Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes

Kevin R Theis¹, Nolwenn M Dheilly², Jonathan L Klassen³, Robert M Brucker⁴, John F Baines⁵, Thomas C G Bosch⁶, John F Cryan⁷, Scott F Gilbert⁸, Charles J Goodnight⁹, Elisabeth A Lloyd¹⁰, Jan Sapp¹¹, Philippe Vandenkoornhuyse¹², Ilana Zilber-Rosenberg¹³, Eugene Rosenberg¹⁴, Seth R Bordenstein¹⁵

Affiliations

¹ Department of Immunology and Microbiology, Wayne State University, Detroit, Michigan, USA; Wayne State University Perinatal Initiative, Detroit, Michigan, USA.
² School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York, USA.
³ Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USA.
⁴ The Rowland Institute at Harvard, Harvard University, Cambridge, Massachusetts, USA.
⁵ Max Planck Institute for Evolutionary Biology, Plön, Germany; Institute for Experimental Medicine, Christian Albrechts University of Kiel, Kiel, Germany.
⁶ Zoological Institute, Christian Albrechts University, Kiel, Germany.
⁷ Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland; APC Microbiome Institute, University College Cork, Cork, Ireland.
⁸ Department of Biology, Swarthmore College, Swarthmore, Pennsylvania, USA.
⁹ Department of Biology, University of Vermont, Burlington, Vermont, USA.
¹⁰ History and Philosophy of Science Department, Indiana University, Bloomington, Indiana, USA.
¹¹ Department of Biology, York University, Toronto, Ontario, Canada.
¹² Université de Rennes 1, CNRS, UMR6553 EcoBio, Rennes, France.
¹³ Independent Researcher, Givat Shmuel, Israel.
¹⁴ Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Tel Aviv, Israel.
¹⁵ Departments of Biological Sciences and Pathology, Microbiology and Immunology, Vanderbilt University, Nashville, Tennessee, USA.

PMID:27822520
PMCID: PMC5069740
DOI: 10.1128/mSystems.00028-16

Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes

Kevin R Theis et al. mSystems.2016.

.2016 Mar 29;1(2):e00028-16.

doi: 10.1128/mSystems.00028-16. eCollection 2016 Mar-Apr.

Authors

Affiliations

¹ Department of Immunology and Microbiology, Wayne State University, Detroit, Michigan, USA; Wayne State University Perinatal Initiative, Detroit, Michigan, USA.
² School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York, USA.
³ Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USA.
⁴ The Rowland Institute at Harvard, Harvard University, Cambridge, Massachusetts, USA.
⁵ Max Planck Institute for Evolutionary Biology, Plön, Germany; Institute for Experimental Medicine, Christian Albrechts University of Kiel, Kiel, Germany.
⁶ Zoological Institute, Christian Albrechts University, Kiel, Germany.
⁷ Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland; APC Microbiome Institute, University College Cork, Cork, Ireland.
⁸ Department of Biology, Swarthmore College, Swarthmore, Pennsylvania, USA.
⁹ Department of Biology, University of Vermont, Burlington, Vermont, USA.
¹⁰ History and Philosophy of Science Department, Indiana University, Bloomington, Indiana, USA.
¹¹ Department of Biology, York University, Toronto, Ontario, Canada.
¹² Université de Rennes 1, CNRS, UMR6553 EcoBio, Rennes, France.
¹³ Independent Researcher, Givat Shmuel, Israel.
¹⁴ Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Tel Aviv, Israel.
¹⁵ Departments of Biological Sciences and Pathology, Microbiology and Immunology, Vanderbilt University, Nashville, Tennessee, USA.

PMID:27822520
PMCID: PMC5069740
DOI: 10.1128/mSystems.00028-16

Abstract

Given the complexity of host-microbiota symbioses, scientists and philosophers are asking questions at new biological levels of hierarchical organization-what is a holobiont and hologenome? When should this vocabulary be applied? Are these concepts a null hypothesis for host-microbe systems or limited to a certain spectrum of symbiotic interactions such as host-microbial coevolution? Critical discourse is necessary in this nascent area, but productive discourse requires that skeptics and proponents use the same lexicon. For instance, critiquing the hologenome concept is not synonymous with critiquing coevolution, and arguing that an entity is not a primary unit of selection dismisses the fact that the hologenome concept has always embraced multilevel selection. Holobionts and hologenomes are incontrovertible, multipartite entities that result from ecological, evolutionary, and genetic processes at various levels. They are not restricted to one special process but constitute a wider vocabulary and framework for host biology in light of the microbiome.

Keywords: ecology; evolution; hologenome; microbiome.

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Figures

**FIG 1**
Holobionts are entities comprised of the host and all of its symbiotic microbes, including those which affect the holobiont’s phenotype and have coevolved with the host (blue), those which affect the holobiont’s phenotype but have not coevolved with the host (red), and those which do not affect the holobiont’s phenotype at all (gray). Microbes may be transmitted vertically or horizontally, may be acquired from the environment, and can be constant or inconstant in the host. Therefore, holobiont phenotypes can change in time and space as microbes come into and out of the holobiont. Microbes in the environment are not part of the holobiont (white). Hologenomes then encompass the genomes of the host and all of its microbes at any given time point, with individual genomes and genes falling into the same three functional categories of blue, red, and gray. Holobionts and hologenomes are entities, whereas coevolution or the evolution of host-symbiont interactions are processes.

See this image and copyright information in PMC

References

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1. Rosenberg E, Zilber-Rosenberg I. 2013. The hologenome concept: human, animal and plant microbiota. Springer, Basel, Switzerland.
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Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes

Affiliations

Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes

Authors

Affiliations

Abstract

Figures

References

LinkOut - more resources

Full Text Sources

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