Alterations in the gut resistomes of endangered wild equids associated with anthropogenic activities: Insights for One Health surveillance.

Overview

• This study investigates how human activities influence antibiotic resistance genes in the gut microbiomes of endangered wild horses and related species, highlighting the importance of monitoring antibiotic resistance in wildlife for overall health.

Background and Purpose

• Antibiotic resistance genes (ARGs) are increasingly recognized as environmental contaminants that pose risks to both human and animal health.
• Understanding how anthropogenic (human-related) management practices affect the movement and presence of these ARGs in endangered wildlife is crucial but not well understood.
• This study focuses on the gut microbiomes—the collection of microorganisms living in the digestive tracts—of three equid species (wild horses) in Xinjiang, China: Przewalski’s horses (both wild and captive), Mongolian khulans (wild asses), and domestic horses.

Methodology

• Researchers used fecal metagenomics, a technique analyzing the genetic material from feces, to identify and quantify:
  • Antibiotic resistance genes (ARGs)
  • Metal resistance genes (MRGs)
  • Mobile genetic elements (MGEs), which can transfer resistance genes between bacteria
• A total of 47 fecal samples were analyzed.
• Further, genome-resolved analysis was performed by assembling metagenome-assembled genomes (MAGs) to discover bacteria carrying these resistance elements.
• Advanced statistical approaches like co-occurrence network analysis and structural equation modeling were used to understand relationships between the variables.

Key Findings

• ARG Diversity and Abundance:
  • 380 different ARG subtypes were identified across samples.
  • Przewalski’s horses (both wild and captive) and domestic horses had higher ARG loads compared to Mongolian khulans.
• Metal Resistance Genes (MRGs):
  • Mongolian khulans had a higher burden of metal resistance genes, which could relate to environmental exposures.
• Mobile Genetic Elements (MGEs):
  • 26 types of MGEs were found in the samples.
  • Within Przewalski’s horses, those in captivity showed higher MGE loads, suggesting increased potential for gene transfer in managed environments.
  • Specific genes like tet(W) (tetracycline resistance), lnu(C) (lincosamide resistance), vanYG1 (vancomycin), transposase genes, and IS91 transposable elements were enriched in captive horses.
• Relationships and Dynamics:
  • Captive management settings were positively associated with the presence of the IS91 element.
  • IS91 is linked with the enrichment of ARGs and the co-occurrence of ARGs with metal resistance genes, implying a mechanism for spreading resistance.
• Microbial Hosts of Resistance:
  • 590 medium- to high-quality MAGs recovered.
  • MAGs carrying ARGs, MRGs, and MGEs mostly belonged to anaerobic gut bacteria including Prevotella, Alloprevotella, Cryptobacteroides, and Limivicinus.
  • This highlights specific bacterial genera as key reservoirs and vectors of resistance genes in the gut environment.

Implications and Significance

• Human management practices, especially captive breeding and protected area management, influence the abundance and mobility of antibiotic resistance genes in endangered equids.
• The enrichment of mobile genetic elements in captive animals suggests that human-associated environments may promote the spread of resistance genes within wildlife microbiomes.
• Endangered wild horses can serve as sentinel species—early indicators of antibiotic resistance reservoirs that exist at the interface between wildlife, humans, and the environment.
• This supports the One Health approach, which emphasizes integrated surveillance and management of health risks affecting humans, animals, and ecosystems.
• Monitoring ARGs and MGEs in wildlife management and conservation programs is recommended to better understand and mitigate the spread of antimicrobial resistance.