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Zoo gut plastispheres enable pathogen escape and adaptation
Zipei Luo1, Yilun Liu1, Haimei Wu1
1National Engineering Laboratory of Applied Technology for Forestry & Ecology in South China, and Laboratory of Urban Forest Ecology of Hunan Province; Department of Ecology and Environment, Central South University of Forestry and Technology, Changsha, Hunan Province 410004, China.
Abstract:
In zoos, intensive human contact and artificial feeding may create pathways for microplastic (MP) ingestion and gut colonization. We hypothesized that ingested MPs form intestinal plastispheres with elevated pathogenic potential and enhanced environmental persistence. To test this, we surveyed feces from 15 zoo-dwelling species and coupled particle characterization, feces-derived intestinal simulations, metagenomic sequencing, and a subsequent water-exposure experiment. Zoo feces contained more abundant MPs than reported for wild counterparts, with fragments predominating and polyethylene terephthalate (PET)/polystyrene (PS) dominating polymer profiles. MP burdens tracked human-animal interaction patterns, with human-fed species (e.g., Tiger, Elephant) carrying the highest loads (88-212 items/g). MPs supported dense biofilms whose composition diverged from bulk gut communities, exhibiting greater compositional variability and substrate-specific assembly. Metagenomic analyses revealed coordinated enrichment of potentially pathogenic taxa, virulence factor genes (VFGs), and antibiotic resistance genes (ARGs), with ARG profiles dominated by efflux- and inactivation-related mechanisms and tightly associated with mobile genetic elements. Elevated Type II/III/IV/VI secretion systems and effector delivery-related VFGs occurred within extracellular polymeric substance-rich biofilms, suggesting enhanced potential for ARG retention and horizontal gene transfer. During the 35-day aquatic exposure, MP-associated communities persisted longer than non-plastic particle-associated communities and free gut microbiota, suggesting that plastic-specific properties promote microbial persistence. PET/PS plastispheres showed the slowest declines in bacterial activity and favored the persistence of Enterococcus, Enterobacter, and Clostridium. Overall, intestinal MPs in zoo animals may select, enrich, and export high-risk microbiomes, highlighting the need for MP mitigation and evidence-based management of zoos and adjacent ecosystems.
Insights
Microplastics (MPs) in zoo animals form gut biofilms that enrich pathogens and antibiotic resistance genes. These "plastispheres" persist in water, potentially spreading harmful microbes from zoos into ecosystems.
Area of Science:
- Environmental Science
- Microbiology
- Veterinary Science
Background:
- Intensive human contact and artificial feeding in zoos can lead to microplastic (MP) ingestion by animals.
- Ingested MPs may form intestinal plastispheres, potentially increasing pathogenic risks and environmental persistence.
Purpose of the Study:
- To investigate if ingested MPs in zoo animals create intestinal plastispheres with elevated pathogenic potential and environmental persistence.
- To analyze MP abundance, polymer types, and associated microbial communities in feces from various zoo species.
Main Methods:
- Fecal samples from 15 zoo species were analyzed for MPs.
- Intestinal simulations, metagenomic sequencing, and aquatic exposure experiments were conducted.
- Particle characterization and biofilm composition were examined.
Main Results:
- Zoo animal feces had higher MP abundance than wild counterparts, with polyethylene terephthalate (PET) and polystyrene (PS) fragments dominating.
- MP-associated biofilms showed enrichment of pathogenic taxa, virulence factors, and antibiotic resistance genes (ARGs).
- MP-associated microbial communities persisted longer in aquatic environments compared to non-plastic particles.
Conclusions:
- Intestinal MPs in zoo animals can select for and export high-risk microbiomes, including pathogens and ARGs.
- Plastispheres promote microbial persistence, posing a risk for spreading these communities into adjacent ecosystems.
- Mitigation of MPs and evidence-based zoo management are crucial for environmental and animal health.
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