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

• Published in: Zoology (Jena) 2019-04, Vol.133, p.81-87
• Main Authors: Jaspers, Cornelia, Fraune, Sebastian, Arnold, A. Elizabeth, Miller, David J., Bosch, Thomas C.G., Voolstra, Christian R.
• Format: Article
• Language: English
• Subjects: Adaptation; Aiptasia; Animals; Holobiont; Hydra; Integrative approach; Microbiota; Model organism; Model system; Nematostella; Reductionism; Symbiosis
• ISSN: 0944-2006; 1873-2720
• DOI: 10.1016/j.zool.2019.02.007

•The metaorganism framework is a powerful new concept to help provide answers to longstanding biological questions.•The intricacy of metaorganisms requires a holistic framework using reductionist and integrative approaches for their study.•We provide a critical evaluation of perspectives and limitations relevant to studying organisms in a metaorganism framework.•Marker gene approaches are a first step in characterizing microbes but are not sufficient to establish functional relevance.•Controlled environments, microbial manipulation, and model systems can be used to elucidate function of microbes of metaorganisms. 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 struct