Host-Microbe Coevolution Thesis


Host-Microbe Coevolution: Applying Evidence from Model Systems to Complex Marine Invertebrate Holobionts

Paul A. O’Brien,a,b,c Nicole S. Webster,b,c,d David J. Miller,e,f David G. Bourne,b,c

college of Science and Engineering, James Cook University, Townsville, QLD, Australia bAustralian Institute of Marine Science, Townsville, QLD, Australia cAIMS@JCU, Townsville, QLD, Australia dAustralian Centre for Ecogenomics, University of Queensland, Brisbane, QLD, Australia eARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, Australia fCentre for Tropical Bioinformatics and Molecular Biology, James Cook University, Townsville, QLD, Australia

ABSTRACT Marine invertebrates often host diverse microbial communities, making it difficult to identify important symbionts and to understand how these communities are structured. This complexity has also made it challenging to assign microbial functions and to unravel the myriad of interactions among the microbiota. Here we propose to address these issues by applying evidence from model systems of host- microbe coevolution to complex marine invertebrate microbiomes. Coevolution is the reciprocal adaptation of one lineage in response to another and can occur through the interaction of a host and its beneficial symbiont. A classic indicator of coevolution is codivergence of host and microbe, and evidence of this is found in both corals and sponges. Metabolic collaboration between host and microbe is of- ten linked to codivergence and appears likely in complex holobionts, where micro- bial symbionts can interact with host cells through production and degradation of metabolic compounds. Neutral models are also useful to distinguish selected mi- crobes against a background population consisting predominately of random associ- ates. Enhanced understanding of the interactions between marine invertebrates and their microbial communities is urgently required as coral reefs face unprecedented local and global pressures and as active restoration approaches, including manipula- tion of the microbiome, are proposed to improve the health and tolerance of reef species. On the basis of a detailed review of the literature, we propose three re- search criteria for examining coevolution in marine invertebrates: (i) identifying sto- chastic and deterministic components of the microbiome, (ii) assessing codivergence of host and microbe, and (iii) confirming the intimate association based on shared metabolic function.

KEYWORDS codivergence, coevolution, marine invertebrates, microbiome, phylosymbiosis

Coevolution theory dates back to the 19th century (box 1), and coevolution iscurrently referred to as the reciprocal evolution of one lineage in response to another (1). This definition encompasses a broad range of interactions such as predator- prey, host-symbiont, and host-parasite interactions or interactions among the members of a community of organisms such as a host and its associated microbiome (1, 2). In the case of host-microbe associations, this has produced some of the most remarkable evolutionary outcomes that have shaped life on Earth, such as the eukaryotic cell, multicellularity, and the development of organ systems (3, 4). It is now recognized that microbial associations with a multicellular host represent the rule rather than the

Citation O’Brien PA, Webster NS, Miller DJ, Bourne DG. 2019. Host-microbe coevolution: applying evidence from model systems to complex marine invertebrate holobionts. mBio 10:e02241-18. .02241-18.

Editor Danielle A. Garsin, University of Texas Health Science Center at Houston

Copyright © 2019 O’Brien et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

Address correspondence to David G. Bourne, [email protected].

Published 5 February 2019

MINIREVIEW Host-Microbe Biology


January/February 2019 Volume 10 Issue 1 e02241-18 ® 1

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