Van Puyvelde et al, 2018). Antibiotic resistance genes evolved as defense mechanisms, so natural ARGs are diverse, present in low abundances, and persist in microbial communities with no known human contamination (Segawa et al, 2013; Jardine et al, 2019). Their propensity to be exchanged via horizontal gene transfer has allowed ARGs to pass between and persist within host-associated and environmental microbial communities (Baquero et al, 2009; Forsberg et al, 2012; Martínez, 2012). The increased selective pressure from human antibiotic use, coupled with widespread human encroachment into natural environments, is expanding ARG reservoirs in wildlife and their environments (Gatica and Cytryn, 2013; Berglund, 2015; Anthony et al, 2018)
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