IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42769-3.html
   My bibliography  Save this article

Eco-evolutionary feedbacks in the human gut microbiome

Author

Listed:
  • Benjamin H. Good

    (Stanford University
    Stanford University
    Chan Zuckerberg Biohub—San Francisco)

  • Layton B. Rosenfeld

    (Stanford University)

Abstract

Gut microbiota can evolve within their hosts on human-relevant timescales, but little is known about how these changes influence (or are influenced by) the composition of their local community. Here, by combining ecological and evolutionary analyses of a large cohort of human gut metagenomes, we show that the short-term evolution of the microbiota is linked with shifts in its ecological structure. These correlations are not simply explained by expansions of the evolving species, and often involve additional fluctuations in distantly related taxa. We show that similar feedbacks naturally emerge in simple resource competition models, even in the absence of cross-feeding or predation. These results suggest that the structure and function of host microbiota may be shaped by their local evolutionary history, which could have important implications for personalized medicine and microbiome engineering.

Suggested Citation

  • Benjamin H. Good & Layton B. Rosenfeld, 2023. "Eco-evolutionary feedbacks in the human gut microbiome," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42769-3
    DOI: 10.1038/s41467-023-42769-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42769-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-42769-3?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. Jason Lloyd-Price & Anup Mahurkar & Gholamali Rahnavard & Jonathan Crabtree & Joshua Orvis & A. Brantley Hall & Arthur Brady & Heather H. Creasy & Carrie McCracken & Michelle G. Giglio & Daniel McDona, 2017. "Strains, functions and dynamics in the expanded Human Microbiome Project," Nature, Nature, vol. 550(7674), pages 61-66, October.
    2. Jason Lloyd-Price & Anup Mahurkar & Gholamali Rahnavard & Jonathan Crabtree & Joshua Orvis & A. Brantley Hall & Arthur Brady & Heather H. Creasy & Carrie McCracken & Michelle G. Giglio & Daniel McDona, 2017. "Erratum: Strains, functions and dynamics in the expanded Human Microbiome Project," Nature, Nature, vol. 551(7679), pages 256-256, November.
    3. Elizabeth Stanley Shepherd & William C. DeLoache & Kali M. Pruss & Weston R. Whitaker & Justin L. Sonnenburg, 2018. "An exclusive metabolic niche enables strain engraftment in the gut microbiota," Nature, Nature, vol. 557(7705), pages 434-438, May.
    4. Yang Bai & Daniel B. Müller & Girish Srinivas & Ruben Garrido-Oter & Eva Potthoff & Matthias Rott & Nina Dombrowski & Philipp C. Münch & Stijn Spaepen & Mitja Remus-Emsermann & Bruno Hüttel & Alice C., 2015. "Functional overlap of the Arabidopsis leaf and root microbiota," Nature, Nature, vol. 528(7582), pages 364-369, December.
    5. Seth Rakoff-Nahoum & Kevin R. Foster & Laurie E. Comstock, 2016. "The evolution of cooperation within the gut microbiota," Nature, Nature, vol. 533(7602), pages 255-259, May.
    6. Thomas Scheuerl & Meirion Hopkins & Reuben W. Nowell & Damian W. Rivett & Timothy G. Barraclough & Thomas Bell, 2020. "Bacterial adaptation is constrained in complex communities," Nature Communications, Nature, vol. 11(1), pages 1-8, December.
    7. Ohad Manor & Chengzhen L. Dai & Sergey A. Kornilov & Brett Smith & Nathan D. Price & Jennifer C. Lovejoy & Sean M. Gibbons & Andrew T. Magis, 2020. "Health and disease markers correlate with gut microbiome composition across thousands of people," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    8. Liang Tian & Xu-Wen Wang & Ang-Kun Wu & Yuhang Fan & Jonathan Friedman & Amber Dahlin & Matthew K. Waldor & George M. Weinstock & Scott T. Weiss & Yang-Yu Liu, 2020. "Deciphering functional redundancy in the human microbiome," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    9. Kevin R. Foster & Jonas Schluter & Katharine Z. Coyte & Seth Rakoff-Nahoum, 2017. "The evolution of the host microbiome as an ecosystem on a leash," Nature, Nature, vol. 548(7665), pages 43-51, August.
    10. Benjamin H. Good & Michael J. McDonald & Jeffrey E. Barrick & Richard E. Lenski & Michael M. Desai, 2017. "The dynamics of molecular evolution over 60,000 generations," Nature, Nature, vol. 551(7678), pages 45-50, November.
    11. Benjamin A. Siranosian & Erin F. Brooks & Tessa Andermann & Andrew R. Rezvani & Niaz Banaei & Hua Tang & Ami S. Bhatt, 2022. "Rare transmission of commensal and pathogenic bacteria in the gut microbiome of hospitalized adults," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    12. Nittay Meroz & Nesli Tovi & Yael Sorokin & Jonathan Friedman, 2021. "Community composition of microbial microcosms follows simple assembly rules at evolutionary timescales," Nature Communications, Nature, vol. 12(1), pages 1-9, 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. Kerstin Thriene & Karin B. Michels, 2023. "Human Gut Microbiota Plasticity throughout the Life Course," IJERPH, MDPI, vol. 20(2), pages 1-14, January.
    2. Brian D. Huang & Thomas M. Groseclose & Corey J. Wilson, 2022. "Transcriptional programming in a Bacteroides consortium," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. N. Frazão & A. Konrad & M. Amicone & E. Seixas & D. Güleresi & M. Lässig & I. Gordo, 2022. "Two modes of evolution shape bacterial strain diversity in the mammalian gut for thousands of generations," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Sang Chul Park & Il-Ho Park & Joong Seob Lee & Sung Min Park & Sung Hun Kang & Seok-Min Hong & Soo-Hwan Byun & Yong Gi Jung & Seok Jin Hong, 2021. "Microbiome of Unilateral Chronic Rhinosinusitis: A Controlled Paired Analysis," IJERPH, MDPI, vol. 18(18), pages 1-16, September.
    5. Doris Vandeputte & Lindsey Commer & Raul Y. Tito & Gunter Kathagen & João Sabino & Séverine Vermeire & Karoline Faust & Jeroen Raes, 2021. "Temporal variability in quantitative human gut microbiome profiles and implications for clinical research," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    6. Louis J. Cohen & Sun M. Han & Pearson Lau & Daniela Guisado & Yupu Liang & Toshiki G. Nakashige & Thamina Ali & David Chiang & Adeeb Rahman & Sean F. Brady, 2022. "Unraveling function and diversity of bacterial lectins in the human microbiome," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Patrick A. Jonge & Koen Wortelboer & Torsten P. M. Scheithauer & Bert-Jan H. Born & Aeilko H. Zwinderman & Franklin L. Nobrega & Bas E. Dutilh & Max Nieuwdorp & Hilde Herrema, 2022. "Gut virome profiling identifies a widespread bacteriophage family associated with metabolic syndrome," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    8. Ying Liao & Yan-Xia Wu & Minzhong Tang & Yi-Wei Chen & Jin-Ru Xie & Yan Du & Tong-Min Wang & Yong-Qiao He & Wen-Qiong Xue & Xiao-Hui Zheng & Qiao-Yun Liu & Mei-Qi Zheng & Yi-Jing Jia & Xia-Ting Tong &, 2024. "Microbes translocation from oral cavity to nasopharyngeal carcinoma in patients," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Soo Hwan Byun & Sunki Lee & Sung Hun Kang & Hyo Geun Choi & Seok Jin Hong, 2020. "Cross-Sectional Analysis of the Association between Periodontitis and Cardiovascular Disease Using the Korean Genome and Epidemiology Study Data," IJERPH, MDPI, vol. 17(14), pages 1-12, July.
    10. John C. Boik, 2020. "Science-Driven Societal Transformation, Part I: Worldview," Sustainability, MDPI, vol. 12(17), pages 1-28, August.
    11. Serhii Aif & Nico Appold & Lucas Kampman & Oskar Hallatschek & Jona Kayser, 2022. "Evolutionary rescue of resistant mutants is governed by a balance between radial expansion and selection in compact populations," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    12. Zhaohui Cao & Wenlong Zuo & Lanxiang Wang & Junyu Chen & Zepeng Qu & Fan Jin & Lei Dai, 2023. "Spatial profiling of microbial communities by sequential FISH with error-robust encoding," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    13. Yadid M. Algavi & Elhanan Borenstein, 2023. "A data-driven approach for predicting the impact of drugs on the human microbiome," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    14. Connor Sharp & Kevin R. Foster, 2022. "Host control and the evolution of cooperation in host microbiomes," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    15. Barbara Emmenegger & Julien Massoni & Christine M. Pestalozzi & Miriam Bortfeld-Miller & Benjamin A. Maier & Julia A. Vorholt, 2023. "Identifying microbiota community patterns important for plant protection using synthetic communities and machine learning," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Yask Gupta & Anna Lara Ernst & Artem Vorobyev & Foteini Beltsiou & Detlef Zillikens & Katja Bieber & Simone Sanna-Cherchi & Angela M. Christiano & Christian D. Sadik & Ralf J. Ludwig & Tanya Sezin, 2023. "Impact of diet and host genetics on the murine intestinal mycobiome," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    17. Guy Amit & Amir Bashan, 2023. "Top-down identification of keystone taxa in the microbiome," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    18. Mingxing Wang & An-Hui Ge & Xingzhu Ma & Xiaolin Wang & Qiujin Xie & Like Wang & Xianwei Song & Mengchen Jiang & Weibing Yang & Jeremy D. Murray & Yayu Wang & Huan Liu & Xiaofeng Cao & Ertao Wang, 2024. "Dynamic root microbiome sustains soybean productivity under unbalanced fertilization," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Anna S. Weiss & Lisa S. Niedermeier & Alexandra von Strempel & Anna G. Burrichter & Diana Ring & Chen Meng & Karin Kleigrewe & Chiara Lincetto & Johannes Hübner & Bärbel Stecher, 2023. "Nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    20. Jing Liang & Jiafan Zhang & Zongmu Yao & Shouyang Luo & Lei Tian & Chunjie Tian & Yu Sun, 2022. "Preliminary Findings of Polypropylene Carbonate (PPC) Plastic Film Mulching Effects on the Soil Microbial Community," Agriculture, MDPI, vol. 12(3), pages 1-13, March.

    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:14:y:2023:i:1:d:10.1038_s41467-023-42769-3. 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.