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

There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

Abstract

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.

Related collections

Most cited references 18

Record: found
Abstract: found
Article: not found

Engineering Microbiomes to Improve Plant and Animal Health.

C Mueller, J Sachs (2015)

Animal and plant microbiomes encompass diverse microbial communities that colonize every accessible host tissue. These microbiomes enhance host functions, contributing to host health and fitness. A novel approach to improve animal and plant fitness is to artificially select upon microbiomes, thus engineering evolved microbiomes with specific effects on host fitness. We call this engineering approach host-mediated microbiome selection, because this method selects upon microbial communities indirectly through the host and leverages host traits that evolved to influence microbiomes. In essence, host phenotypes are used as probes to gauge and manipulate those microbiome functions that impact host fitness. To facilitate research on host-mediated microbiome engineering, we explain and compare the principal methods to impose artificial selection on microbiomes; discuss advantages and potential challenges of each method; offer a skeptical appraisal of each method in light of these potential challenges; and outline experimental strategies to optimize microbiome engineering. Finally, we develop a predictive framework for microbiome engineering that organizes research around principles of artificial selection, quantitative genetics, and microbial community-ecology.

0 comments Cited 213 times – based on 0 reviews      Review now

Bookmark

Record: found
Abstract: found
Article: not found

The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia.

Robert M. Brucker, Seth Bordenstein (2013)

Although the gut microbiome influences numerous aspects of organismal fitness, its role in animal evolution and the origin of new species is largely unknown. Here we present evidence that beneficial bacterial communities in the guts of closely related species of the genus Nasonia form species-specific phylosymbiotic assemblages that cause lethality in interspecific hybrids. Bacterial constituents and abundance are irregular in hybrids relative to parental controls, and antibiotic curing of the gut bacteria significantly rescues hybrid survival. Moreover, feeding bacteria to germ-free hybrids reinstates lethality and recapitulates the expression of innate immune genes observed in conventionally reared hybrids. We conclude that in this animal complex, the gut microbiome and host genome represent a coadapted "hologenome" that breaks down during hybridization, promoting hybrid lethality and assisting speciation.

0 comments Cited 173 times – based on 0 reviews      Review now

Bookmark

Record: found
Abstract: found
Article: not found

Metaorganisms as the new frontier.

Thomas Bosch, Margaret J. McFall-Ngai (2011)

Because it appears that almost all organisms are part of an interdependent metaorganism, an understanding of the underlying host-microbe species associations, and of evolution and molecular underpinnings, has become the new frontier in zoology. The availability of novel high-throughput sequencing methods, together with the conceptual understanding that advances mostly originate at the intersection of traditional disciplinary boundaries, enable biologists to dissect the mechanisms that control the interdependent associations of species. In this review article, we outline some of the issues in inter-species interactions, present two case studies illuminating the necessity of interfacial research when addressing complex and fundamental zoological problems, and show that an interdisciplinary approach that seeks to understand co-evolved multi-species relationships will connect genomes, phenotypes, ecosystems and the evolutionary forces that have shaped them. We hope that this article inspires other collaborations of a similar nature on the diverse landscape commonly referred to as "zoology". Copyright © 2011 Elsevier GmbH. All rights reserved.

0 comments Cited 156 times – based on 0 reviews      Review now

Bookmark

All references

Author and article information

Contributors

Jack A. Gilbert: Role: Editor

Journal

Journal ID (nlm-ta): mSystems

Journal ID (iso-abbrev): mSystems

Journal ID (hwp): msys

Journal ID (pmc): msys

Journal ID (publisher-id): mSystems

Title: mSystems

Publisher: American Society for Microbiology (1752 N St., N.W., Washington, DC )

ISSN (Electronic): 2379-5077

Publication date (Electronic): 29 March 2016

Publication date Collection: Mar-Apr 2016

Volume: 1

Issue: 2

Electronic Location Identifier: e00028-16

Affiliations

[a ]Department of Immunology and Microbiology, Wayne State University, Detroit, Michigan, USA

[b ]Wayne State University Perinatal Initiative, Detroit, Michigan, USA

[c ]School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York, USA

[d ]Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USA

[e ]The Rowland Institute at Harvard, Harvard University, Cambridge, Massachusetts, USA

[f ]Max Planck Institute for Evolutionary Biology, Plön, Germany

[g ]Institute for Experimental Medicine, Christian Albrechts University of Kiel, Kiel, Germany

[h ]Zoological Institute, Christian Albrechts University, Kiel, Germany

[i ]Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland

[j ]APC Microbiome Institute, University College Cork, Cork, Ireland

[k ]Department of Biology, Swarthmore College, Swarthmore, Pennsylvania, USA

[l ]Department of Biology, University of Vermont, Burlington, Vermont, USA

[m ]History and Philosophy of Science Department, Indiana University, Bloomington, Indiana, USA

[n ]Department of Biology, York University, Toronto, Ontario, Canada

[o ]Université de Rennes 1, CNRS, UMR6553 EcoBio, Rennes, France

[p ]Independent Researcher, Givat Shmuel, Israel

[q ]Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Tel Aviv, Israel

[r ]Departments of Biological Sciences and Pathology, Microbiology and Immunology, Vanderbilt University, Nashville, Tennessee, USA

Argonne National Laboratory

Author notes

Address correspondence to Kevin R. Theis, ktheis@ 123456med.wayne.edu , or Seth R. Bordenstein, s.bordenstein@ 123456vanderbilt.edu .

Citation Theis KR, Dheilly NM, Klassen JL, Brucker RM, Baines JF, Bosch TCG, Cryan JF, Gilbert SF, Goodnight CJ, Lloyd EA, Sapp J, Vandenkoornhuyse P, Zilber-Rosenberg I, Rosenberg E, Bordenstein SR. 2016. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1(2):e00028-16. doi: 10.1128/mSystems.00028-16.