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

Cornelia Jaspers, Sebastian Fraume, A. Elizabeth Arnold, J. David Miller, Thomas Bosch, Christian R. Voolstra*

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

185 Downloads (Pure)

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
JournalJournal of Zoology
Volume133
Pages (from-to)81-87
ISSN0952-8369
DOIs
Publication statusPublished - 2019

Keywords

  • Reductionism
  • Integrative approach
  • Holobiont
  • Adaptation
  • Model system
  • Model organism
  • Aiptasia
  • Hydra
  • Nematostella

Cite this

Jaspers, Cornelia ; Fraume, Sebastian ; Arnold, A. Elizabeth ; Miller, J. David ; Bosch, Thomas ; Voolstra, Christian R. . / Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches. In: Journal of Zoology. 2019 ; Vol. 133. pp. 81-87.
@article{62af31d5b65848daadc812bb523e5dce,
title = "Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches",
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.",
keywords = "Reductionism, Integrative approach, Holobiont, Adaptation, Model system, Model organism, Aiptasia, Hydra, Nematostella",
author = "Cornelia Jaspers and Sebastian Fraume and Arnold, {A. Elizabeth} and Miller, {J. David} and Thomas Bosch and Voolstra, {Christian R.}",
year = "2019",
doi = "10.1016/j.zool.2019.02.007",
language = "English",
volume = "133",
pages = "81--87",
journal = "Journal of Zoology",
issn = "0952-8369",
publisher = "Wiley-Blackwell",

}

Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches. / Jaspers, Cornelia; Fraume, Sebastian; Arnold, A. Elizabeth; Miller, J. David; Bosch, Thomas; Voolstra, Christian R. .

In: Journal of Zoology, Vol. 133, 2019, p. 81-87.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches

AU - Jaspers, Cornelia

AU - Fraume, Sebastian

AU - Arnold, A. Elizabeth

AU - Miller, J. David

AU - Bosch, Thomas

AU - Voolstra, Christian R.

PY - 2019

Y1 - 2019

N2 - 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.

AB - 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.

KW - Reductionism

KW - Integrative approach

KW - Holobiont

KW - Adaptation

KW - Model system

KW - Model organism

KW - Aiptasia

KW - Hydra

KW - Nematostella

U2 - 10.1016/j.zool.2019.02.007

DO - 10.1016/j.zool.2019.02.007

M3 - Journal article

VL - 133

SP - 81

EP - 87

JO - Journal of Zoology

JF - Journal of Zoology

SN - 0952-8369

ER -