Potential role of viruses in white plague coral disease

White plague (WP)-like diseases of tropical corals are implicated in reef decline worldwide, although their etiological cause is generally unknown. Studies thus far have focused on bacterial or eukaryotic pathogens as the source of these diseases; no studies have examined the role of viruses. Using a combination of transmission electron microscopy (TEM) and 454 pyrosequencing, we compared 24 viral metagenomes generated from Montastraea annularis corals showing signs of WP-like disease and/or bleaching, control conspecific corals, and adjacent seawater. TEM was used for visual inspection of diseased coral tissue. No bacteria were visually identified within diseased coral tissues, but viral particles and sequence similarities to eukaryotic circular Rep-encoding single-stranded DNA viruses and their associated satellites (SCSDVs) were abundant in WP diseased tissues. In contrast, sequence similarities to SCSDVs were not found in any healthy coral tissues, suggesting SCSDVs might have a role in WP disease. Furthermore, Herpesviridae gene signatures dominated healthy tissues, corroborating reports that herpes-like viruses infect all corals. Nucleocytoplasmic large DNA virus (NCLDV) sequences, similar to those recently identified in cultures of Symbiodinium (the algal symbionts of corals), were most common in bleached corals. This finding further implicates that these NCLDV viruses may have a role in bleaching, as suggested in previous studies. This study determined that a specific group of viruses is associated with diseased Caribbean corals and highlights the potential for viral disease in regional coral reef decline.

• Publication year

  2013

• Venue

  The ISME Journal

• Publication date

  2013-08-15

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1038/ismej.2013.137PMID 23949663PMCID 3906806
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Disturbance Driven Colony Fragmentation as a Driver of a Coral Disease Outbreak

  2013cited by this paper
• Severe respiratory illness caused by a novel coronavirus, in a patient transferred to the United Kingdom from the Middle East, September 2012.

  2012cited by this paper
• Phage therapy of the white plague-like disease of Favia favus in the Red Sea

  2012cited by this paper
• Incubation period as part of the case definition of severe respiratory illness caused by a novel coronavirus.

  2012cited by this paper
• A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics

  2012influential reference
• Unique nucleocytoplasmic dsDNA and +ssRNA viruses are associated with the dinoflagellate endosymbionts of corals

  2012cited by this paper
• Metagenomics and future perspectives in virus discovery

  2012cited by this paper
• Spread like a wildfire--the omnipresence of porcine circovirus type 2 (PCV2) and its ever-expanding association with diseases in pigs.

  2012cited by this paper
• Rapidly expanding genetic diversity and host range of the Circoviridae viral family and other Rep encoding small circular ssDNA genomes.

  2012influential reference
• Fast Identification and Removal of Sequence Contamination from Genomic and Metagenomic Datasets

  2011cited by this paper
• Shifts in bacterial communities of two caribbean reef-building coral species affected by white plague disease

  2011cited by this paper
• Amplification Methods Bias Metagenomic Libraries of Uncultured Single-Stranded and Double-Stranded DNA Viruses

  2011cited by this paper
• Viruses of reef-building scleractinian corals

  2011cited by this paper
• Recombination in Eukaryotic Single Stranded DNA Viruses

  2011influential reference
• Spatial heterogeneity of bacterial communities in the mucus of Montastraea annularis

  2011cited by this paper
• Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef.

  2011influential reference
• Human Pathogen Shown to Cause Disease in the Threatened Eklhorn Coral Acropora palmata

  2011cited by this paper
• The Urgent Need for Robust Coral Disease Diagnostics

  2011cited by this paper
• Fine-structural analysis of black band disease-infected coral reveals boring cyanobacteria and novel bacteria.

  2011cited by this paper
• Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences

  2010cited by this paper
• Human enteric viruses in groundwater indicate offshore transport of human sewage to coral reefs of the Upper Florida Keys.

  2010cited by this paper
• A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus

  2010cited by this paper
• Community cyberinfrastructure for Advanced Microbial Ecology Research and Analysis: the CAMERA resource

  2010cited by this paper
• Detection of a Novel Astrovirus in Brain Tissue of Mink Suffering from Shaking Mink Syndrome by Use of Viral Metagenomics

  2010cited by this paper
• Multiple displacement amplification compromises quantitative analysis of metagenomes

  2010cited by this paper
• Metagenomic analysis of viruses in reclaimed water.

  2009cited by this paper
• The Phycodnaviridae: the story of how tiny giants rule the world.

  2009influential reference
• Phage Therapy of Coral White Plague Disease: Properties of Phage BA3

  2009cited by this paper
• Novel anellovirus discovered from a mortality event of captive California sea lions.

  2009cited by this paper
• Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata

  2009cited by this paper
• Metagenomic analysis of stressed coral holobionts.

  2009influential reference
• Coral bleaching and disease should not be underestimated as causes of Caribbean coral reef decline

  2009cited by this paper
• Frequent Detection of Highly Diverse Variants of Cardiovirus, Cosavirus, Bocavirus, and Circovirus in Sewage Samples Collected in the United States

  2009cited by this paper
• Effects of a changing climate on the dynamics of coral infectious disease: a review of the evidence.

  2009cited by this paper
• Microbial disease and the coral holobiont.

  2009cited by this paper
• Viral communities associated with healthy and bleaching corals

  2008influential reference
• Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa

  2008influential reference
• Amplification of Uncultured Single-Stranded DNA Viruses from Rice Paddy Soil

  2008cited by this paper
• Prevalence of virus-like particles within a staghorn scleractinian coral (Acropora muricata) from the Great Barrier Reef

  2008cited by this paper
• Chromatin control of herpes simplex virus lytic and latent infection

  2008cited by this paper
• Morphological diversity of virus-like particles within the surface microlayer of scleractinian corals

  2007cited by this paper
• Metagenomic analysis of the microbial community associated with the coral Porites astreoides.

  2007influential reference
• Analysis of multiple enteric viral targets as sewage markers in coral reefs.

  2007cited by this paper
• The role of microorganisms in coral health, disease and evolution

  2007cited by this paper
• Environmental Whole-Genome Amplification To Access Microbial Populations in Contaminated Sediments

  2006cited by this paper
• Coral bleaching and disease combine to cause extensive mortality on reefs in US Virgin Islands

  2006cited by this paper
• Status and progress in coral reef disease research.

  2006cited by this paper
• Thalassomonas loyana sp. nov., a causative agent of the white plague-like disease of corals on the Eilat coral reef.

  2006cited by this paper
• Genome sequencing in microfabricated high-density picolitre reactors

  2005cited by this paper
• An enemy within? Observations of virus-like particles in reef corals.

  2005cited by this paper
• The Elusive Baseline of Marine Disease: Are Diseases in Ocean Ecosystems Increasing?

  2004cited by this paper
• White Plague, White Band, and Other “White” Diseases

  2004cited by this paper
• Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals

  2004influential reference
• MUSCLE: multiple sequence alignment with high accuracy and high throughput.

  2004cited by this paper
• The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis.

  2003cited by this paper
• Aurantimonas coralicida gen. nov., sp. nov., the causative agent of white plague type II on Caribbean scleractinian corals.

  2003cited by this paper
• Long-Term Region-Wide Declines in Caribbean Corals

  2003cited by this paper
• The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata

  2002cited by this paper
• Preliminary evidence for human fecal contamination in corals of the Florida Keys, USA.

  2002cited by this paper
• Integrating microbiological, microsensor, molecular, and physiologic techniques in the study of coral disease pathogenesis

  2001influential reference
• Change in marine communities : an approach to statistical analysis and interpretation

  2001influential reference
• The significance of coral disease epizootiology for coral reef conservation

  2000cited by this paper
• Emerging marine diseases--climate links and anthropogenic factors.

  1999cited by this paper
• Evidence that a plant virus switched hosts to infect a vertebrate and then recombined with a vertebrate-infecting virus.

  1999cited by this paper
• Florida's mystery coral-killer identified

  1998cited by this paper
• Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria

  1992cited by this paper
• Basic local alignment search tool.

  1990cited by this paper
• Vitality of reef coral populations off Key Largo, Florida: Recruitment and mortality

  1977influential reference
• Microbial Disease and the Coral Holobiont

  year unknowncited by this paper
• Bioinformatics Applications Note Data and Text Mining Metavir: a Web Server Dedicated to Virome Analysis

  year unknowncited by this paper

• The epidermal ecotone: a proposed model system for marine viral ecology at the animal-environmental interface.

  2026cites this paper
• Transmission Electron Microscopy of Coral Tissue

  2024cites this paper
• Globally distributed bacteriophage genomes reveal mechanisms of tripartite phage–bacteria–coral interactions

  2024cites this paper
• Stony coral tissue loss disease: a review of emergence, impacts, etiology, diagnostics, and intervention

  2024cites this paper
• A genome-centric view of the role of the Acropora kenti microbiome in coral health and resilience

  2024cites this paper
• Viruses of a key coral symbiont exhibit temperature-driven productivity across a reefscape

  2023cites this paper
• Dynamics of the Apostichopus californicus-associated flavivirus under suboxic conditions and organic matter amendment

  2023cites this paper
• Four Novel Caudoviricetes Bacteriophages Isolated from Baltic Sea Water Infect Colonizers of Aurelia aurita

  2023cites this paper
• Ecotoxicological Effects of Four Commonly Used Organic Solvents on the Scleractinian Coral Montipora digitata

  2023cites this paper
• Recent advancements in coral health, microbiome interactions and climate change.

  2023cites this paper
• Effects of Ocean Warming on the Underexplored Members of the Coral Microbiome

  2022cites this paper
• The compact genome of the sponge Oopsacas minuta (Hexactinellida) is lacking key metazoan core genes

  2022cites this paper
• A Review of Marine Viruses in Coral Ecosystem

  2021cites this paper
• Pollution

  2021cites this paper
• Ciliated protozoan occurrence and association in the pathogenesis of coral disease.

  2021cites this paper
• Extending the natural adaptive capacity of coral holobionts

  2021cites this paper
• Similarities and Differences Between Two Deadly Caribbean Coral Diseases: White Plague and Stony Coral Tissue Loss Disease

  2021cites this paper
• OCTOCORALLIA, HEXACORALLIA, SCLERACTINIA, AND OTHER CORALS

  2021cites this paper
• ANALYSIS OF COMPOSITION AND ABUNDANCE OF VIRAL COMMUNITIES ASSOCIATED WITH CORAL Acropora formosa

  2021cites this paper
• Multi-Variate Analyses of Coral Mortality From the 2014–2015 Stony Coral Tissue Loss Disease Outbreak Off Miami-Dade County, Florida

  2021cites this paper
• Microbial bioindicators of Stony Coral Tissue Loss Disease identified in corals and overlying waters using a rapid field-based sequencing approach.

  2021cites this paper
• Stony Coral Tissue Loss Disease biomarker bacteria identified in corals and overlying waters using a rapid field-based sequencing approach

  2021cites this paper
• Thermal stress triggers productive viral infection of a key coral reef symbiont

  2021cites this paper
• Microbial dysbiosis reflects disease resistance in diverse coral species

  2021cites this paper
• Environmental and biological drivers of white plague disease on shallow and mesophotic coral reefs

  2021cites this paper
• Prophage Tracer: precisely tracing prophages in prokaryotic genomes using overlapping split-read alignment

  2021cites this paper
• Mussismilia braziliensis White Plague Disease Is Characterized by an Affected Coral Immune System and Dysbiosis

  2020cites this paper
• Diseases and pathogens of marine invertebrate corals in Indian reefs.

  2020cites this paper
• An Unconventional Flavivirus and Other RNA Viruses in the Sea Cucumber (Holothuroidea; Echinodermata) Virome

  2020cites this paper
• Coral-Associated Viral Assemblages From the Central Red Sea Align With Host Species and Contribute to Holobiont Genetic Diversity

  2020cites this paper
• Coral Bleaching Phenotypes Associated With Differential Abundances of Nucleocytoplasmic Large DNA Viruses

  2020cites this paper
• Unveiling Crucivirus Diversity by Mining Metagenomic Data

  2020cites this paper
• Increased Algal Symbiont Density Reduces Host Immunity in a Threatened Caribbean Coral Species, Orbicella faveolata

  2020cites this paper
• Deciphering Coral Disease Dynamics: Integrating Host, Microbiome, and the Changing Environment

  2020cites this paper
• Stony Coral Tissue Loss Disease in Florida Is Associated With Disruption of Host–Zooxanthellae Physiology

  2020cites this paper
• Mussismilia braziliensis White Plague Disease Is Characterized by an Affected Coral Immune System and Dysbiosis

  2020cites this paper
• Initial Virome Characterization of the Common Cnidarian Lab Model Nematostella vectensis

  2020cites this paper
• Ecology, histopathology, and microbial ecology of a white-band disease outbreak in the threatened staghorn coral Acropora cervicornis.

  2020cites this paper
• Metagenomic analysis of viral communities in diseased Baikal sponge Lubomirskia baikalensis

  2019cites this paper
• Physiology, syntrophy and viral interplay in the marine sponge holobiont

  2019cites this paper
• Thermal stress modifies the marine sponge virome.

  2019cites this paper
• Eukaryotic Circular Rep-Encoding Single-Stranded DNA (CRESS DNA) Viruses: Ubiquitous Viruses With Small Genomes and a Diverse Host Range.

  2019cites this paper
• Validation of ICESat-2 ATLAS Bathymetry and Analysis of ATLAS's Bathymetric Mapping Performance

  2019cites this paper
• Regional coral disease outbreak overwhelms impacts from a local dredge project

  2019cites this paper
• Technical pitfalls that bias comparative microbial community analyses of aquatic disease Ian Hewson.

  2019cites this paper
• IDENTIFIKASI BAKTERI PATOGEN PENYEBAB PENYAKIT PURPLE SYNDROME PADA KARANG FUNGIA DI PULAU HARI SULAWESI TENGGARA

  2019cites this paper
• Disentangling causation: complex roles of coral‐associated microorganisms in disease

  2018cites this paper
• Megaviridae-like particles associated with Symbiodinium spp. from the endemic coral Mussismilia braziliensis

  2018cites this paper
• COMPARISON OF FUNGAL COMMUNITIES ASSOCIATED WITH ORBICELLA FAVEOLATA IN APPARENTLY HEALTHY AND WHITE PLAGUE-LIKE DISEASED STATES

  2018influential citation
• First insight into the viral community of the cnidarian model metaorganism Aiptasia using RNA-Seq data

  2018cites this paper
• Host-microbe interactions in octocoral holobionts - recent advances and perspectives

  2018cites this paper
• Novel T4 bacteriophages associated with black band disease in corals.

  2018cites this paper
• Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny

  2018cites this paper
• Viruses in corals: hidden drivers of coral bleaching and disease?

  2018cites this paper
• Corallivory and the microbial debacle in two branching scleractinians

  2018influential citation
• Reef invertebrate viromics: diversity, host specificity and functional capacity

  2018influential citation
• Association of coral algal symbionts with a diverse viral community responsive to heat shock

  2017cites this paper
• The role of viruses in coral health and disease.

  2017cites this paper
• Rapid adaptive responses to climate change in corals

  2017cites this paper
• Gene expression of benthic amphipods (genus: Diporeia) in relation to a circular ssDNA virus across two Laurentian Great Lakes

  2017cites this paper
• Aquatic viral metagenomics: Lights and shadows.

  2017cites this paper
• Exploratory analysis of Symbiodinium transcriptomes reveals potential latent infection by large dsDNA viruses

  2017cites this paper
• Competing forces maintain the Hydra metaorganism

  2017cites this paper
• Virus–host interactions and their roles in coral reef health and disease

  2017cites this paper
• Viruses: contributors to and mitigators of black band disease in corals

  2017influential citation
• Unraveling the microbial processes of black band disease in corals through integrated genomics

  2017cites this paper
• Microbial processes driving coral reef organic carbon flow

  2017cites this paper
• Circular replication-associated protein encoding DNA viruses identified in the faecal matter of various animals in New Zealand.

  2016cites this paper
• White Syndrome-Affected Corals Have a Distinct Microbiome at Disease Lesion Fronts

  2016cites this paper
• Unprecedented Disease-Related Coral Mortality in Southeastern Florida

  2016cites this paper
• Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems.

  2016cites this paper
• HoloVir: A Workflow for Investigating the Diversity and Function of Viruses in Invertebrate Holobionts

  2016cites this paper
• Antimicrobial peptides in marine invertebrate health and disease

  2016cites this paper
• Shifting white pox aetiologies affecting Acropora palmata in the Florida Keys, 1994–2014

  2016cites this paper
• Viral Outbreak in Corals Associated with an In Situ Bleaching Event: Atypical Herpes-Like Viruses and a New Megavirus Infecting Symbiodinium

  2016cites this paper
• Exploring the function and behaviour of natural populations of coral reef microbes

  2016influential citation
• RNA-Seq of the Caribbean reef-building coral Orbicella faveolata (Scleractinia-Merulinidae) under bleaching and disease stress expands models of coral innate immunity

  2016cites this paper
• Metaproteomics reveals metabolic transitions between healthy and diseased stony coral Mussismilia braziliensis

  2016cites this paper
• Cycloviruses, gemycircularviruses and other novel replication-associated protein encoding circular viruses in Pacific flying fox (Pteropus tonganus) faeces.

  2016cites this paper
• Single-stranded DNA phages: from early molecular biology tools to recent revolutions in environmental microbiology.

  2016cites this paper
• Impact of environmental changes on Oculina patagonica coral holobiont

  2016cites this paper
• Identification of CRESS DNA viruses in faeces of Pacific flying foxes in the Tongan archipelago

  2016cites this paper
• Insights into the Coral Microbiome : Underpinning the Health and Resilience of Reef Ecosystems

  2016cites this paper
• Tales from the crypt and coral reef: the successes and challenges of identifying new herpesviruses using metagenomics

  2015cites this paper
• Influence of local environmental variables on the viral consortia associated with the coral Montipora capitata from Kaneohe Bay, Hawaii, USA

  2015cites this paper
• Diseases of Coral Reef Organisms

  2015cites this paper
• Coral Mucus Is a Hot Spot for Viral Infections

  2015cites this paper
• Diversity and comparative genomics of Microviridae in Sphagnum- dominated peatlands

  2015influential citation
• Novel circular single-stranded DNA viruses identified in marine invertebrates reveal high sequence diversity and consistent predicted intrinsic disorder patterns within putative structural proteins

  2015influential citation
• Ciliates associated with signs of disease on two Caribbean corals

  2015cites this paper
• From cholera to corals: Viruses as drivers of virulence in a major coral bacterial pathogen

  2015cites this paper
• The versatile nature of coral-associated viruses.

  2015cites this paper
• Assessment of the Impact of Super Storm Sandy on Coral Reefs of Guantanamo Bay, Cuba

  2015cites this paper
• A transcriptome resource for the coral, Orbicella faveolata (Scleractinia-Meruliniidae) – an emerging model of coral innate immunity

  2015influential citation
• Coral—the world's most diverse symbiotic ecosystem

  2015cites this paper
• Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease

  2015influential citation
• Metagenomic characterization of viral communities in corals: mining biological signal from methodological noise.

  2015cites this paper
• Phage-bacteria network analysis and its implication for the understanding of coral disease.

  2015influential citation
• Multiple mechanisms of transmission of the Caribbean coral disease white plague

  2015influential citation
• VÀ LONG NAM

  2015cites this paper