Host-microbiota interactions: from holobiont theory to analysis

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Abstract

In the recent years, the holobiont concept has emerged as a theoretical and experimental framework to study the interactions between hosts and their associated microbial communities in all types of ecosystems. The spread of this concept in many branches of biology results from the fairly recent realization of the ubiquitous nature of host-associated microbes and their central role in host biology, ecology, and evolution. Through this special series “Host-microbiota interactions: from holobiont theory to analysis,” we wanted to promote this field of research which has considerable implications for human health, food production, and ecosystem protection. In this preface, we highlight a collection of articles selected for this special issue that show, use, or debate the concept of holobiont to approach taxonomically and ecologically diverse organisms, from humans and plants to sponges and insects. We also identify some theoretical and methodological challenges and propose directions for future research on holobionts.

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Structure, Function and Diversity of the Healthy Human Microbiome

Tatiana Vishnivetskaya, Jeroen Raes (2014)

Studies of the human microbiome have revealed that even healthy individuals differ remarkably in the microbes that occupy habitats such as the gut, skin, and vagina. Much of this diversity remains unexplained, although diet, environment, host genetics, and early microbial exposure have all been implicated. Accordingly, to characterize the ecology of human-associated microbial communities, the Human Microbiome Project has analyzed the largest cohort and set of distinct, clinically relevant body habitats to date. We found the diversity and abundance of each habitat’s signature microbes to vary widely even among healthy subjects, with strong niche specialization both within and among individuals. The project encountered an estimated 81–99% of the genera, enzyme families, and community configurations occupied by the healthy Western microbiome. Metagenomic carriage of metabolic pathways was stable among individuals despite variation in community structure, and ethnic/racial background proved to be one of the strongest associations of both pathways and microbes with clinical metadata. These results thus delineate the range of structural and functional configurations normal in the microbial communities of a healthy population, enabling future characterization of the epidemiology, ecology, and translational applications of the human microbiome.

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Animals in a bacterial world, a new imperative for the life sciences.

Margaret McFall-Ngai, Michael Hadfield, Thomas Bosch … (2013)

In the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal-bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other's genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal-bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world.

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The healthy human microbiome

Jason Lloyd-Price, Galeb Abu-Ali, Curtis Huttenhower (2016)

Humans are virtually identical in their genetic makeup, yet the small differences in our DNA give rise to tremendous phenotypic diversity across the human population. By contrast, the metagenome of the human microbiome—the total DNA content of microbes inhabiting our bodies—is quite a bit more variable, with only a third of its constituent genes found in a majority of healthy individuals. Understanding this variability in the “healthy microbiome” has thus been a major challenge in microbiome research, dating back at least to the 1960s, continuing through the Human Microbiome Project and beyond. Cataloguing the necessary and sufficient sets of microbiome features that support health, and the normal ranges of these features in healthy populations, is an essential first step to identifying and correcting microbial configurations that are implicated in disease. Toward this goal, several population-scale studies have documented the ranges and diversity of both taxonomic compositions and functional potentials normally observed in the microbiomes of healthy populations, along with possible driving factors such as geography, diet, and lifestyle. Here, we review several definitions of a ‘healthy microbiome’ that have emerged, the current understanding of the ranges of healthy microbial diversity, and gaps such as the characterization of molecular function and the development of ecological therapies to be addressed in the future.

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Contributors

Jean-Christophe Simon:

ORCID: http://orcid.org/0000-0003-0620-5835

jean-christophe.simon@inra.fr

Journal

Journal ID (nlm-ta): Microbiome

Journal ID (iso-abbrev): Microbiome

Title: Microbiome

Publisher: BioMed Central (London )

ISSN (Electronic): 2049-2618

Publication date (Electronic): 11 January 2019

Publication date PMC-release: 11 January 2019

Publication date Collection: 2019

Volume: 7

Electronic Location Identifier: 5

Affiliations

[1 ]ISNI 0000 0001 2191 9284, GRID grid.410368.8, UMR 1349, IGEPP (Institut de Génétique, Environnement et Protection des Plantes), INRA, Agrocampus Ouest, , Université Rennes 1, ; Domaine de la Motte, 35653 Le Rheu Cedex, France

[2 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, Centre for Digestive and Gut Health, , Imperial College London, ; London, W2 1NY UK

[3 ]ISNI 0000 0001 0807 5670, GRID grid.5600.3, School of Biosciences, , Cardiff University, ; Cardiff, CF10 3AX UK

[4 ]ISNI 0000 0001 2308 1657, GRID grid.462844.8, Muséum National d’Histoire Naturelle, Institut de Systématique, Évolution, Biodiversité, ISYEB-UMR 7205-CNRS, MNHN, UPMC, EPHE, , Sorbonne Universités, ; 57 Rue Cuvier-CP39, F-75005 Paris, France

[5 ]ISNI 0000 0001 2370 4076, GRID grid.8585.0, Faculty of Biology, , University of Gdansk, ; Ul. Wita Stwosza 59, 80-308 Gdansk, Poland

Author information

Jean-Christophe Simon http://orcid.org/0000-0003-0620-5835

Article

Publisher ID: 619

DOI: 10.1186/s40168-019-0619-4

PMC ID: 6330386

PubMed ID: 30635058

SO-VID: 1f19ecdb-817a-4f54-b4d4-bb2a91b4beb8

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Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 21 December 2018

Date accepted : 3 January 2019

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Keywords: host-microbiota interactions,holobiont,hologenome,metagenomics,symbiosis

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Keywords: host-microbiota interactions, holobiont, hologenome, metagenomics, symbiosis

Host-microbiota interactions: from holobiont theory to analysis

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Microbial Genomics

Most cited references 37

Structure, Function and Diversity of the Healthy Human Microbiome

Animals in a bacterial world, a new imperative for the life sciences.

The healthy human microbiome

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