TY - JOUR
T1 - Multilayer networks of plasmid genetic similarity reveal potential pathways of gene transmission
AU - Shapiro, Julie Teresa
AU - Zorea, Alvah
AU - Kav, Aya Brown
AU - Ontiveros, Vicente J.
AU - Mizrahi, Itzhak
AU - Pilosof, Shai
N1 - Publisher Copyright:
© 2023, The Author(s).
PY - 2023/5/1
Y1 - 2023/5/1
N2 - Antimicrobial resistance (AMR) is a significant threat to public health. Plasmids are principal vectors of AMR genes, significantly contributing to their spread and mobility across hosts. Nevertheless, little is known about the dynamics of plasmid genetic exchange across animal hosts. Here, we use theory and methodology from network and disease ecology to investigate the potential of gene transmission between plasmids using a data set of 21 plasmidomes from a single dairy cow population. We constructed a multilayer network based on pairwise plasmid genetic similarity. Genetic similarity is a signature of past genetic exchange that can aid in identifying potential routes and mechanisms of gene transmission within and between cows. Links between cows dominated the transmission network, and plasmids containing mobility genes were more connected. Modularity analysis revealed a network cluster where all plasmids contained a mobM gene, and one where all plasmids contained a beta-lactamase gene. Cows that contain both clusters also share transmission pathways with many other cows, making them candidates for super-spreading. In support, we found signatures of gene super-spreading in which a few plasmids and cows are responsible for most gene exchange. An agent-based transmission model showed that a new gene invading the cow population will likely reach all cows. Finally, we showed that edge weights contain a non-random signature for the mechanisms of gene transmission, allowing us to differentiate between dispersal and genetic exchange. These results provide insights into how genes, including those providing AMR, spread across animal hosts.
AB - Antimicrobial resistance (AMR) is a significant threat to public health. Plasmids are principal vectors of AMR genes, significantly contributing to their spread and mobility across hosts. Nevertheless, little is known about the dynamics of plasmid genetic exchange across animal hosts. Here, we use theory and methodology from network and disease ecology to investigate the potential of gene transmission between plasmids using a data set of 21 plasmidomes from a single dairy cow population. We constructed a multilayer network based on pairwise plasmid genetic similarity. Genetic similarity is a signature of past genetic exchange that can aid in identifying potential routes and mechanisms of gene transmission within and between cows. Links between cows dominated the transmission network, and plasmids containing mobility genes were more connected. Modularity analysis revealed a network cluster where all plasmids contained a mobM gene, and one where all plasmids contained a beta-lactamase gene. Cows that contain both clusters also share transmission pathways with many other cows, making them candidates for super-spreading. In support, we found signatures of gene super-spreading in which a few plasmids and cows are responsible for most gene exchange. An agent-based transmission model showed that a new gene invading the cow population will likely reach all cows. Finally, we showed that edge weights contain a non-random signature for the mechanisms of gene transmission, allowing us to differentiate between dispersal and genetic exchange. These results provide insights into how genes, including those providing AMR, spread across animal hosts.
UR - http://www.scopus.com/inward/record.url?scp=85148700907&partnerID=8YFLogxK
U2 - 10.1038/s41396-023-01373-5
DO - 10.1038/s41396-023-01373-5
M3 - Article
C2 - 36759552
AN - SCOPUS:85148700907
SN - 1751-7362
VL - 17
SP - 649
EP - 659
JO - ISME Journal
JF - ISME Journal
IS - 5
ER -