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Disentangling host–microbiota complexity through hologenomics

Nature Reviews Genetics volume 23, pages 281–297 (2022)Cite this article

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Abstract

Research on animal–microbiota interactions has become a central topic in biological sciences because of its relevance to basic eco-evolutionary processes and applied questions in agriculture and health. However, animal hosts and their associated microbial communities are still seldom studied in a systemic fashion. Hologenomics, the integrated study of the genetic features of a eukaryotic host alongside that of its associated microbes, is becoming a feasible — yet still underexploited — approach that overcomes this limitation. Acknowledging the biological and genetic properties of both hosts and microbes, along with the advantages and disadvantages of implemented techniques, is essential for designing optimal studies that enable some of the major questions in biology to be addressed.

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Fig. 1: Diversity and ecological relevance of host–microbiota systems.
Fig. 2: Overview of the five essential criteria for designing and interpreting hologenomic studies.
Fig. 3: Decomposition of hologenomic complexity.
Fig. 4: Hologenomic complexity of study systems.
Fig. 5: Examples of biological processes addressed by the different models of host–microbiota interactions.
Fig. 6: Decomposition of hologenomic complexity and its impact on results.

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Acknowledgements

The authors thank the Danish National Research Foundation award DNRF143 ‘A Center for Evolutionary Hologenomics’ for funding their research. A.A. acknowledges Lundbeckfonden grant R250-2017-1351. A.A., M.T.L. and M.T.P.G. were supported by the European Union (H2020-SFS-2018-1 project HoloFood-817729). M.T.L. and M.T.P.G. acknowledge the FHF (Norwegian Seafood Research Fund; “HoloFish”, grant No. 901436). S.B.A. acknowledges Lundbeckfonden Fellowship R335-2019-1513 ‘Understanding the Health Effects of Microbial Interactions’ and Independent Research Council Denmark Sapere Aude grant 9064-00029B ‘Understanding the Effects of Microbial Interactions on Host Health’.

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Authors and Affiliations

  1. Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark

    Antton Alberdi, Sandra B. Andersen, Morten T. Limborg, Robert R. Dunn & M. Thomas P. Gilbert

  2. Department of Applied Ecology, North Carolina State University, Raleigh, NC, USA

    Robert R. Dunn

  3. University Museum, Norwegian University of Science and Technology (NTNU), Trondheim, Norway

    M. Thomas P. Gilbert

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A.A. researched data for the article. All authors made substantial contributions to discussions of the content and writing the article and reviewed and/or edited the manuscript before submission.

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Glossary

Metagenotype

The specific state of the microbial metagenome characterized at a particular moment and at a given resolution.

Hologenotype

The entire genetic constitution of an individual eukaryotic organism and its associated microorganisms characterized at a given moment and at a given resolution.

Metagenome-assembled genomes

(MAGs). Partial or semi-complete draft bacterial genomes reconstructed through metagenomic assembly and binning from samples containing mixtures of microbial taxa.

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Alberdi, A., Andersen, S.B., Limborg, M.T. et al. Disentangling host–microbiota complexity through hologenomics. Nat Rev Genet 23, 281–297 (2022). https://doi.org/10.1038/s41576-021-00421-0

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