IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0008584.html
   My bibliography  Save this article

Site and Strain-Specific Variation in Gut Microbiota Profiles and Metabolism in Experimental Mice

Author

Listed:
  • Melissa K Friswell
  • Helen Gika
  • Ian J Stratford
  • Georgios Theodoridis
  • Brian Telfer
  • Ian D Wilson
  • Andrew J McBain

Abstract

Background: The gastrointestinal tract microbiota (GTM) of mammals is a complex microbial consortium, the composition and activities of which influences mucosal development, immunity, nutrition and drug metabolism. It remains unclear whether the composition of the dominant GTM is conserved within animals of the same strain and whether stable GTMs are selected for by host-specific factors or dictated by environmental variables. Methodology/Principal Findings: The GTM composition of six highly inbred, genetically distinct strains of mouse (C3H, C57, GFEC, CD1, CBA nu/nu and SCID) was profiled using eubacterial –specific PCR-DGGE and quantitative PCR of feces. Animals exhibited strain-specific fecal eubacterial profiles that were highly stable (c. >95% concordance over 26 months for C57). Analyses of mice that had been relocated before and after maturity indicated marked, reproducible changes in fecal consortia and that occurred only in young animals. Implantation of a female BDF1 mouse with genetically distinct (C57 and Agoutie) embryos produced highly similar GTM profiles (c. 95% concordance) between mother and offspring, regardless of offspring strain, which was also reflected in urinary metabolite profiles. Marked institution-specific GTM profiles were apparent in C3H mice raised in two different research institutions. Conclusion/Significance: Strain-specific data were suggestive of genetic determination of the composition and activities of intestinal symbiotic consortia. However, relocation studies and uterine implantation demonstrated the dominance of environmental influences on the GTM. This was manifested in large variations between isogenic adult mice reared in different research institutions.

Suggested Citation

  • Melissa K Friswell & Helen Gika & Ian J Stratford & Georgios Theodoridis & Brian Telfer & Ian D Wilson & Andrew J McBain, 2010. "Site and Strain-Specific Variation in Gut Microbiota Profiles and Metabolism in Experimental Mice," PLOS ONE, Public Library of Science, vol. 5(1), pages 1-9, January.
  • Handle: RePEc:plo:pone00:0008584
    DOI: 10.1371/journal.pone.0008584
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0008584
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0008584&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0008584?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. Peter J. Turnbaugh & Ruth E. Ley & Michael A. Mahowald & Vincent Magrini & Elaine R. Mardis & Jeffrey I. Gordon, 2006. "An obesity-associated gut microbiome with increased capacity for energy harvest," Nature, Nature, vol. 444(7122), pages 1027-1031, December.
    2. T. Andrew Clayton & John C. Lindon & Olivier Cloarec & Henrik Antti & Claude Charuel & Gilles Hanton & Jean-Pierre Provost & Jean-Loïc Le Net & David Baker & Rosalind J. Walley & Jeremy R. Everett & J, 2006. "Pharmaco-metabonomic phenotyping and personalized drug treatment," Nature, Nature, vol. 440(7087), pages 1073-1077, April.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Aaron C Ericsson & J Wade Davis & William Spollen & Nathan Bivens & Scott Givan & Catherine E Hagan & Mark McIntosh & Craig L Franklin, 2015. "Effects of Vendor and Genetic Background on the Composition of the Fecal Microbiota of Inbred Mice," PLOS ONE, Public Library of Science, vol. 10(2), pages 1-19, February.
    2. Hannah Lees & Jonathan Swann & Simon M Poucher & Jeremy K Nicholson & Elaine Holmes & Ian D Wilson & Julian R Marchesi, 2014. "Age and Microenvironment Outweigh Genetic Influence on the Zucker Rat Microbiome," PLOS ONE, Public Library of Science, vol. 9(9), pages 1-11, September.
    3. Camilla Hartmann Friis Hansen & Dennis Sandris Nielsen & Miloslav Kverka & Zuzana Zakostelska & Klara Klimesova & Tomas Hudcovic & Helena Tlaskalova-Hogenova & Axel Kornerup Hansen, 2012. "Patterns of Early Gut Colonization Shape Future Immune Responses of the Host," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-7, March.
    4. Willie A Bidot & Aaron C Ericsson & Craig L Franklin, 2018. "Effects of water decontamination methods and bedding material on the gut microbiota," PLOS ONE, Public Library of Science, vol. 13(10), pages 1-16, October.

    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. Shinji Fukuda & Yumiko Nakanishi & Eisuke Chikayama & Hiroshi Ohno & Tsuneo Hino & Jun Kikuchi, 2009. "Evaluation and Characterization of Bacterial Metabolic Dynamics with a Novel Profiling Technique, Real-Time Metabolotyping," PLOS ONE, Public Library of Science, vol. 4(3), pages 1-10, March.
    2. Doratha A Byrd & Jun Chen & Emily Vogtmann & Autumn Hullings & Se Jin Song & Amnon Amir & Muhammad G Kibriya & Habibul Ahsan & Yu Chen & Heidi Nelson & Rob Knight & Jianxin Shi & Nicholas Chia & Rashm, 2019. "Reproducibility, stability, and accuracy of microbial profiles by fecal sample collection method in three distinct populations," PLOS ONE, Public Library of Science, vol. 14(11), pages 1-19, November.
    3. Kiran Konain & Sadia & Turfa Nadeem & Adeed Khan & Warda Iqbal & Arsalan & Amir Javed & Ruby Khan & Kainat Jamil & Kainat Jamil, 2018. "Importance of Probiotics in Gastrointestinal Tract," Journal of Asian Scientific Research, Asian Economic and Social Society, vol. 8(3), pages 128-143, March.
    4. Marjolein Heddes & Baraa Altaha & Yunhui Niu & Sandra Reitmeier & Karin Kleigrewe & Dirk Haller & Silke Kiessling, 2022. "The intestinal clock drives the microbiome to maintain gastrointestinal homeostasis," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Hanafi, Mohamed & Ouertani, Samia Samar & Boccard, Julien & Mazerolles, Gérard & Rudaz, Serge, 2015. "Multi-way PLS regression: Monotony convergence of tri-linear PLS2 and optimality of parameters," Computational Statistics & Data Analysis, Elsevier, vol. 83(C), pages 129-139.
    6. Hui Xia & Beijia Zhou & Jing Sui & Wenqing Ma & Shaokang Wang & Ligang Yang & Guiju Sun, 2022. "Lycium barbarum Polysaccharide Regulates the Lipid Metabolism and Alters Gut Microbiota in High-Fat Diet Induced Obese Mice," IJERPH, MDPI, vol. 19(19), pages 1-12, September.
    7. Davillas, Apostolos & Pudney, Stephen, 2016. "Concordance of health states in couples. Analysis of self-reported, nurse administered and blood-based biomarker data in Understanding Society," ISER Working Paper Series 2016-15, Institute for Social and Economic Research.
    8. Vinod Nikhra, 2019. "Therapeutic Potential of Gut Microbiome Manipulation: Concepts in Fecal Microbiota Transplantation," Current Research in Diabetes & Obesity Journal, Juniper Publishers Inc., vol. 11(1), pages 1-9, June.
    9. Cristiane R. S. Câmara & Carlos A. Urrea & Vicki Schlegel, 2013. "Pinto Beans ( Phaseolus vulgaris L.) as a Functional Food: Implications on Human Health," Agriculture, MDPI, vol. 3(1), pages 1-22, February.
    10. Vinod Nikhra, 2019. "The Novel Dimensions of Cardio-Metabolic Health Gut Microbiota, Dysbiosis and its Fallouts," Current Research in Diabetes & Obesity Journal, Juniper Publishers Inc., vol. 11(1), pages 28-37, June.
    11. James Robert White & Niranjan Nagarajan & Mihai Pop, 2009. "Statistical Methods for Detecting Differentially Abundant Features in Clinical Metagenomic Samples," PLOS Computational Biology, Public Library of Science, vol. 5(4), pages 1-11, April.
    12. Zemin Zheng & Jinchi Lv & Wei Lin, 2021. "Nonsparse Learning with Latent Variables," Operations Research, INFORMS, vol. 69(1), pages 346-359, January.
    13. Karen D. Corbin & Elvis A. Carnero & Blake Dirks & Daria Igudesman & Fanchao Yi & Andrew Marcus & Taylor L. Davis & Richard E. Pratley & Bruce E. Rittmann & Rosa Krajmalnik-Brown & Steven R. Smith, 2023. "Host-diet-gut microbiome interactions influence human energy balance: a randomized clinical trial," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. Michael DiMarzio & Brigida Rusconi & Neela H Yennawar & Mark Eppinger & Andrew D Patterson & Edward G Dudley, 2017. "Identification of a mouse Lactobacillus johnsonii strain with deconjugase activity against the FXR antagonist T-β-MCA," PLOS ONE, Public Library of Science, vol. 12(9), pages 1-15, September.
    15. Hanan H. Wahid & Ayesha Bahez & Mohammed I. A. Mustafa Mahmud & Farih N. Hashim & Norhidayah Kamarudin & Roesnita Baharuddin & Ahmad M. Ahmad Mustafa & Hamizah Ismail, 2022. "Maternal Risk Factors For Group B Streptococcus (Gbs) Vaginal Colonization," Acta Scientifica Malaysia (ASM), Zibeline International Publishing, vol. 6(2), pages 55-58, August.
    16. Tamar Ringel-Kulka & Jing Cheng & Yehuda Ringel & Jarkko Salojärvi & Ian Carroll & Airi Palva & Willem M de Vos & Reetta Satokari, 2013. "Intestinal Microbiota in Healthy U.S. Young Children and Adults—A High Throughput Microarray Analysis," PLOS ONE, Public Library of Science, vol. 8(5), pages 1-10, May.
    17. Hannah Lees & Jonathan Swann & Simon M Poucher & Jeremy K Nicholson & Elaine Holmes & Ian D Wilson & Julian R Marchesi, 2014. "Age and Microenvironment Outweigh Genetic Influence on the Zucker Rat Microbiome," PLOS ONE, Public Library of Science, vol. 9(9), pages 1-11, September.
    18. 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.
    19. Liat Shenhav & Ori Furman & Leah Briscoe & Mike Thompson & Justin D Silverman & Itzhak Mizrahi & Eran Halperin, 2019. "Modeling the temporal dynamics of the gut microbial community in adults and infants," PLOS Computational Biology, Public Library of Science, vol. 15(6), pages 1-21, June.
    20. Isaac G. Crusoe & Ian C. Chiwaya & Tasnim I. Habib, 2024. "Immune Control of Gut Microbiota Prevents Obesity and the Effect of Antibiotic on Microbial Population," International Journal of Research and Scientific Innovation, International Journal of Research and Scientific Innovation (IJRSI), vol. 11(5), pages 1-9, May.

    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:plo:pone00:0008584. 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: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    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.