skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Metagenomic insights into the taxonomy, function, and dysbiosis of prokaryotic communities in octocorals

Journal Article · · Microbiome
ORCiD logo [1];  [2];  [3];  [3];  [1];  [4];  [4];  [5];  [3];  [6]
  1. Universidade de Lisboa, Lisbon (Portugal)
  2. Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Ensenada, Baja California (Mexico)
  3. Helmholtz Centre for Environmental Research (UFZ), Leipzig (Germany)
  4. Universidade do Algarve, Faro (Portugal)
  5. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
  6. Universidade de Lisboa, Lisbon (Portugal); Universidade do Algarve, Faro (Portugal); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
+ Show Author Affiliations

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.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1826912
Journal Information:
Microbiome, Vol. 9, Issue 1; ISSN 2049-2618
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English

References (82)

Ankyrin-repeat proteins from sponge symbionts modulate amoebal phagocytosis journal August 2013
Minimum Information about a Biosynthetic Gene cluster journal August 2015
Associations between species and groups of sites: indices and statistical inference journal December 2009
Bacteriome Structure, Function, and Probiotics in Fish Larviculture: The Good, the Bad, and the Gaps journal February 2021
The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4) journal October 2015
Compositional homogeneity in the pathobiome of a new, slow-spreading coral disease journal November 2019
A framework for estimating niche metrics using the resemblance between qualitative resources journal April 2011
Bacterial Communities of the Gorgonian Octocoral Pseudopterogorgia elisabethae journal August 2013
On the Importance of the Microbiome and Pathobiome in Coral Health and Disease journal January 2017
CRISPR-Cas Defense System and Potential Prophages in Cyanobacteria Associated with the Coral Black Band Disease journal December 2016
Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis journal July 2006
Long-Term Temperature Stress in the Coral Model Aiptasia Supports the “Anna Karenina Principle” for Bacterial Microbiomes journal May 2019
A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-western Mediterranean), summer 1999 journal July 2000
The Draft Genome of an Octocoral, Dendronephthya gigantea journal March 2019
InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams journal May 2015
Microbiota of Healthy Corals Are Active against Fungi in a Light-Dependent Manner journal August 2014
Bacteria of the genus Endozoicomonas dominate the microbiome of the Mediterranean gorgonian coral Eunicella cavolini journal April 2013
Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation journal December 2018
Expressing cytotoxic compounds in Escherichia coli Nissle 1917 for tumor-targeting therapy journal March 2019
metaSPAdes: a new versatile metagenomic assembler journal March 2017
Piggyback-the-Winner in host-associated microbial communities journal July 2016
Metagenomic analysis of the microbial community associated with the coral Porites astreoides journal November 2007
Transcriptome, expression, and activity analyses reveal a vital heat shock protein 70 in the stress response of stony coral Pocillopora damicornis journal February 2018
EBI metagenomics in 2016 - an expanding and evolving resource for the analysis and archiving of metagenomic data journal November 2015
Marine natural products journal January 2016
Culturing captures members of the soil rare biosphere: Rare biosphere of soil journal July 2012
Ecological Shifts in Mediterranean Coralligenous Assemblages Related to Gorgonian Forest Loss journal July 2014
The DNA Exonucleases of Escherichia coli journal June 2011
Bisucaberin B, a Linear Hydroxamate Class Siderophore from the Marine Bacterium Tenacibaculum mesophilum journal April 2013
CRISPR Interference Limits Horizontal Gene Transfer in Staphylococci by Targeting DNA journal December 2008
MetaWRAP—a flexible pipeline for genome-resolved metagenomic data analysis journal September 2018
Mass mortality hits gorgonian forests at Montecristo Island journal October 2018
Primary Isolation and Characterization of Tenacibaculum maritimum from Chilean Atlantic Salmon Mortalities Associated with a Pseudochattonella spp. Algal Bloom journal June 2017
Coral-Associated Bacteria and Their Role in the Biogeochemical Cycling of Sulfur journal April 2009
Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea journal April 2016
The past, present, and future of coral heat stress studies journal August 2019
Modulation of the Arginase Pathway in the Context of Microbial Pathogenesis: A Metabolic Enzyme Moonlighting as an Immune Modulator journal June 2010
Coral microbiome dynamics, functions and design in a changing world journal July 2019
Comparative genome analysis provides novel insight into the interaction of Aquimarina sp. AD1, BL5 and AD10 with their macroalgal host journal August 2019
MIBiG 2.0: a repository for biosynthetic gene clusters of known function journal October 2019
Lytic to temperate switching of viral communities journal March 2016
Disturbance to conserved bacterial communities in the cold-water gorgonian coral Eunicella verrucosa journal August 2014
Stress and stability: applying the Anna Karenina principle to animal microbiomes journal August 2017
Transient Shifts in Bacterial Communities Associated with the Temperate Gorgonian Paramuricea clavata in the Northwestern Mediterranean Sea journal February 2013
Responses of Coral-Associated Bacterial Communities to Local and Global Stressors journal August 2017
The Assimilation of Diazotroph-Derived Nitrogen by Scleractinian Corals Depends on Their Metabolic Status journal March 2017
Microbial functional structure of Montastraea faveolata , an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies journal February 2010
Paenibacterin, a novel broad-spectrum lipopeptide antibiotic, neutralises endotoxins and promotes survival in a murine model of Pseudomonas aeruginosa-induced sepsis journal July 2014
Pseudoalteromonas phenolica sp. nov., a novel marine bacterium that produces phenolic anti-methicillin-resistant Staphylococcus aureus substances journal March 2003
Accelerated Profile HMM Searches journal October 2011
Evidence for host specificity among dominant bacterial symbionts in temperate gorgonian corals journal August 2015
Diseases affect cold-water corals too: Eunicella verrucosa (Cnidaria: Gorgonacea) necrosis in SW England journal June 2007
Effects of sample handling and cultivation bias on the specificity of bacterial communities in keratose marine sponges journal November 2014
Characterization of heat-shock response of the marine bacterium Vibrio harveyi journal May 1995
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Host-microbe interactions in octocoral holobionts - recent advances and perspectives journal April 2018
Comparative Assessment of Mediterranean Gorgonian-Associated Microbial Communities Reveals Conserved Core and Locally Variant Bacteria journal October 2016
Microbes in the coral holobiont: partners through evolution, development, and ecological interactions journal January 2015
16SrDNA Pyrosequencing of the Mediterranean Gorgonian Paramuricea clavata Reveals a Link among Alterations in Bacterial Holobiont Members, Anthropogenic Influence and Disease Outbreaks journal June 2013
A multifaceted role for polyamines in bacterial pathogens journal April 2008
The gorgonian coral Eunicella labiata hosts a distinct prokaryotic consortium amenable to cultivation journal October 2017
antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline journal April 2019
Spatial and depth-associated distribution patterns of shallow gorgonians in the Algarve coast (Portugal, NE Atlantic) journal December 2012
Genomic blueprints of sponge-prokaryote symbiosis are shared by low abundant and cultivatable Alphaproteobacteria journal February 2019
Insights into Secondary Metabolism from a Global Analysis of Prokaryotic Biosynthetic Gene Clusters journal July 2014
Isolation and activity of Xenorhabdus antimicrobial compounds against the plant pathogens Erwinia amylovora and Phytophthora nicotianae journal September 2009
Discovery of recombinases enables genome mining of cryptic biosynthetic gene clusters in Burkholderiales species journal April 2018
Bioactive Secondary Metabolites from Octocoral-Associated Microbes—New Chances for Blue Growth journal December 2018
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes journal October 2018
Genome-reconstruction for eukaryotes from complex natural microbial communities journal March 2018
A genomic view of the reef-building coral Porites lutea and its microbial symbionts journal September 2019
Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems journal September 2016
The nature of plant growth-promoting effects of a pseudoalteromonad associated with the marine algae Laminaria japonica and linked to catalase excretion journal May 2006
Identification of Candidate Coral Pathogens on White Band Disease-Infected Staghorn Coral journal August 2015
A member of the Roseobacter clade, Octadecabacter sp., is the dominant symbiont in the brittle star Amphipholis squamata journal February 2018
Vibrio infections triggering mass mortality events in a warming Mediterranean Sea: Vibrio infections triggering sea-fan mass mortality journal March 2010
Temporal dynamics of prokaryotic communities in the marine sponge Sarcotragus spinosulus journal June 2014
Type III Secretion System of Beneficial Rhizobacteria Pseudomonas simiae WCS417 and Pseudomonas defensor WCS374 journal July 2019
Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales journal July 2016
Spirochaetes dominate the microbial community associated with the red coral Corallium rubrum on a broad geographic scale journal June 2016
Antibacterial Activity of Pseudoalteromonas in the Coral Holobiont journal July 2012
Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis journal June 2010

Linked Research (6)

Similar Records

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Host-microbe interactions
Symbiosis
Holobiont
Gorgonians
Eunicella
Leptogorgia
Secondary metabolism
Necrosis