Cargando…

Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease

BACKGROUND: Coral reefs face unprecedented declines in diversity and cover, a development largely attributed to climate change-induced bleaching and subsequent disease outbreaks. Coral-associated microbiomes may strongly influence the fitness of their hosts and alter heat tolerance and disease susce...

Descripción completa

Detalles Bibliográficos
Autores principales: Sweet, Michael, Burian, Alfred, Fifer, James, Bulling, Mark, Elliott, David, Raymundo, Laurie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6873542/
https://www.ncbi.nlm.nih.gov/pubmed/31752998
http://dx.doi.org/10.1186/s40168-019-0759-6
_version_ 1783472682996596736
author Sweet, Michael
Burian, Alfred
Fifer, James
Bulling, Mark
Elliott, David
Raymundo, Laurie
author_facet Sweet, Michael
Burian, Alfred
Fifer, James
Bulling, Mark
Elliott, David
Raymundo, Laurie
author_sort Sweet, Michael
collection PubMed
description BACKGROUND: Coral reefs face unprecedented declines in diversity and cover, a development largely attributed to climate change-induced bleaching and subsequent disease outbreaks. Coral-associated microbiomes may strongly influence the fitness of their hosts and alter heat tolerance and disease susceptibility of coral colonies. Here, we describe a new coral disease found in Micronesia and present a detailed assessment of infection-driven changes in the coral microbiome. RESULTS: Combining field monitoring and histological, microscopic and next-generation barcoding assessments, we demonstrate that the outbreak of the disease, named ‘grey-patch disease’, is associated with the establishment of cyanobacterial biofilm overgrowing coral tissue. The disease is characterised by slow progression rates, with coral tissue sometimes growing back over the GPD biofilm. Network analysis of the corals’ microbiome highlighted the clustering of specific microbes which appeared to benefit from the onset of disease, resulting in the formation of ‘infection clusters’ in the microbiomes of apparently healthy corals. CONCLUSIONS: Our results appear to be in contrast to the recently proposed Anna-Karenina principle, which states that disturbances (such as disease) trigger chaotic dynamics in microbial communities and increase β-diversity. Here, we show significantly higher community similarity (compositional homogeneity) in the pathobiome of diseased corals, compared to the microbiome associated with apparently healthy tissue. A possible explanation for this pattern is strong competition between the pathogenic community and those associated with the ‘healthy’ coral holobiont, homogenising the composition of the pathobiome. Further, one of our key findings is that multiple agents appear to be involved in degrading the corals’ defences causing the onset of this disease. This supports recent findings indicating a need for a shift from the one-pathogen-one-disease paradigm to exploring the importance of multiple pathogenic players in any given disease.
format Online
Article
Text
id pubmed-6873542
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-68735422019-12-12 Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease Sweet, Michael Burian, Alfred Fifer, James Bulling, Mark Elliott, David Raymundo, Laurie Microbiome Research BACKGROUND: Coral reefs face unprecedented declines in diversity and cover, a development largely attributed to climate change-induced bleaching and subsequent disease outbreaks. Coral-associated microbiomes may strongly influence the fitness of their hosts and alter heat tolerance and disease susceptibility of coral colonies. Here, we describe a new coral disease found in Micronesia and present a detailed assessment of infection-driven changes in the coral microbiome. RESULTS: Combining field monitoring and histological, microscopic and next-generation barcoding assessments, we demonstrate that the outbreak of the disease, named ‘grey-patch disease’, is associated with the establishment of cyanobacterial biofilm overgrowing coral tissue. The disease is characterised by slow progression rates, with coral tissue sometimes growing back over the GPD biofilm. Network analysis of the corals’ microbiome highlighted the clustering of specific microbes which appeared to benefit from the onset of disease, resulting in the formation of ‘infection clusters’ in the microbiomes of apparently healthy corals. CONCLUSIONS: Our results appear to be in contrast to the recently proposed Anna-Karenina principle, which states that disturbances (such as disease) trigger chaotic dynamics in microbial communities and increase β-diversity. Here, we show significantly higher community similarity (compositional homogeneity) in the pathobiome of diseased corals, compared to the microbiome associated with apparently healthy tissue. A possible explanation for this pattern is strong competition between the pathogenic community and those associated with the ‘healthy’ coral holobiont, homogenising the composition of the pathobiome. Further, one of our key findings is that multiple agents appear to be involved in degrading the corals’ defences causing the onset of this disease. This supports recent findings indicating a need for a shift from the one-pathogen-one-disease paradigm to exploring the importance of multiple pathogenic players in any given disease. BioMed Central 2019-11-22 /pmc/articles/PMC6873542/ /pubmed/31752998 http://dx.doi.org/10.1186/s40168-019-0759-6 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Sweet, Michael
Burian, Alfred
Fifer, James
Bulling, Mark
Elliott, David
Raymundo, Laurie
Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease
title Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease
title_full Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease
title_fullStr Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease
title_full_unstemmed Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease
title_short Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease
title_sort compositional homogeneity in the pathobiome of a new, slow-spreading coral disease
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6873542/
https://www.ncbi.nlm.nih.gov/pubmed/31752998
http://dx.doi.org/10.1186/s40168-019-0759-6
work_keys_str_mv AT sweetmichael compositionalhomogeneityinthepathobiomeofanewslowspreadingcoraldisease
AT burianalfred compositionalhomogeneityinthepathobiomeofanewslowspreadingcoraldisease
AT fiferjames compositionalhomogeneityinthepathobiomeofanewslowspreadingcoraldisease
AT bullingmark compositionalhomogeneityinthepathobiomeofanewslowspreadingcoraldisease
AT elliottdavid compositionalhomogeneityinthepathobiomeofanewslowspreadingcoraldisease
AT raymundolaurie compositionalhomogeneityinthepathobiomeofanewslowspreadingcoraldisease