IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45638-9.html
   My bibliography  Save this article

Duplicated antibiotic resistance genes reveal ongoing selection and horizontal gene transfer in bacteria

Author

Listed:
  • Rohan Maddamsetti

    (Duke University
    Duke University)

  • Yi Yao

    (Duke University
    Duke University)

  • Teng Wang

    (Duke University
    Duke University)

  • Junheng Gao

    (Duke University School of Medicine)

  • Vincent T. Huang

    (Duke University
    Duke University)

  • Grayson S. Hamrick

    (Duke University
    Duke University
    Duke University)

  • Hye-In Son

    (Duke University
    Duke University)

  • Lingchong You

    (Duke University
    Duke University
    Duke University
    Duke University School of Medicine)

Abstract

Horizontal gene transfer (HGT) and gene duplication are often considered as separate mechanisms driving the evolution of new functions. However, the mobile genetic elements (MGEs) implicated in HGT can copy themselves, so positive selection on MGEs could drive gene duplications. Here, we use a combination of modeling and experimental evolution to examine this hypothesis and use long-read genome sequences of tens of thousands of bacterial isolates to examine its generality in nature. Modeling and experiments show that antibiotic selection can drive the evolution of duplicated antibiotic resistance genes (ARGs) through MGE transposition. A key implication is that duplicated ARGs should be enriched in environments associated with antibiotic use. To test this, we examined the distribution of duplicated ARGs in 18,938 complete bacterial genomes with ecological metadata. Duplicated ARGs are highly enriched in bacteria isolated from humans and livestock. Duplicated ARGs are further enriched in an independent set of 321 antibiotic-resistant clinical isolates. Our findings indicate that duplicated genes often encode functions undergoing positive selection and horizontal gene transfer in microbial communities.

Suggested Citation

  • Rohan Maddamsetti & Yi Yao & Teng Wang & Junheng Gao & Vincent T. Huang & Grayson S. Hamrick & Hye-In Son & Lingchong You, 2024. "Duplicated antibiotic resistance genes reveal ongoing selection and horizontal gene transfer in bacteria," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45638-9
    DOI: 10.1038/s41467-024-45638-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45638-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-45638-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Sheetal R. Modi & Henry H. Lee & Catherine S. Spina & James J. Collins, 2013. "Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome," Nature, Nature, vol. 499(7457), pages 219-222, July.
    2. David Zeevi & Tal Korem & Anastasia Godneva & Noam Bar & Alexander Kurilshikov & Maya Lotan-Pompan & Adina Weinberger & Jingyuan Fu & Cisca Wijmenga & Alexandra Zhernakova & Eran Segal, 2019. "Structural variation in the gut microbiome associates with host health," Nature, Nature, vol. 568(7750), pages 43-48, April.
    3. Howard Ochman & Jeffrey G. Lawrence & Eduardo A. Groisman, 2000. "Lateral gene transfer and the nature of bacterial innovation," Nature, Nature, vol. 405(6784), pages 299-304, May.
    4. Allison J. Lopatkin & Hannah R. Meredith & Jaydeep K. Srimani & Connor Pfeiffer & Rick Durrett & Lingchong You, 2017. "Persistence and reversal of plasmid-mediated antibiotic resistance," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    5. Chris S. Smillie & Mark B. Smith & Jonathan Friedman & Otto X. Cordero & Lawrence A. David & Eric J. Alm, 2011. "Ecology drives a global network of gene exchange connecting the human microbiome," Nature, Nature, vol. 480(7376), pages 241-244, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Patrick Munk & Christian Brinch & Frederik Duus Møller & Thomas N. Petersen & Rene S. Hendriksen & Anne Mette Seyfarth & Jette S. Kjeldgaard & Christina Aaby Svendsen & Bram Bunnik & Fanny Berglund & , 2022. "Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Peter J. Diebold & Matthew W. Rhee & Qiaojuan Shi & Nguyen Vinh Trung & Fayaz Umrani & Sheraz Ahmed & Vandana Kulkarni & Prasad Deshpande & Mallika Alexander & Ngo Hoa & Nicholas A. Christakis & Najee, 2023. "Clinically relevant antibiotic resistance genes are linked to a limited set of taxa within gut microbiome worldwide," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Tazzyman, Samuel J. & Bonhoeffer, Sebastian, 2013. "Fixation probability of mobile genetic elements such as plasmids," Theoretical Population Biology, Elsevier, vol. 90(C), pages 49-55.
    4. Aletheia Atzinger & Jeffrey G Lawrence, 2020. "Selection for ancient periodic motifs that do not impart DNA bending," PLOS Genetics, Public Library of Science, vol. 16(10), pages 1-25, October.
    5. Izabela Wolak & Małgorzata Czatzkowska & Monika Harnisz & Jan Paweł Jastrzębski & Łukasz Paukszto & Paulina Rusanowska & Ewa Felis & Ewa Korzeniewska, 2022. "Metagenomic Analysis of the Long-Term Synergistic Effects of Antibiotics on the Anaerobic Digestion of Cattle Manure," Energies, MDPI, vol. 15(5), pages 1-19, March.
    6. João F Matias Rodrigues & Andreas Wagner, 2009. "Evolutionary Plasticity and Innovations in Complex Metabolic Reaction Networks," PLOS Computational Biology, Public Library of Science, vol. 5(12), pages 1-11, December.
    7. Gina Paola Rodriguez-Castaño & Federico E Rey & Alejandro Caro-Quintero & Alejandro Acosta-González, 2020. "Gut-derived Flavonifractor species variants are differentially enriched during in vitro incubation with quercetin," PLOS ONE, Public Library of Science, vol. 15(12), pages 1-21, December.
    8. Rong Liu & You Zou & Wei-Quan Wang & Jun-Hong Chen & Lei Zhang & Jia Feng & Ji-Ye Yin & Xiao-Yuan Mao & Qing Li & Zhi-Ying Luo & Wei Zhang & Dao-Ming Wang, 2023. "Gut microbial structural variation associates with immune checkpoint inhibitor response," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. Suzanne Humphrey & Álvaro San Millán & Macarena Toll-Riera & John Connolly & Alejandra Flor-Duro & John Chen & Carles Ubeda & R. Craig MacLean & José R. Penadés, 2021. "Staphylococcal phages and pathogenicity islands drive plasmid evolution," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    10. Yinyin Ma & Josep Ramoneda & David R. Johnson, 2023. "Timing of antibiotic administration determines the spread of plasmid-encoded antibiotic resistance during microbial range expansion," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    11. Charles K Fisher & Thierry Mora & Aleksandra M Walczak, 2017. "Variable habitat conditions drive species covariation in the human microbiota," PLOS Computational Biology, Public Library of Science, vol. 13(4), pages 1-18, April.
    12. Nils Giordano & Marinna Gaudin & Camille Trottier & Erwan Delage & Charlotte Nef & Chris Bowler & Samuel Chaffron, 2024. "Genome-scale community modelling reveals conserved metabolic cross-feedings in epipelagic bacterioplankton communities," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    13. Nara Figueroa-Bossi & Rocío Fernández-Fernández & Patricia Kerboriou & Philippe Bouloc & Josep Casadesús & María Antonia Sánchez-Romero & Lionello Bossi, 2024. "Transcription-driven DNA supercoiling counteracts H-NS-mediated gene silencing in bacterial chromatin," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    14. Brian D. Huang & Dowan Kim & Yongjoon Yu & Corey J. Wilson, 2024. "Engineering intelligent chassis cells via recombinase-based MEMORY circuits," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Samuel C. Forster & Junyan Liu & Nitin Kumar & Emily L. Gulliver & Jodee A. Gould & Alejandra Escobar-Zepeda & Tapoka Mkandawire & Lindsay J. Pike & Yan Shao & Mark D. Stares & Hilary P. Browne & B. A, 2022. "Strain-level characterization of broad host range mobile genetic elements transferring antibiotic resistance from the human microbiome," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    16. Lashin, Sergey A. & Matushkin, Yury G. & Suslov, Valentin V. & Kolchanov, Nikolay A., 2012. "Computer modeling of genome complexity variation trends in prokaryotic communities under varying habitat conditions," Ecological Modelling, Elsevier, vol. 224(1), pages 124-129.
    17. Liang Chen & Na Zhao & Jiabao Cao & Xiaolin Liu & Jiayue Xu & Yue Ma & Ying Yu & Xuan Zhang & Wenhui Zhang & Xiangyu Guan & Xiaotong Yu & Zhipeng Liu & Yanqun Fan & Yang Wang & Fan Liang & Depeng Wang, 2022. "Short- and long-read metagenomics expand individualized structural variations in gut microbiomes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    18. Shao-Ming Gao & Han-Lan Fei & Qi Li & Li-Ying Lan & Li-Nan Huang & Peng-Fei Fan, 2024. "Eco-evolutionary dynamics of gut phageome in wild gibbons (Hoolock tianxing) with seasonal diet variations," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    19. Jennifer Kuzma & James Romanchek & Adam Kokotovich, 2008. "Upstream Oversight Assessment for Agrifood Nanotechnology: A Case Studies Approach," Risk Analysis, John Wiley & Sons, vol. 28(4), pages 1081-1098, August.
    20. Kihyun Lee & Sebastien Raguideau & Kimmo Sirén & Francesco Asnicar & Fabio Cumbo & Falk Hildebrand & Nicola Segata & Chang-Jun Cha & Christopher Quince, 2023. "Population-level impacts of antibiotic usage on the human gut microbiome," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45638-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.