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      Microbial contributions to the persistence of coral reefs

      1 , 2 , * , 3

      The ISME Journal

      Nature Publishing Group

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          Abstract

          On contemplating the adaptive capacity of reef organisms to a rapidly changing environment, the microbiome offers significant and greatly unrecognised potential. Microbial symbionts contribute to the physiology, development, immunity and behaviour of their hosts, and can respond very rapidly to changing environmental conditions, providing a powerful mechanism for acclimatisation and also possibly rapid evolution of coral reef holobionts. Environmentally acquired fluctuations in the microbiome can have significant functional consequences for the holobiont phenotype upon which selection can act. Environmentally induced changes in microbial abundance may be analogous to host gene duplication, symbiont switching / shuffling as a result of environmental change can either remove or introduce raw genetic material into the holobiont; and horizontal gene transfer can facilitate rapid evolution within microbial strains. Vertical transmission of symbionts is a key feature of many reef holobionts and this would enable environmentally acquired microbial traits to be faithfully passed to future generations, ultimately facilitating microbiome-mediated transgenerational acclimatisation (MMTA) and potentially even adaptation of reef species in a rapidly changing climate. In this commentary, we highlight the capacity and mechanisms for MMTA in reef species, propose a modified Price equation as a framework for assessing MMTA and recommend future areas of research to better understand how microorganisms contribute to the transgenerational acclimatisation of reef organisms, which is essential if we are to reliably predict the consequences of global change for reef ecosystems.

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          Most cited references 26

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          Mechanisms of reef coral resistance to future climate change.

          Reef corals are highly sensitive to heat, yet populations resistant to climate change have recently been identified. To determine the mechanisms of temperature tolerance, we reciprocally transplanted corals between reef sites experiencing distinct temperature regimes and tested subsequent physiological and gene expression profiles. Local acclimatization and fixed effects, such as adaptation, contributed about equally to heat tolerance and are reflected in patterns of gene expression. In less than 2 years, acclimatization achieves the same heat tolerance that we would expect from strong natural selection over many generations for these long-lived organisms. Our results show both short-term acclimatory and longer-term adaptive acquisition of climate resistance. Adding these adaptive abilities to ecosystem models is likely to slow predictions of demise for coral reef ecosystems.
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            The human gut microbiome: ecology and recent evolutionary changes.

            The human gastrointestinal tract is divided into sections, allowing digestion and nutrient absorption in the proximal region to be separate from the vast microbial populations in the large intestine, thereby reducing conflict between host and microbes. In the distinct habitats of the gut, environmental filtering and competitive exclusion between microbes are the driving factors shaping microbial diversity, and stochastic factors during colonization history and in situ evolution are likely to introduce intersubject variability. Adaptive strategies of microbes with different niches are genomically encoded: Specialists have smaller genomes than generalists, and microbes with environmental reservoirs have large accessory genomes. A shift toward a Neolithic diet increased loads of simple carbohydrates and selected for their increased breakdown and absorption in the small intestine. Humans who outcompeted microbes for the new substrates obtained more energy from their diets and prospered, an evolutionary process reflected in modern population genetics. The three-way interactions between human genetics, diet, and the microbiota fundamentally shaped modern populations and continue to affect health globally.
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              Diversity, structure and convergent evolution of the global sponge microbiome

              Sponges (phylum Porifera) are early-diverging metazoa renowned for establishing complex microbial symbioses. Here we present a global Porifera microbiome survey, set out to establish the ecological and evolutionary drivers of these host–microbe interactions. We show that sponges are a reservoir of exceptional microbial diversity and major contributors to the total microbial diversity of the world's oceans. Little commonality in species composition or structure is evident across the phylum, although symbiont communities are characterized by specialists and generalists rather than opportunists. Core sponge microbiomes are stable and characterized by generalist symbionts exhibiting amensal and/or commensal interactions. Symbionts that are phylogenetically unique to sponges do not disproportionally contribute to the core microbiome, and host phylogeny impacts complexity rather than composition of the symbiont community. Our findings support a model of independent assembly and evolution in symbiont communities across the entire host phylum, with convergent forces resulting in analogous community organization and interactions.
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                Author and article information

                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group
                1751-7362
                1751-7370
                October 2017
                16 May 2017
                1 October 2017
                : 11
                : 10
                : 2167-2174
                Affiliations
                [1 ]Australian Institute of Marine Science , Townsville, Queensland, Australia
                [2 ]Australian Centre for Ecogenomics, University of Queensland , Brisbane, Queensland, Australia
                [3 ]GEOMAR Helmholtz Centre for Ocean Research Kiel , Kiel, Germany
                Author notes
                [* ]Australian Institute of Marine Science , PMB 3 Townsville Mail Centre, Townsville, Queensland 4810, Australia. E-mail: n.webster@ 123456aims.gov.au
                Article
                ismej201766
                10.1038/ismej.2017.66
                5607359
                28509908
                Copyright © 2017 The Author(s)

                This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/4.0/

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                Microbiology & Virology

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