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

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 bi...

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Autores principales: Alejandra Hernandez-Agreda, William Leggat, Pim Bongaerts, César Herrera, Tracy D. Ainsworth
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:7e9ef1efb2744f5ca7b792b3150fc7a62021-11-15T15:58:20ZRethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere10.1128/mBio.00812-182150-7511https://doaj.org/article/7e9ef1efb2744f5ca7b792b3150fc7a62018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00812-18https://doaj.org/toc/2150-7511ABSTRACT 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.Alejandra Hernandez-AgredaWilliam LeggatPim BongaertsCésar HerreraTracy D. AinsworthAmerican Society for MicrobiologyarticlebacteriacoralholobiontmicrobiomesymbiosisMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution DOAJ
collection DOAJ
language EN
topic bacteria
coral
holobiont
microbiome
symbiosis
Microbiology
QR1-502
spellingShingle bacteria
coral
holobiont
microbiome
symbiosis
Microbiology
QR1-502
Alejandra Hernandez-Agreda
William Leggat
Pim Bongaerts
César Herrera
Tracy D. Ainsworth
Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere
description 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.
format article
author Alejandra Hernandez-Agreda
William Leggat
Pim Bongaerts
César Herrera
Tracy D. Ainsworth
author_facet Alejandra Hernandez-Agreda
William Leggat
Pim Bongaerts
César Herrera
Tracy D. Ainsworth
author_sort Alejandra Hernandez-Agreda
title Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere
title_short Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere
title_full Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere
title_fullStr Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere
title_full_unstemmed Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere
title_sort rethinking the coral microbiome: simplicity exists within a diverse microbial biosphere
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/7e9ef1efb2744f5ca7b792b3150fc7a6
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AT williamleggat rethinkingthecoralmicrobiomesimplicityexistswithinadiversemicrobialbiosphere
AT pimbongaerts rethinkingthecoralmicrobiomesimplicityexistswithinadiversemicrobialbiosphere
AT cesarherrera rethinkingthecoralmicrobiomesimplicityexistswithinadiversemicrobialbiosphere
AT tracydainsworth rethinkingthecoralmicrobiomesimplicityexistswithinadiversemicrobialbiosphere
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