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Research Article | Ecological and Evolutionary Science

Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere

Alejandra Hernandez-Agreda, William Leggat, Pim Bongaerts, César Herrera, Tracy D. Ainsworth
Nicole Dubilier, Editor
Alejandra Hernandez-Agreda
aAustralian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia
bCollege of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Australia
eCalifornia Academy of Sciences, San Francisco, California, USA
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William Leggat
aAustralian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia
bCollege of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Australia
cSchool of Environmental and Life Sciences, The University of Newcastle, Ourimbah, Australia
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Pim Bongaerts
dGlobal Change Institute, The University of Queensland, Brisbane, Australia
eCalifornia Academy of Sciences, San Francisco, California, USA
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César Herrera
fTropWATER, Centre for Tropical Water & Aquatic Ecosystem Research, James Cook University, Townsville, Australia
gCollege of Science and Engineering, James Cook University, Townsville, Australia
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Tracy D. Ainsworth
aAustralian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia
hSchool of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, Australia
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Nicole Dubilier
Max Planck Institute for Marine Microbiology
Roles: Editor
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DOI: 10.1128/mBio.00812-18
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ABSTRACT

Studies of the coral microbiome predominantly characterize the microbial community of the host species as a collective, rather than that of the individual. This ecological perspective on the coral microbiome has led to the conclusion that the coral holobiont is the most diverse microbial biosphere studied thus far. However, investigating the microbiome of the individual, rather than that of the species, highlights common and conserved community attributes which can provide insights into the significance of microbial associations to the host. Here, we show there are consistent characteristics between individuals in the proposed three components of the coral microbiome (i.e., “environmentally responsive community,” “resident or individual microbiome,” and “core microbiome”). We found that the resident microbiome of a photoendosymbiotic coral harbored <3% (∼605 phylotypes) of the 16S rRNA phylotypes associated with all investigated individuals of that species (“species-specific microbiome”) (∼21,654 phylotypes; individuals from Pachyseris speciosa [n = 123], Mycedium elephantotus [n = 95], and Acropora aculeus [n = 91] from 10 reef locations). The remaining bacterial phylotypes (>96%) (environmentally responsive community) of the species-specific microbiome were in fact not found in association with the majority of individuals of the species. Only 0.1% (∼21 phylotypes) of the species-specific microbiome of each species was shared among all individuals of the species (core microbiome), equating to ∼3.4% of the resident microbiome. We found taxonomic redundancy and consistent patterns of composition, structure, and taxonomic breadth across individual microbiomes from the three coral species. Our results demonstrate that the coral microbiome is structured at the individual level.

IMPORTANCE We propose that the coral holobiont should be conceptualized as a diverse transient microbial community that is responsive to the surrounding environment and encompasses a simple, redundant, resident microbiome and a small conserved core microbiome. Most importantly, we show that the coral microbiome is comparable to the microbiomes of other organisms studied thus far. Accurately characterizing the coral-microbe interactions provides an important baseline from which the functional roles and the functional niches within which microbes reside can be deciphered.

  • Copyright © 2018 Hernandez-Agreda et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere
Alejandra Hernandez-Agreda, William Leggat, Pim Bongaerts, César Herrera, Tracy D. Ainsworth
mBio Oct 2018, 9 (5) e00812-18; DOI: 10.1128/mBio.00812-18

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Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere
Alejandra Hernandez-Agreda, William Leggat, Pim Bongaerts, César Herrera, Tracy D. Ainsworth
mBio Oct 2018, 9 (5) e00812-18; DOI: 10.1128/mBio.00812-18
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KEYWORDS

bacteria
coral
holobiont
microbiome
symbiosis

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