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A 3-dimensional mathematical model of microbial proliferation that generates the characteristic cumulative relative abundance distributions in gut microbiomes

Author

Listed:
  • Lena Takayasu
  • Wataru Suda
  • Eiichiro Watanabe
  • Shinji Fukuda
  • Kageyasu Takanashi
  • Hiroshi Ohno
  • Misako Takayasu
  • Hideki Takayasu
  • Masahira Hattori

Abstract

The gut microbiome is highly variable among individuals, largely due to differences in host lifestyle and physiology. However, little is known about the underlying processes or rules that shape the complex microbial community. In this paper, we show that the cumulative relative abundance distribution (CRAD) of microbial species can be approximated by a power law function, and found that the power exponent of CRADs generated from 16S rRNA gene and metagenomic data for normal gut microbiomes of humans and mice was similar consistently with ∼0.9. A similarly robust power exponent was observed in CRADs of gut microbiomes during dietary interventions and several diseases. However, the power exponent was found to be ∼0.6 in CRADs from gut microbiomes characterized by lower species richness, such as those of human infants and the small intestine of mice. In addition, the CRAD of gut microbiomes of mice treated with antibiotics differed slightly from those of infants and the small intestines of mice. Based on these observations, in addition to data on the spatial distribution of microbes in the digestive tract, we developed a 3-dimensional mathematical model of microbial proliferation that reproduced the experimentally observed CRAD patterns. Our model indicated that the CRAD may be determined by the ratio of emerging to pre-existing species during non-uniform spatially competitive proliferation, independent of species composition.

Suggested Citation

  • Lena Takayasu & Wataru Suda & Eiichiro Watanabe & Shinji Fukuda & Kageyasu Takanashi & Hiroshi Ohno & Misako Takayasu & Hideki Takayasu & Masahira Hattori, 2017. "A 3-dimensional mathematical model of microbial proliferation that generates the characteristic cumulative relative abundance distributions in gut microbiomes," PLOS ONE, Public Library of Science, vol. 12(8), pages 1-20, August.
    • Handle: RePEc:plo:pone00:0180863
    DOI: 10.1371/journal.pone.0180863
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    1. Lawrence A. David & Corinne F. Maurice & Rachel N. Carmody & David B. Gootenberg & Julie E. Button & Benjamin E. Wolfe & Alisha V. Ling & A. Sloan Devlin & Yug Varma & Michael A. Fischbach & Sudha B. , 2014. "Diet rapidly and reproducibly alters the human gut microbiome," Nature, Nature, vol. 505(7484), pages 559-563, January.
    2. Aurélie Cotillard & Sean P. Kennedy & Ling Chun Kong & Edi Prifti & Nicolas Pons & Emmanuelle Le Chatelier & Mathieu Almeida & Benoit Quinquis & Florence Levenez & Nathalie Galleron & Sophie Gougis & , 2013. "Dietary intervention impact on gut microbial gene richness," Nature, Nature, vol. 500(7464), pages 585-588, August.
    3. Amir Bashan & Travis E. Gibson & Jonathan Friedman & Vincent J. Carey & Scott T. Weiss & Elizabeth L. Hohmann & Yang-Yu Liu, 2016. "Universality of human microbial dynamics," Nature, Nature, vol. 534(7606), pages 259-262, June.
    4. Peter J. Turnbaugh & Ruth E. Ley & Micah Hamady & Claire M. Fraser-Liggett & Rob Knight & Jeffrey I. Gordon, 2007. "The Human Microbiome Project," Nature, Nature, vol. 449(7164), pages 804-810, October.
    5. Fredrik H. Karlsson & Valentina Tremaroli & Intawat Nookaew & Göran Bergström & Carl Johan Behre & Björn Fagerberg & Jens Nielsen & Fredrik Bäckhed, 2013. "Gut metagenome in European women with normal, impaired and diabetic glucose control," Nature, Nature, vol. 498(7452), pages 99-103, June.
    6. Les Dethlefsen & Sue Huse & Mitchell L Sogin & David A Relman, 2008. "The Pervasive Effects of an Antibiotic on the Human Gut Microbiota, as Revealed by Deep 16S rRNA Sequencing," PLOS Biology, Public Library of Science, vol. 6(11), pages 1-18, November.
    7. Peter J. Turnbaugh & Micah Hamady & Tanya Yatsunenko & Brandi L. Cantarel & Alexis Duncan & Ruth E. Ley & Mitchell L. Sogin & William J. Jones & Bruce A. Roe & Jason P. Affourtit & Michael Egholm & Be, 2009. "A core gut microbiome in obese and lean twins," Nature, Nature, vol. 457(7228), pages 480-484, January.
    8. Igor Volkov & Jayanth R. Banavar & Stephen P. Hubbell & Amos Maritan, 2007. "Patterns of relative species abundance in rainforests and coral reefs," Nature, Nature, vol. 450(7166), pages 45-49, November.
    9. Tanya Yatsunenko & Federico E. Rey & Mark J. Manary & Indi Trehan & Maria Gloria Dominguez-Bello & Monica Contreras & Magda Magris & Glida Hidalgo & Robert N. Baldassano & Andrey P. Anokhin & Andrew C, 2012. "Human gut microbiome viewed across age and geography," Nature, Nature, vol. 486(7402), pages 222-227, June.
    10. Catherine A. Lozupone & Jesse I. Stombaugh & Jeffrey I. Gordon & Janet K. Jansson & Rob Knight, 2012. "Diversity, stability and resilience of the human gut microbiota," Nature, Nature, vol. 489(7415), pages 220-230, September.
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