Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches

Cornelia Jaspers, Sebastian Fraune, A. Elizabeth Arnold, David J. Miller, Thomas C.G. Bosch, Christian R. Voolstra

Research output: Contribution to journalArticlepeer-review

43 Scopus citations

Abstract

Current research highlights the importance of associated microbes in contributing to the functioning, health, and even adaptation of their animal, plant, and fungal hosts. As such, we are witnessing a shift in research that moves away from focusing on the eukaryotic host sensu stricto to research into the complex conglomerate of the host and its associated microorganisms (i.e., microbial eukaryotes, archaea, bacteria, and viruses), the so-called metaorganism, as the biological entity. While recent research supports and encourages the adoption of such an integrative view, it must be understood that microorganisms are not involved in all host processes and not all associated microorganisms are functionally important. As such, our intention here is to provide a critical review and evaluation of perspectives and limitations relevant to studying organisms in a metaorganism framework and the functional toolbox available to do so. We note that marker gene-guided approaches that primarily characterize microbial diversity are a first step in delineating associated microbes but are not sufficient to establish proof of their functional relevance. More sophisticated tools and experiments are necessary to reveal the specific functions of associated microbes. This can be accomplished through the study of metaorganisms in less complex environments, the targeted manipulation of microbial associates, or work at the mechanistic level with the toolbox available in model systems. We conclude that the metaorganism framework is a powerful new concept to help provide answers to longstanding biological questions such as the evolution and ecology of organismal complexity and the importance of organismal symbioses to ecosystem functioning. The intricacy of the metaorganism requires a holistic framework combining reductionist and integrative approaches to resolve the structure and function of its member species and to disclose the various roles that microorganisms play in the biology of their hosts.
Original languageEnglish (US)
Pages (from-to)81-87
Number of pages7
JournalZoology
Volume133
DOIs
StatePublished - Mar 1 2019

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: This manuscript originated from discussions and conversations at the Boden Conference on Cnidarian Metaorganisms, March 11 to 14, 2018. We are deeply grateful to Nicholas J. Butterfield for contributing to many of the discussions and conceptual ideas that are outlined in this manuscript. We are grateful to the sponsors of the Boden Research Conferen Australian Academy of Science, Great Barrier Reef Foundation, Ian Potter Foundation, ARCCOE for Coral Reef Studies, and the Collaborative Research Centre (CRC 1182, funded through the German Research Foundation, DFG) “Origin and Function of Metaorganisms”. CRV acknowledges funding by the King Abdullah University of Science and Technology (KAUST); CJ, SF, and TCGB acknowledge support from the CRC 1182 “Origin and Function of Metaorganisms” funded through the DFG. TCGB acknowledges support from the Canadian Institute for Advanced Research (CIFAR). The figures were produced by Xavier Pita, scientific illustrator at King Abdullah University of Science and Technology (KAUST). The authors thank the two anonymous reviewers who contributed to the quality of the manuscript with their thoughts and suggestions.

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