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Cited by 1,240Gut microbiota and healthPhilosophy and History of ScienceInsect symbiosis and bacterial influences

Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes

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Bordenstein, Seth R., Theis, Kevin R.·2015·PLOS Biology
DOI 10.1371/journal.pbio.1002226PMC PMC4540581
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Abstract

Groundbreaking research on the universality and diversity of microorganisms is now challenging the life sciences to upgrade fundamental theories that once seemed untouchable. To fully appreciate the change that the field is now undergoing, one has to place the epochs and foundational principles of Darwin, Mendel, and the modern synthesis in light of the current advances that are enabling a new vision for the central importance of microbiology. Animals and plants are no longer heralded as autonomous entities but rather as biomolecular networks composed of the host plus its associated microbes, i.e., "holobionts." As such, their collective genomes forge a "hologenome," and models of animal and plant biology that do not account for these intergenomic associations are incomplete. Here, we integrate these concepts into historical and contemporary visions of biology and summarize a predictive and refutable framework for their evaluation. Specifically, we present ten principles that clarify and append what these concepts are and are not, explain how they both support and extend existing theory in the life sciences, and discuss their potential ramifications for the multifaceted approaches of zoology and botany. We anticipate that the conceptual and evidence-based foundation provided in this essay will serve as a roadmap for hypothesis-driven, experimentally validated research on holobionts and their hologenomes, thereby catalyzing the continued fusion of biology's subdisciplines. At a time when symbiotic microbes are recognized as fundamental to all aspects of animal and plant biology, the holobiont and hologenome concepts afford a holistic view of biological complexity that is consistent with the generally reductionist approaches of biology.

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  • Over time the microbiota has co-evolved with host organisms, becoming mutually co-dependent for survival.

    “Over time the microbiota has co-evolved with host organisms, becoming mutually co-dependent for survival (Bordenstein and Theis, 2015;Gaulke et al., 2018).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Bordenstein and Theis, 2015

    Box 2 discusses host–microbiota interactions as potential settings for coevolution, and section V describes obligate symbionts that supply nutrients to particular hosts. Neither passage establishes that microbiota and hosts generally became mutually dependent on each other for survival; the claim extends those specific or qualified points to all such relationships. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • The holobiont concept describes the ecological unit comprising both the host species and its symbiotic microbiota.

    “The concept of the holobiont has been developed to describe the ecological unit comprising both the host species and its symbiotic microbiota (Bordenstein and Theis, 2015;Shropshire and Bordenstein, 2016;Zilber-Rosenberg and Rosenberg, 2008).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Bordenstein and Theis, 2015

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Cited by

Sorted by citations

Authors
Bordenstein, S. R., & Theis, K. R.
Affiliations
  • Vanderbilt University (US)
  • University of Michigan (US)
Corresponding author
Bordenstein, Seth R.
ORCID
Venue
PLOS Biology
Publisher
Public Library of Science (PLoS)
Published
2015-08-18
Volume
13
Issue
8
Pages
e1002226
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
DOI
10.1371/journal.pbio.1002226
PMC
PMC4540581
OpenAlex
W1951069276
Cited by
1,240
References
8
Citations by year
2026: 96 · 2025: 90 · 2024: 122 · 2023: 119 · 2022: 117 · 2021: 144 · 2020: 131 · 2019: 103 · 2018: 124 · 2017: 101 · 2016: 83 · 2015: 6 · 2013: 1
FWCI
45.47
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Science Foundation (0939454, 0920505, 1456778, 1046149)
  • National Institute of Diabetes and Digestive and Kidney Diseases (P30DK058404)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy and History of Science
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
Keywords
holobiont, hologenome, host-microbe symbiosis, microbiome, host biology, microbial diversity, history of biology, Modern Synthesis, reductionism
MeSH terms
Animals, Biological Evolution, Humans, Mutation, Plants, Selection, Genetic, Symbiosis, Metagenome, Microbiota

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