Metagenomic insights into the taxonomy, function, and dysbiosis of prokaryotic communities in octocorals
Abstract
Background. In octocorals (Cnidaria Octocorallia), the functional relationship between host health and its symbiotic consortium has yet to be determined. Here, we employed comparative metagenomics to uncover the distinct functional and phylogenetic features of the microbiomes of healthy Eunicella gazella, Eunicella verrucosa, and Leptogorgia sarmentosa tissues, in contrast with the microbiomes found in seawater and sediments. We further explored how the octocoral microbiome shifts to a pathobiome state in E. gazella. Results. Multivariate analyses based on 16S rRNA genes, Clusters of Orthologous Groups of proteins (COGs), Protein families (Pfams), and secondary metabolite-biosynthetic gene clusters annotated from 20 Illumina-sequenced metagenomes each revealed separate clustering of the prokaryotic communities of healthy tissue samples of the three octocoral species from those of necrotic E. gazella tissue and surrounding environments. While the healthy octocoral microbiome was distinguished by so-far uncultivated Endozoicomonadaceae, Oceanospirillales, and Alteromonadales phylotypes in all host species, a pronounced increase of Flavobacteriaceae and Alphaproteobacteria, originating from seawater, was observed in necrotic E. gazella tissue. Increased abundances of eukaryotic-like proteins, exonucleases, restriction endonucleases, CRISPR/Cas proteins, and genes encoding for heat-shock proteins, inorganic ion transport, and iron storage distinguished the prokaryotic communities of healthy octocoral tissue regardless of the host species. An increase ofmore »
- Authors:
-
[1];
- Universidade de Lisboa, Lisbon (Portugal)
- Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Ensenada, Baja California (Mexico)
- Helmholtz Centre for Environmental Research (UFZ), Leipzig (Germany)
- Universidade do Algarve, Faro (Portugal)
- USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
- Universidade de Lisboa, Lisbon (Portugal); Universidade do Algarve, Faro (Portugal); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1826912
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Microbiome
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2049-2618
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Host-microbe interactions; Symbiosis; Holobiont; Gorgonians; Eunicella; Leptogorgia; Secondary metabolism; Necrosis
Citation Formats
Keller-Costa, T., Lago-Lestón, A., Saraiva, J. P., Toscan, R., Silva, S. G., Gonçalves, J., Cox, C. J., Kyrpides, N., Nunes da Rocha, U., and Costa, R. Metagenomic insights into the taxonomy, function, and dysbiosis of prokaryotic communities in octocorals. United States: N. p., 2021.
Web. doi:10.1186/s40168-021-01031-y.
Keller-Costa, T., Lago-Lestón, A., Saraiva, J. P., Toscan, R., Silva, S. G., Gonçalves, J., Cox, C. J., Kyrpides, N., Nunes da Rocha, U., & Costa, R. Metagenomic insights into the taxonomy, function, and dysbiosis of prokaryotic communities in octocorals. United States. https://doi.org/10.1186/s40168-021-01031-y
Keller-Costa, T., Lago-Lestón, A., Saraiva, J. P., Toscan, R., Silva, S. G., Gonçalves, J., Cox, C. J., Kyrpides, N., Nunes da Rocha, U., and Costa, R. Thu .
"Metagenomic insights into the taxonomy, function, and dysbiosis of prokaryotic communities in octocorals". United States. https://doi.org/10.1186/s40168-021-01031-y. https://www.osti.gov/servlets/purl/1826912.
@article{osti_1826912,
title = {Metagenomic insights into the taxonomy, function, and dysbiosis of prokaryotic communities in octocorals},
author = {Keller-Costa, T. and Lago-Lestón, A. and Saraiva, J. P. and Toscan, R. and Silva, S. G. and Gonçalves, J. and Cox, C. J. and Kyrpides, N. and Nunes da Rocha, U. and Costa, R.},
abstractNote = {Background. In octocorals (Cnidaria Octocorallia), the functional relationship between host health and its symbiotic consortium has yet to be determined. Here, we employed comparative metagenomics to uncover the distinct functional and phylogenetic features of the microbiomes of healthy Eunicella gazella, Eunicella verrucosa, and Leptogorgia sarmentosa tissues, in contrast with the microbiomes found in seawater and sediments. We further explored how the octocoral microbiome shifts to a pathobiome state in E. gazella. Results. Multivariate analyses based on 16S rRNA genes, Clusters of Orthologous Groups of proteins (COGs), Protein families (Pfams), and secondary metabolite-biosynthetic gene clusters annotated from 20 Illumina-sequenced metagenomes each revealed separate clustering of the prokaryotic communities of healthy tissue samples of the three octocoral species from those of necrotic E. gazella tissue and surrounding environments. While the healthy octocoral microbiome was distinguished by so-far uncultivated Endozoicomonadaceae, Oceanospirillales, and Alteromonadales phylotypes in all host species, a pronounced increase of Flavobacteriaceae and Alphaproteobacteria, originating from seawater, was observed in necrotic E. gazella tissue. Increased abundances of eukaryotic-like proteins, exonucleases, restriction endonucleases, CRISPR/Cas proteins, and genes encoding for heat-shock proteins, inorganic ion transport, and iron storage distinguished the prokaryotic communities of healthy octocoral tissue regardless of the host species. An increase of arginase and nitric oxide reductase genes, observed in necrotic E. gazella tissues, suggests the existence of a mechanism for suppression of nitrite oxide production by which octocoral pathogens may overcome the host’s immune system. Conclusions. This is the first study to employ primer-less, shotgun metagenome sequencing to unveil the taxonomic, functional, and secondary metabolism features of prokaryotic communities in octocorals. Our analyses reveal that the octocoral microbiome is distinct from those of the environmental surroundings, is host genus (but not species) specific, and undergoes large, complex structural changes in the transition to the dysbiotic state. Host-symbiont recognition, abiotic-stress response, micronutrient acquisition, and an antiviral defense arsenal comprising multiple restriction endonucleases, CRISPR/Cas systems, and phage lysogenization regulators are signatures of prokaryotic communities in octocorals. We argue that these features collectively contribute to the stabilization of symbiosis in the octocoral holobiont and constitute beneficial traits that can guide future studies on coral reef conservation and microbiome therapy.},
doi = {10.1186/s40168-021-01031-y},
journal = {Microbiome},
number = 1,
volume = 9,
place = {United States},
year = {Thu Mar 25 00:00:00 EDT 2021},
month = {Thu Mar 25 00:00:00 EDT 2021}
}
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