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

Consortium Australian Acad Sci Bod

Research output: Contribution to journalReview article

1 Citation (Scopus)

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
Pages (from-to)81-87
Number of pages7
JournalZoology
Volume133
DOIs
Publication statusPublished - Apr 2019

Cite this

@article{59dcb61e26b84fc38c56657874151e97,
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, MICROBE INTERACTIONS, ANEMONE MODEL, CORAL, BACTERIA, METAMORPHOSIS, ORGANISMS, DIVERSITY, AIPTASIA, HOST, SEA",
author = "{Consortium Australian Acad Sci Bod} and Cornelia Jaspers and Sebastian Fraune and Arnold, {A. Elizabeth} and Miller, {David J.} and Bosch, {Thomas C. G.} and Voolstra, {Christian R.} and Maja Adamska and Tracy Ainsworth and Eldon Ball and Chloe Boote and David Bourne and Butterfield, {Nicholas J.} and Chan, {Cheong Xin} and Ira Cooke and Cowman, {Peter F.} and Aaron Darling and Davy, {Simon K.} and Amin Mohamed and Katharina Fabricius and Sofia Fortunato and Alejandra Hernandez and Mia Hoogenboom and Aurelie Moya and Lucia Pita and Ragan, {Mark A.} and Robbins, {Steven J.} and Andrade, {Natalia R.} and Kazuhiro Sakamaki and Verena Schoepf and Thorsten Seemann and Chuya Shinzato and Jaroslaw Stolarski and Jan Strugnell and Shunichi Takahashi and Sen-Lin Tang and Nicole Webster and Brooke Whitelaw and Hua Ying",
year = "2019",
month = "4",
doi = "10.1016/j.zool.2019.02.007",
language = "English",
volume = "133",
pages = "81--87",
journal = "Zoology",
issn = "0944-2006",
publisher = "Urban und Fischer Verlag Jena",

}

Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches. / Consortium Australian Acad Sci Bod.

In: Zoology, Vol. 133, 04.2019, p. 81-87.

Research output: Contribution to journalReview article

TY - JOUR

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

AU - Consortium Australian Acad Sci Bod

AU - Jaspers, Cornelia

AU - Fraune, Sebastian

AU - Arnold, A. Elizabeth

AU - Miller, David J.

AU - Bosch, Thomas C. G.

AU - Voolstra, Christian R.

AU - Adamska, Maja

AU - Ainsworth, Tracy

AU - Ball, Eldon

AU - Boote, Chloe

AU - Bourne, David

AU - Butterfield, Nicholas J.

AU - Chan, Cheong Xin

AU - Cooke, Ira

AU - Cowman, Peter F.

AU - Darling, Aaron

AU - Davy, Simon K.

AU - Mohamed, Amin

AU - Fabricius, Katharina

AU - Fortunato, Sofia

AU - Hernandez, Alejandra

AU - Hoogenboom, Mia

AU - Moya, Aurelie

AU - Pita, Lucia

AU - Ragan, Mark A.

AU - Robbins, Steven J.

AU - Andrade, Natalia R.

AU - Sakamaki, Kazuhiro

AU - Schoepf, Verena

AU - Seemann, Thorsten

AU - Shinzato, Chuya

AU - Stolarski, Jaroslaw

AU - Strugnell, Jan

AU - Takahashi, Shunichi

AU - Tang, Sen-Lin

AU - Webster, Nicole

AU - Whitelaw, Brooke

AU - Ying, Hua

PY - 2019/4

Y1 - 2019/4

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

KW - MICROBE INTERACTIONS

KW - ANEMONE MODEL

KW - CORAL

KW - BACTERIA

KW - METAMORPHOSIS

KW - ORGANISMS

KW - DIVERSITY

KW - AIPTASIA

KW - HOST

KW - SEA

U2 - 10.1016/j.zool.2019.02.007

DO - 10.1016/j.zool.2019.02.007

M3 - Review article

VL - 133

SP - 81

EP - 87

JO - Zoology

JF - Zoology

SN - 0944-2006

ER -