Abstract
There is growing evidence that anthropogenic sources of antibiotics and antimicrobial-resistant bacteria can spill over into natural ecosystems, raising questions about the role wild animals play in the emergence, maintenance, and dispersal of antibiotic resistance genes. In particular, we lack an understanding of how resistance genes circulate within wild animal populations, including whether specific host characteristics, such as social associations, promote interhost transmission of these genes. In this study, we used social network analysis to explore the forces shaping population-level patterns of resistant Escherichia coli in wild giraffe (Giraffa camelopardalis) and assess the relative importance of social contact for the dissemination of resistant E. coli between giraffe. Of 195 giraffe sampled, only 5.1% harbored E. coli isolates resistant to one or more tested antibiotics. Whole-genome sequencing on a subset of resistant isolates revealed a number of acquired resistance genes with linkages to mobile genetic elements. However, we found no evidence that the spread of resistance genes among giraffe was facilitated by interhost associations. Giraffe with lower social degree were more likely to harbor resistant E. coli, but this relationship was likely driven by a correlation between an individual's social connectedness and age. Indeed, resistant E. coli was most frequently detected in socially isolated neonates, indicating that resistant E. coli may have a selective advantage in the gastrointestinal tracts of neonates compared to other age classes. Taken together, these results suggest that the maintenance of antimicrobial-resistant bacteria in wild populations may, in part, be determined by host traits and microbial competition dynamics within the host.
| Language | English (US) |
|---|---|
| Article number | e02136-18 |
| Journal | Applied and Environmental Microbiology |
| Volume | 85 |
| Issue number | 1 |
| DOIs | |
| State | Published - Jan 1 2019 |
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Keywords
- Antibiotic resistance
- Escherichia coli
- Social network analysis
- Transmission dynamics
- Wildlife
ASJC Scopus subject areas
- Biotechnology
- Food Science
- Applied Microbiology and Biotechnology
- Ecology
Cite this
Assessing transmission of antimicrobialresistant Escherichia coli in wild giraffe contact networks. / Miller, Elizabeth A.; Johnson, Timothy J.; Omondi, George; Atwill, Edward R; Isbell, Lynne A.; Mccowan, Brenda; VanderWaal, Kimberly.
In: Applied and Environmental Microbiology, Vol. 85, No. 1, e02136-18, 01.01.2019.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Assessing transmission of antimicrobialresistant Escherichia coli in wild giraffe contact networks
AU - Miller, Elizabeth A.
AU - Johnson, Timothy J.
AU - Omondi, George
AU - Atwill, Edward R
AU - Isbell, Lynne A.
AU - Mccowan, Brenda
AU - VanderWaal, Kimberly
PY - 2019/1/1
Y1 - 2019/1/1
N2 - There is growing evidence that anthropogenic sources of antibiotics and antimicrobial-resistant bacteria can spill over into natural ecosystems, raising questions about the role wild animals play in the emergence, maintenance, and dispersal of antibiotic resistance genes. In particular, we lack an understanding of how resistance genes circulate within wild animal populations, including whether specific host characteristics, such as social associations, promote interhost transmission of these genes. In this study, we used social network analysis to explore the forces shaping population-level patterns of resistant Escherichia coli in wild giraffe (Giraffa camelopardalis) and assess the relative importance of social contact for the dissemination of resistant E. coli between giraffe. Of 195 giraffe sampled, only 5.1% harbored E. coli isolates resistant to one or more tested antibiotics. Whole-genome sequencing on a subset of resistant isolates revealed a number of acquired resistance genes with linkages to mobile genetic elements. However, we found no evidence that the spread of resistance genes among giraffe was facilitated by interhost associations. Giraffe with lower social degree were more likely to harbor resistant E. coli, but this relationship was likely driven by a correlation between an individual's social connectedness and age. Indeed, resistant E. coli was most frequently detected in socially isolated neonates, indicating that resistant E. coli may have a selective advantage in the gastrointestinal tracts of neonates compared to other age classes. Taken together, these results suggest that the maintenance of antimicrobial-resistant bacteria in wild populations may, in part, be determined by host traits and microbial competition dynamics within the host.
AB - There is growing evidence that anthropogenic sources of antibiotics and antimicrobial-resistant bacteria can spill over into natural ecosystems, raising questions about the role wild animals play in the emergence, maintenance, and dispersal of antibiotic resistance genes. In particular, we lack an understanding of how resistance genes circulate within wild animal populations, including whether specific host characteristics, such as social associations, promote interhost transmission of these genes. In this study, we used social network analysis to explore the forces shaping population-level patterns of resistant Escherichia coli in wild giraffe (Giraffa camelopardalis) and assess the relative importance of social contact for the dissemination of resistant E. coli between giraffe. Of 195 giraffe sampled, only 5.1% harbored E. coli isolates resistant to one or more tested antibiotics. Whole-genome sequencing on a subset of resistant isolates revealed a number of acquired resistance genes with linkages to mobile genetic elements. However, we found no evidence that the spread of resistance genes among giraffe was facilitated by interhost associations. Giraffe with lower social degree were more likely to harbor resistant E. coli, but this relationship was likely driven by a correlation between an individual's social connectedness and age. Indeed, resistant E. coli was most frequently detected in socially isolated neonates, indicating that resistant E. coli may have a selective advantage in the gastrointestinal tracts of neonates compared to other age classes. Taken together, these results suggest that the maintenance of antimicrobial-resistant bacteria in wild populations may, in part, be determined by host traits and microbial competition dynamics within the host.
KW - Antibiotic resistance
KW - Escherichia coli
KW - Social network analysis
KW - Transmission dynamics
KW - Wildlife
UR - http://www.scopus.com/inward/record.url?scp=85059768204&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85059768204&partnerID=8YFLogxK
U2 - 10.1128/AEM.02136-18
DO - 10.1128/AEM.02136-18
M3 - Article
VL - 85
JO - Applied and Environmental Microbiology
T2 - Applied and Environmental Microbiology
JF - Applied and Environmental Microbiology
SN - 0099-2240
IS - 1
M1 - e02136-18
ER -