Toxicopathological Effects of the Sunscreen UV Filter, Oxybenzone (Benzophenone-3), on Coral Planulae and Cultured Primary Cells and Its Environmental Contamination in Hawaii and the U.S. Virgin Islands by CA Downs, et. al.

Coral-list post by Cheryl Woodley

I’d like to bring to your attention a new study published yesterday in the
journal *Archives of Environmental Contamination and Toxicology* showing
that a chemical widely used in personal care products such as sunscreen,
poses an ecological threat to corals and coral reefs and threatens their
existence.

Oxybenzone (also known as BP-3; Benzophenone-3) is found in over 3,500
sunscreen products worldwide, and pollutes coral reefs from swimmers
wearing sunscreens and through wastewater discharges from municipal sewage
outfalls and from coastal septic systems. Between 6,000 and 14,000 tons of
sunscreen lotion are emitted into coral reef areas each year, much of which
contains between one and 10% oxybenzone. The authors estimate that this
puts at least 10% of global reefs at risk of high exposure, based on reef
distribution in coastal tourist areas.

Toxicopathological effects of the sunscreen UV filter, oxybenzone on coral
planulae demonstrates that exposure of coral planulae (baby coral) to
oxybenzone, produces gross morphological deformities, damages their DNA,
and, most alarmingly, acts as an endocrine disruptor. The latter causes the
coral to encase itself in its own skeleton leading to death.

These effects were observed as low as 62 parts per trillion, the equivalent
to a drop of water in six and a half Olympic-sized swimming pools

Measurements of oxybenzone in seawater within coral reefs in Hawaii and the
U.S. Virgin Islands found concentrations ranging from 800 parts per
trillion to 1.4 parts per million. This is over 12 times higher than the
concentrations necessary to impact on coral

Article
Archives of Environmental Contamination and Toxicology, pp 1-24

First online: 20 October 2015

Toxicopathological Effects of the Sunscreen UV Filter, Oxybenzone (Benzophenone-3), on Coral Planulae and Cultured Primary Cells and Its Environmental Contamination in Hawaii and the U.S. Virgin Islands
C. A. Downs, Esti Kramarsky-Winter, Roee Segal, John Fauth, Sean Knutson, Omri Bronstein, Frederic R. Ciner, Rina Jeger, Yona Lichtenfel and 5 more

UV light on corals

Special thanks to Coral-list@noaa.gov

$39.95 / €34.95 / £29.95 *

* Final gross prices may vary according to local VAT.
Get Access

Abstract

Benzophenone-3 (BP-3; oxybenzone) is an ingredient in sunscreen lotions and personal-care products that protects against the damaging effects of ultraviolet light. Oxybenzone is an emerging contaminant of concern in marine environments—produced by swimmers and municipal, residential, and boat/ship wastewater discharges. We examined the effects of oxybenzone on the larval form (planula) of the coral Stylophora pistillata, as well as its toxicity in vitro to coral cells from this and six other coral species. Oxybenzone is a photo-toxicant; adverse effects are exacerbated in the light. Whether in darkness or light, oxybenzone transformed planulae from a motile state to a deformed, sessile condition. Planulae exhibited an increasing rate of coral bleaching in response to increasing concentrations of oxybenzone. Oxybenzone is a genotoxicant to corals, exhibiting a positive relationship between DNA-AP lesions and increasing oxybenzone concentrations. Oxybenzone is a skeletal endocrine disruptor; it induced ossification of the planula, encasing the entire planula in its own skeleton. The LC50 of planulae exposed to oxybenzone in the light for an 8- and 24-h exposure was 3.1 mg/L and 139 µg/L, respectively. The LC50s for oxybenzone in darkness for the same time points were 16.8 mg/L and 779 µg/L. Deformity EC20 levels (24 h) of planulae exposed to oxybenzone were 6.5 µg/L in the light and 10 µg/L in darkness. Coral cell LC50s (4 h, in the light) for 7 different coral species ranges from 8 to 340 µg/L, whereas LC20s (4 h, in the light) for the same species ranges from 0.062 to 8 µg/L. Coral reef contamination of oxybenzone in the U.S. Virgin Islands ranged from 75 µg/L to 1.4 mg/L, whereas Hawaiian sites were contaminated between 0.8 and 19.2 µg/L. Oxybenzone poses a hazard to coral reef conservation and threatens the resiliency of coral reefs to climate change.

Coral-list: Jeffrey Maynard announces Nature Climate Change publication “Projections of Climate Conditions that increase coral disease susceptibility and pathogen abundance and virulence.”

We’d like to bring your attention to a paper recently published in *Nature
Climate Change *titled: *Projections of climate conditions that increase
coral disease susceptibility and pathogen abundance and virulence. *

We present and compare climate model projections of temperature conditions
that will increase coral susceptibility to disease, pathogen abundance and
pathogen virulence under both moderate (RCP 4.5) and fossil fuel aggressive
(RCP 8.5) emissions scenarios. We also compare projections for the onset of
disease-conducive conditions and severe annual coral bleaching, and produce
a disease risk summary that combines climate stress with stress caused by
local human activities.

Some highlight results:

1. Disease is as likely to cause coral mortality as bleaching in the coming
decades. As evidence of this, at 96% of reef locations at least 2 of the 3
temperature conditions examined occur before annual severe coral bleaching
is projected to occur.

2. There are areas that meet 2 or all 3 of the temperature conditions
examined and have high or very high anthropogenic stress. These
are priority locations for reducing stress caused by local human activities
and testing management interventions to reduce disease impacts.

3. The emissions scenarios RCP8.5 and 4.5 take time to diverge and there is
little difference between the scenarios for the timing of the various
disease-promoting conditions being met. This is further evidence that
reducing stress caused by local human activities will be critically
important to reducing disease impacts in the coming decades.

The role of disease as a significant driver of future reef community
composition is under-appreciated, especially in the Indo-Pacific. Our paper
strongly suggests disease needs to be given greater consideration in
management planning. Further, we need to develop more early warning tools
for disease similar to the few already developed and the tools available
for monitoring bleaching risk from NOAA Coral Reef Watch.

The article can be accessed from the front page here:

http://www.nature.com/nclimate/journal/vaop/ncurrent/full/nclimate2625.html

A short story about the article:

http://www.news.cornell.edu/stories/2015/05/scientists-expect-more-coral-disease-under-climate-change

Our author team: Jeff Maynard, Ruben van Hooidonk, Mark Eakin, Marjetta
Puotinen, Melissa Garren, Gareth Williams, Scott Heron, Joleah Lamb,
Ernesto Weil, Bette Willis, and Drew Harvell.

*Funders: NOAA Climate Program Office and US National Science Foundation.


Jeffrey A. Maynard
Research Faculty – Dept of Ecology and Evolutionary Biology, Cornell
University
Research Scientist – CRIOBE & EPHE/CNRS of Moorea, Polynesia and Paris,
France.
Manager – Marine Applied Research Center, North Carolina.
P (mobile): +1 (910) 616-1096
E: maynardmarine@gmail.com
Skype: jefmaynard
_______________________________________________
Coral-List mailing list
Coral-List@coral.aoml.noaa.gov
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Molecular Ecology: Bacterial profiling of White Plague Disease across corals and oceans indicates a conserved and distinct disease microbiome by C. Roder, C. Arif, C. Daniels, E.Weil, C. Voolstral

Bacterial profiling of White Plague Disease across corals and oceans indicates a conserved and distinct disease microbiome – Roder – 2014 – Molecular Ecology – Wiley Online Library

Article first published online: 29 JAN 2014

DOI: 10.1111/mec.12638

© 2013 The Authors Molecular Ecology John Wiley & Sons Ltd.

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Molecular Ecology: Volume 23, Issue 4, pages 965–974, February 2014

16S rRNA gene microarray;
coral disease;
microbial community;
Orbicella faveolata ;
Orbicella franksi ;
Pavona duerdeni ;
Porites lutea ;
White Plague Disease (WPD);
White Plague-like Disease;
White Syndrome (WS)

Abstract

Coral diseases are characterized by microbial community shifts in coral mucus and tissue, but causes and consequences of these changes are vaguely understood due to the complexity and dynamics of coral-associated bacteria. We used 16S rRNA gene microarrays to assay differences in bacterial assemblages of healthy and diseased colonies displaying White Plague Disease (WPD) signs from two closely related Caribbean coral species, Orbicella faveolata and Orbicella franksi. Analysis of differentially abundant operational taxonomic units (OTUs) revealed strong differences between healthy and diseased specimens, but not between coral species. A subsequent comparison to data from two Indo-Pacific coral species (Pavona duerdeni and Porites lutea) revealed distinct microbial community patterns associated with ocean basin, coral species and health state. Coral species were clearly separated by site, but also, the relatedness of the underlying bacterial community structures resembled the phylogenetic relationship of the coral hosts. In diseased samples, bacterial richness increased and putatively opportunistic bacteria were consistently more abundant highlighting the role of opportunistic conditions in structuring microbial community patterns during disease. Our comparative analysis shows that it is possible to derive conserved bacterial footprints of diseased coral holobionts that might help in identifying key bacterial species related to the underlying etiopathology. Furthermore, our data demonstrate that similar-appearing disease phenotypes produce microbial community patterns that are consistent over coral species and oceans, irrespective of the putative underlying pathogen. Consequently, profiling coral diseases by microbial community structure over multiple coral species might allow the development of a comparative disease framework that can inform on cause and relatedness of coral diseases.

Ecotoxicology: Toxicological effects of the sunscreen UV filter, benzophenone-2, on planulae and in vitro cells of the coral, *Stylophora pistillata* by C. A. Downs • Esti Kramarsky-Winter • John E. Fauth • Roee Segal •Omri Bronstein • Rina Jeger • Yona Lichtenfeld • Cheryl M. Woodley • Paul Pennington • Ariel Kushmaro • Yossi Loya

The article is in the journal Ecotoxicology. A link to the article can be
found at http://link.springer.com/article/10.1007/s10646-013-1161-y

Accepted: 7 December 2013

Abstract Benzophenone-2 (BP-2) is an additive to personal-care products and commercial solutions that protects against the damaging effects of ultraviolet light. BP-2 is an ‘‘emerging contaminant of concern’’ that is often released as a pollutant through municipal and boat/ship wastewater discharges and landfill leachates, as well as through residential septic
fields and unmanaged cesspits. AlthoughBP-2may be a contaminant on coral reefs, its environmental toxicity to reefs is unknown. This poses a potential management issue, since BP-2 is a known endocrine disruptor as well as a weak genotoxicant. We examined the effects of BP-2 on the larval form (planula) of the coral, Stylophora pistillata, as well as its toxicity to in vitro coral cells. BP-2 is a photo-toxicant; adverse effects are exacerbated in the light versus in darkness. Whether in darkness or light,
BP-2 induced coral planulae to transformfromamotile planktonic state to a deformed, sessile condition. Planulae exhibited an increasing rate of coral bleaching in response to increasing concentrations of BP-2. BP-2 is a genotoxicant to corals, exhibiting a strong positive relationship between DNA-AP lesions and increasing BP-2 concentrations. BP-2 exposure in the
light induced extensive necrosis in both the epidermis and gastrodermis. In contrast, BP-2 exposure in darkness induced autophagy and autophagic cell death. The LC50 of BP-2 in the light for an 8 and 24 h exposure was 120 and 165 parts per billion (ppb), respectively. The LC50s for BP-2 in darkness for the same time points were 144 and 548 ppb. Deformity EC20 levels (24
h) were 246 parts per trillion in the light and 9.6 ppb in darkness.

Annual Reviews.org: Climate change influences on marine infectious disease: implications for management and society by Burge, Eakin, Friedman, Froelich, Hershberger, Hoffman, Petes, Preager, Weil, Willis, Ford and Harvell.

2014. *Annual Reviews in Marine Science*. 6: 249-277

Available online:
http://www.annualreviews.org/doi/abs/10.1146/annurev-marine-010213-135029

Climate Change Influences on Marine Infectious Diseases: Implications for Management and Society
Annual Review of Marine Science
Vol. 6: 249-277 (Volume publication date January 2014)
First published online as a Review in Advance on June 27, 2013
DOI: 10.1146/annurev-marine-010213-135029

Colleen A. Burge,1 C. Mark Eakin, Carolyn S. Friedman, Brett Froelich, Paul K. Hershberger, Eileen E. Hofmann, Laura E. Petes, Katherine C. Prager, Ernesto Weil, Bette L. Willis, Susan E. Ford, and C. Drew Harvell1
1Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853; email: cab433@cornell.edu, cdh5@cornell.edu*

ABSTRACT

Infectious diseases are common in marine environments, but the effects of a changing climate on marine pathogens are not well understood. Here we review current knowledge about how the climate drives host-pathogen interactions and infectious disease outbreaks. Climate-related impacts on marine diseases are being documented in corals, shellfish, finfish, and humans; these impacts are less clearly linked for other organisms. Oceans and people are inextricably linked, and marine diseases can both directly and indirectly affect human health, livelihoods, and well-being. We recommend an adaptive management approach to better increase the resilience of ocean systems vulnerable to marine diseases in a changing climate. Land-based management methods of quarantining, culling, and vaccinating are not successful in the ocean; therefore, forecasting conditions that lead to outbreaks and designing tools/approaches to influence these conditions may be the best way to manage marine disease.

Special thanks to Coral-list post by Colleen Burge

PLOS ONE: Hyperspectral Sensing of Disease Stress in the Caribbean Reef-Building Coral, Orbicella faveolata – Perspectives for the Field of Coral Disease Monitoring by David A. Anderson, Roy A. Armstrong, Ernesto Weil

http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0081478

Published: December 04, 2013
DOI: 10.1371/journal.pone.0081478

Abstract

The effectiveness of management plans developed for responding to coral disease outbreaks is limited due to the lack of rapid methods of disease diagnosis. In order to fulfill current management guidelines for responding to coral disease outbreaks, alternative methods that significantly reduce response time must be developed. Hyperspectral sensing has been used by various groups to characterize the spectral signatures unique to asymptomatic and bleached corals. The 2010 combined bleaching and Caribbean yellow band disease outbreak in Puerto Rico provided a unique opportunity to investigate the spectral signatures associated with bleached and Caribbean yellow band-diseased colonies of Orbicella faveolata for the first time. Using derivative and cluster analyses of hyperspectral reflectance data, the present study demonstrates the proof of concept that spectral signatures can be used to differentiate between coral disease states. This method enhanced predominant visual methods of diagnosis by distinguishing between different asymptomatic conditions that are identical in field observations and photographic records. The ability to identify disease-affected tissue before lesions become visible could greatly reduce response times to coral disease outbreaks in monitoring efforts. Finally, spectral signatures associated with the poorly understood Caribbean yellow band disease are presented to guide future research on the role of pigments in the etiology.

Oregon State University: Large study shows pollution impact on coral reefs — and offers solution

Contact: Rebecca Vega-Thurber
Rebecca.vega-thurber@oregonstate.edu
541-737-1851

diver

IMAGE: Diver Andrew Schantz of Florida International University studies the effect of pollution on corals in the Florida Keys.
Click here for more information.

CORVALLIS, Ore. – One of the largest and longest experiments ever done to test the impact of nutrient loading on coral reefs today confirmed what scientists have long suspected – that this type of pollution from sewage, agricultural practices or other sources can lead to coral disease and bleaching.

A three-year, controlled exposure of corals to elevated levels of nitrogen and phosphorus at a study site in the Florida Keys, done from 2009-12, showed that the prevalence of disease doubled and the amount of coral bleaching, an early sign of stress, more than tripled.

However, the study also found that once the injection of pollutants was stopped, the corals were able to recover in a surprisingly short time.

“We were shocked to see the rapid increase in disease and bleaching from a level of pollution that’s fairly common in areas affected by sewage discharge, or fertilizers from agricultural or urban use,” said Rebecca Vega-Thurber, an assistant professor in the College of Science at Oregon State University.

“But what was even more surprising is that corals were able to make a strong recovery within 10 months after the nutrient enrichment was stopped,” Vega-Thurber said. “The problems disappeared. This provides real evidence that not only can nutrient overload cause coral problems, but programs to reduce or eliminate this pollution should help restore coral health. This is actually very good news.”

The findings were published today in Global Change Biology, and offer a glimmer of hope for addressing at least some of the problems that have crippled coral reefs around the world. In the Caribbean Sea, more than 80 percent of the corals have disappeared in recent decades. These reefs, which host thousands of species of fish and other marine life, are a major component of biodiversity in the tropics.

coral

IMAGE: This coral, which was part of a scientific study, is bleached as a result of exposure to elevated levels of nitrogen and phosphorus.
Click here for more information.

Researchers have observed for years the decline in coral reef health where sewage outflows or use of fertilizers, in either urban or agricultural areas, have caused an increase in the loading of nutrients such as nitrogen and phosphorus. But until now almost no large, long-term experiments have actually been done to pin down the impact of nutrient overloads and separate them from other possible causes of coral reef decline.

This research examined the effect of nutrient pollution on more than 1,200 corals in study plots near Key Largo, Fla., for signs of coral disease and bleaching, and removed other factors such as water depth, salinity or temperature that have complicated some previous surveys. Following regular injections of nutrients at the study sites, levels of coral disease and bleaching surged.

One disease that was particularly common was “dark spot syndrome,” found on about 50 percent of diseased individual corals. But researchers also noted that within one year after nutrient injections were stopped at the study site, the level of dark spot syndrome had receded to the same level as control study plots in which no nutrients had been injected.

The exact mechanism by which nutrient overload can affect corals is still unproven, researchers say, although there are theories. The nutrients may add pathogens, may provide the nutrients needed for existing pathogens to grow, may be directly toxic to corals and make them more vulnerable to pathogens – or some combination of these factors.

“A combination of increased stress and a higher level of pathogens is probably the mechanism that affects coral health,” Vega-Thurber said. “What’s exciting about this research is the clear experimental evidence that stopping the pollution can lead to coral recovery. A lot of people have been hoping for some news like this.

“Some of the corals left in the world are actually among the species that are most hardy,” she said. “The others are already dead. We’re desperately trying to save what’s left, and cleaning up the water may be one mechanism that has the most promise.”

VIDEO: This is an interview with Rebecca Vega-Thurber about new findings in a coral reef study off the Florida Keys.
Click here for more information.

Nutrient overloads can increase disease prevalence or severity on many organisms, including plants, amphibians and fish. They’ve also long been suspected in coral reef problems, along with other factors such as temperature stress, reduced fish abundance, increasing human population, and other concerns.

However, unlike factors such as global warming or human population growth, nutrient loading is something that might be more easily addressed on at least a local basis, Vega-Thurber said. Improved sewage treatment or best-management practices to minimize fertilizer runoff from agricultural or urban use might offer practical approaches to mitigate some coral reef declines, she said.

###

Collaborators on this research included Florida International University and the University of Florida. The work was supported by the National Science Foundation and Florida International University.

Editor’s Note: Digital images are available to illustrate this research:

Diver at study site: http://bit.ly/16bCW7w

Bleached coral: http://bit.ly/1bzLpjm

Nutrient dispenser: http://bit.ly/16gC8cp

A package of video interviews and associated B-roll, including underwater video, is also available for downloading in high resolution format:

Underwater b-roll:

http://oregonstate.edu/dept/ncs/media/rebecca-vega-thurber-underwater-b-roll-news-release.mov

Package interview with Dr. Rebecca Vega Thurber:

http://oregonstate.edu/dept/ncs/media/rebecca-vega-thurber-package-news-release.mov

Dr. Rebecca Vega Thurber Interview:

http://oregonstate.edu/dept/ncs/media/rebecca-vega-thurber-interview-news-release.mov

Laboratory b-roll:

http://oregonstate.edu/dept/ncs/media/rebecca-vega-thurber-b-roll-news-release.mov

Rebecca Vega Thurber Interview (audio only):

PLOS ONE: RNA-seq Profiles of Immune Related Genes in the Staghorn Coral Acropora cervicornis Infected with White Band Disease by Silvia Libro mail, Stefan T. Kaluziak, Steven V. Vollmer

http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0081821

Published: Nov 21, 2013
DOI: 10.1371/journal.pone.0081821

Abstract

Coral diseases are among the most serious threats to coral reefs worldwide, yet most coral diseases remain poorly understood. How the coral host responds to pathogen infection is an area where very little is known. Here we used next-generation RNA-sequencing (RNA-seq) to produce a transcriptome-wide profile of the immune response of the Staghorn coral Acropora cervicornis to White Band Disease (WBD) by comparing infected versus healthy (asymptomatic) coral tissues. The transcriptome of A. cervicornis was assembled de novo from A-tail selected Illumina mRNA-seq data from whole coral tissues, and parsed bioinformatically into coral and non-coral transcripts using existing Acropora genomes in order to identify putative coral transcripts. Differentially expressed transcripts were identified in the coral and non-coral datasets to identify genes that were up- and down-regulated due to disease infection. RNA-seq analyses indicate that infected corals exhibited significant changes in gene expression across 4% (1,805 out of 47,748 transcripts) of the coral transcriptome. The primary response to infection included transcripts involved in macrophage-mediated pathogen recognition and ROS production, two hallmarks of phagocytosis, as well as key mediators of apoptosis and calcium homeostasis. The strong up-regulation of the enzyme allene oxide synthase-lipoxygenase suggests a key role of the allene oxide pathway in coral immunity. Interestingly, none of the three primary innate immune pathways – Toll-like receptors (TLR), Complement, and prophenoloxydase pathways, were strongly associated with the response of A. cervicornis to infection. Five-hundred and fifty differentially expressed non-coral transcripts were classified as metazoan (n = 84), algal or plant (n = 52), fungi (n = 24) and protozoans (n = 13). None of the 52 putative Symbiodinium or algal transcript had any clear immune functions indicating that the immune response is driven by the coral host, and not its algal symbionts.
Figures

Citation: Libro S, Kaluziak ST, Vollmer SV (2013) RNA-seq Profiles of Immune Related Genes in the Staghorn Coral Acropora cervicornis Infected with White Band Disease. PLoS ONE 8(11): e81821. doi:10.1371/journal.pone.0081821

Editor: Kenneth Söderhäll, Uppsala University, Sweden

Received: August 22, 2013; Accepted: October 24, 2013; Published: November 21, 2013

Copyright: © 2013 Libro et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: Grant funding was provided by the NSF to Steve Vollmer (NSF-OCE 0751666). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

The global rise in disease epidemics linked to climate change has taken a heavy toll on tropical reef-building corals and the diverse ecosystems they support [1-4]. A prime example is White Band Disease (WBD), which beginning in the late 1970s [5], caused unprecedented Caribbean-wide die-offs of two species of Acropora corals, the Staghorn coral A. cervicornis and the Elkhorn coral A. palmata [6-8]. As a result, both species are now listed as threatened on the US Endangered Species Act [9] and as critically endangered under the International Union for the Conservation of Nature (IUCN) Red List criteria [4]. Despite the devastating impacts of coral diseases on reefs world-wide, little is known about the basic etiology and ecology of most coral diseases [10-12] including basic information about how corals fight diseases [2,12,13], even though information about the coral immune response may be crucial to understanding the future resiliency of reef corals [2].

Genetic surveys indicate that corals and other cnidarians possess the genetic architecture underlying common innate immune pathways, including Toll-like receptors (TLR) as well as components of the complement and prophenoloxidase (PO) pathways [10,14,15]. PO activity and melanization responses have been elicited in corals exposed to pathogens [16-18] and components of the TLR pathway were differentially expressed in corals infected with non-host specific Symbiodinium types [19]. Elements of the complement pathway, such as mannose-binding lectins, appear to be involved in pathogen, symbiont, and self/nonself recognition in Acropora millepora [20]. Although cnidaria lack specialized immune cells, such as macrophages, cnidaria possess mobile amebocytes that are activated upon pathogen exposure or tissue damage [21-24]. Phagocytosis activity in cnidarians is commonly observed in flagellate gastrodermal cells during food uptake [25]. However, several studies have demonstrated that, upon immune stimulation, different populations of amebocytes can exhibit phagocitic activity directed toward wound healing and removal of necrotic tissue, as well as encapsulation of foreign particles [26,27].

Relatively few studies have studied the genetic response of corals infected with disease [28,29]. A microarray study of Pocillopora damicornis infected with Vibrio identified six candidate immune genes including three lectins and three putative antimicrobial proteins [28]. Exposure of A. millepora to bacterial and viral pathogen associated molecular patterns (PAMPs) resulted in up-regulation of few immune related genes including three GTPase of immunity associated proteins (GiMAP) [29], a family of conserved small GTPases involved in the antibacterial response of plants and mammals [30].

White Band Disease represents a good system to investigate the immune response of a reef-building coral. It is one of the few coral diseases that is highly transmissible [31] and host-specific [5,11]. WBD is characterized by an interface of white dying tissue that advances rapidly along the coral colony (Figure 1). Current evidence suggests that the pathogen is bacterial [31-36], but Henle-Koch postulates have not been satisfied. To date, multiple bacteria have been associated with WBD infections, including Vibrio harveyi [33,37] as well as a marine Rickettsia CAR1α [34]. In situ transmission experiments have identified naturally resistant and susceptible genotypes of A. cervicornis [31], indicating that the immune response to WBD varies among individuals.

Figure 1

Figure 1. White Band Disease on Acropora cervicornis.

A colony of the Staghorn coral A. cervicornis infected with White Band Disease showing the characteristic white band of dying and necrotic coral tissue.
doi:10.1371/journal.pone.0081821.g001

Here we used next-generation RNA-sequencing to produce a transcriptome-wide profile of the immune response of A. cervicornis to WBD by comparing infected versus healthy (asymptomatic) coral tissues. The transcriptome of A. cervicornis was assembled de novo from A-tail selected mRNA-seq data from whole coral tissues, and parsed bioinformatically into coral and non-coral transcripts using existing Acropora genomes in order to identify putative coral transcripts. Differentially expressed transcripts were identified in the coral and non-coral datasets to identify which genes were up- and down-regulated due to disease infection and characterize the immune response of the coral.
Results

A de novo assembly of the A. cervicornis transcriptome was assembled from 436.5 million Illumina RNA-sequencing reads from 45 coral samples of A. cervicornis and A. palmata. The total reads were de novo assembled using Trinity [38], resulting in 95,389 transcripts, with a N50 of 363 and N75 of 696. A total of 47,748 transcripts mapped against the existing Acropora genomes [39,40] and were classified as putative coral transcripts while the remaining 47,641 were classified as non-coral transcripts (Table 1).

Table 1. Summary of coral and non-coral transcripts.
Total number of transcripts (n), significantly differentially expressed transcripts (adj p-val<0.05) (DE), number of up-regulated (up) and down-regulated (down) transcripts among the entire dataset and annotated transcripts only (E-val<10-5). First row refers to putative coral transcripts, second row to non-coral transcripts. For this study, five diseased (i.e. infected) and six healthy corals were used to profile the immune response of Staghorn corals infected with WBD. The average number of putative coral reads (±SE) was 4,076,829 (± 898,542) in the diseased coral samples compared to 4,199,946 (±761,894) in the healthy samples. In total, 20,503 coral transcripts (43 %) and 14,253 (30%) non-coral transcripts had strong protein annotations (Blastx e-value < 10-5) (Table 1). Differentially expressed coral transcripts Statistical analysis in DEseq [41] identified 1,805 differentially expressed (DE) transcripts (adj p-value < 0.05) between healthy and WBD coral samples (Table 1, Table S1); 559 of these DE transcripts had reliable protein annotations (Blastx e-values < 10-5) that could be used to characterize the immune response of A. cervicornis infected with WBD (Figure 2a, Figure 3). Annotated transcripts were characterized by gene ontology (GO) and grouped into manually curated categories based on literature searches highlighting immune functions (Table 2). WBD-infected corals exhibited strong gene expression responses for genes related to immunity (n = 72), apoptosis (n = 18) and arachidonic acid metabolism (n = 5). Calcification (n = 14) and calcium homeostasis (n = 21) were also perturbed, as well as cell growth and remodeling (n = 134), cellular processes (n = 188) and general metabolism (n = 43). figure 2

Figure 2. Volcano plots displaying differential gene expression between healthy and disease A. cervicornis.

Figure a. plots gene expression values of the putative coral transcripts, figure b. plots putative non coral transcripts. Each point represents an individual gene transcript. Red points represent significantly differentially expressed transcripts (adj p-value < 0.05). doi:10.1371/journal.pone.0081821.g002 figure 3

Figure 3. Heatmap of immune-related differentially expressed coral transcripts.

Table 2
Table 2. Summary of the main pathways involved in A.cervicornis response to WBD.
Number (N) of differentially expressed (DE) transcripts per category. Function defined by GO terms and manually curated categories. Expression values reported as log2fold change of WBD infected corals relative to healthy corals.

Immune-related processes

Sixty-nine DE transcripts were associated with immunity. Three C-type lectins receptors, C- type mannose receptor 2 (MRC2), macrophage lectin 2 (CLEC10A) and collectin-12 (COLEC12) were up-regulated in infected corals. Two mediators of phagocytosis were up-regulated – the macrophage receptor multiple epidermal growth factor-like domains protein 10 (MEGF10) and actin-22 (act22), which is involved in the phagosome formation. All three subunits of NADPH oxidase (NOX) involved in reactive oxygen species (ROS) production were up-regulated, including cytochrome b-245 heavy chain (CYBB), NADPH oxidase 3 (NOX3) and neutrophil cytosol factor 2 (p67-phox). Other DE immune related genes included nine antioxidants participating in the detoxification of ROS such as peroxidasin (PXDN, n=3) and glutaredoxin (GLRX), and 12 transcripts associated to response to stress such as golgi-associated plant pathogenesis-related protein 1 (GAPR-1, n = 3) and universal stress protein A-like protein (UspA, n = 2).

Little or no differential expression was detected in the three primary innate immune pathways – Toll/TLR, complement and prophenoloxidase (PO) pathways. In the Toll/TLR pathway, two TLR2 homologs and the adaptor molecule TNF receptor-associated factor 3 (TRAF3) were up-regulated in WBD corals. In the complement pathway, two transcripts encoding macrophage-expressed gene protein 1 (MPEG1) were differentially expressed, but they were down regulated in WBD corals. No differentially expressed transcripts were detected in the PO pathway.
Arachidonic acid metabolism

Six DE transcripts participating to the metabolism of arachidonic acid (AA) were up-regulated in diseased corals. Five matched coral allene oxide synthase-lipoxygenase (AOSL), a catalase related hemoprotein that catalyzes the biosynthesis of allene oxide, a precursor of marine eicoesanoids. The sixth transcript matched the enzyme phospholipase A2 (PLA2), involved formation of AA from membrane phospholipids.
Apoptosis

Eighteen DE transcripts were associated with apoptosis, including both pro- and anti-apoptotic regulators such as the extracellular matrix protein thrombospondin 2 and fibroblast growth factor receptor 2 (n = 2), respectively. Tumor necrosis factor receptor superfamily member 1A (TNFRSF1A) and caspase 3 (CASP-3) were up-regulated while caspase 8 (CASP-8) was down-regulated in WBD corals.
Calcification and calcium homeostasis

DE transcripts in this category included 14 proteins participating to carbon dioxide transport, biomineralization and skeletal growth. Two carbonic anhydrases were up-regulated (CA2 and CA3) and one was down-regulated (CA2) in WBD corals. Mediators of calcium homeostasis included 27 DE transcripts participating in calcium ion binding and transport such as calmodulin (CaM, n = 3), calumenin (CALU) and calsequestrin-2 (CASQ2) and were all up-regulated.
Cell growth and remodeling

Among the 138 DE transcripts related to cell growth and remodeling we identified 17 metallopeptidases (15 up, 2 down), 29 cytoskeletal proteins (all up-regulated) and 14 angiogenesis mediators (11 up, 3 down). A large group of DE transcripts were cell adhesion proteins (n = 29), including four up-regulated transcripts encoding sushi, von Willebrand factor type A, EGF and pentraxin domain-containing protein 1 (polydom/SVEP1).
Cell metabolism

Forty-two DE transcripts were associated with cell metabolism. These included 14 mediators of lipid metabolism, in particular, five lipases involved in lipid and phospholipid catabolism (n = 5, all up), such as pancreatic triacylglycerol lipase (PL), pancreatic lipase-related protein 2 (PL-RP2) and phospholipase DDHD1 (DDHD1). Four transcripts participating in fatty acid biosynthesis, such as fatty acid synthase (FASN), acetyl-CoA carboxylase (ACC) and acetyl-CoA carboxylase 1 (ACC1), were all down-regulated in WBD corals, and five transcripts involved in the breakdown of fatty acids such as long-chain-fatty-acid–CoA ligase 1 (LACS1) and 5 (LACS5) were up-regulated.
Non-coral transcripts

Out of the 47,641 putative non-coral transcripts in the dataset, 550 were differentially expressed in WBD infected corals (Table 1, Table S2). Of these 550 DE transcripts, 251 were well-annotated and were all up-regulated (Figure 2b). About 33 % were metazoan, the remaining were putative zooxanthellae (23%), fungi (10%) and protozoa (5%). A small number of transcripts matched bacteria (4%) and viruses (0.1%), while the remaining 23 % were unknown.

Metazoan transcripts (n = 84) included mediators of cell growth and remodeling (n = 16), metabolism (n = 4), cellular processes (n = 61) and two uncharacterized transcripts. Only two immune-related transcripts were identified and were the antioxidant peroxiredoxin-2 (PRDX2) and the metallopeptidase aminopeptidase O (AP-O), which may be involved in leukotrienes synthesis from AA.

Fifty-nine transcripts had plant, algae or Alveolata protein IDs and are presumed or putative Symbiodinum transcripts. Based on GO terms, these Symbiodinium transcripts were associated with cell growth and remodeling (n = 8), cellular processes (n= 38) and metabolism (n = 10), while two were uncharacterized. One transcript matched cysteine proteinase RD21a (RD21), a peptidase involved in defense against fungi. Fungal transcripts (n = 24) belonged to cell processes (n = 20) and metabolism (n = 3) plus one uncharacterized protein. Out of the 14 transcripts matching protozoa, 13 were associated to cellular processes, two to metabolism and one to cell growth and remodeling.

Nine transcripts matched bacterial proteins, six of them were involved in cellular processes (n = 3), metabolism (n = 3) and three were uncharacterized. Two transcripts shared protein IDs annotating to virus proteins (glycoprotein gp2 and one uncharacterized), while the remaining 59 transcripts did not have functional annotations.
Discussion

Our study demonstrates that Acropora cervicornis mounts a vigorous immune response against White Band Disease (WBD) pathogen(s) involving dramatic changes in gene expression across 4% of the coral transcriptome. The identities of the differentially expressed (DE) coral transcripts indicate that the response of A. cervicornis to WBD infection is driven by phagocytosis of apoptotic cells (Figure 3, Table 2). Corals infected with WBD exhibited strong differential expression of transcripts involved in macrophage-mediated pathogen recognition and ROS production, two hallmarks of phagocytosis, as well as key mediators of apoptosis and calcium homeostasis. The strong up-regulation of transcripts involved in arachidonic acid (AA) metabolism and allene oxide synthesis suggests their key role in coral immunity.

The primary signature of phagocytosis activity in WBD infected corals was the up-regulation of four macrophage receptors that recognize and bind to conserved motifs on the surface of target cells. Three of these receptors, MRC2, CLEC10A and COLEC12 belong to the C-type lectin family of proteins that include several Pathogen Recognition Receptors (PRRs). MRC2 recognizes mannose and fucose on glycoproteins of bacteria, viruses and fungi [42] while CLEC10A recognizes galactose and N-acetyl-galactosamine residues [43]. COLEC12is a scavenger receptor that shares structural similarity with macrophage scavenger receptor class A type I (SR-AI), a surface membrane receptor that mediates binding and phagocytosis of gram-positive, gram-negative bacteria and yeasts [44]. The fourth receptor, MEGF10, is membrane protein that promotes the clearance of apoptotic cells by causing macrophages to adhere and engulf them [45]. The stronger up-regulation of the three macrophage PRRs (2.2, 5.4 and 4.1 fold) compared to the one apoptotic cell recognizing receptor MEGF10 (2.17 fold) suggests the response is primarily driven by phagocytosis of microbes. A second signature of phagocytosis was the up-regulation of transcripts linked to ROS production, including three subunits of the enzymatic complex NADPH oxidase (NOX). ROS production is a general and highly conserved response to invading pathogens and stress and the release of ROS from the mitochondria can induce apoptosis in metazoan and yeasts [46,47]. During phagocytosis, ROS are generated in mature phagosomes (i.e. specialized vacuoles in phagocytic cells) [48] to kill engulfed cells [49]. In cnidarians, ROS production has been observed in the hydroid Hydra vulgaris exposed to the immune stimulant lipopolysaccaride (LPS) [50] and in reef corals during thermal and UV-induced bleaching [51,52], possibly due to the breakdown of the mitochondrial and photosynthetic membranes [53,54].

In WBD infected corals, it is possible that phagocytosis is aimed either at the removal of invading pathogens and/or used to clear damaged apoptotic cells [55]. The genetic signature of phagocytosis in WBD infected corals raises questions about the identity of these phagocytic immune cells in A. cervicornis. Cnidaria lack specialized immune cells, but do possess mobile amebocytes. Aggregations of amebocytes have been observed in the gorgonian coral Gorgonia ventalina infected with pathogenic fungi [24] and near wounded tissues in the soft coral Plexaurella fusifera [26]. Histological examination revealed that amebocytes exhibited phagocytic and PO activity [27] as well as antimicrobial activity against Gram-negative bacteria and ROS production [56]. Interestingly, certain populations of ameboid cells always show phagocytic activity, while others only acquire it upon immune activation [27]. These findings indicate that cnidaria, traditionally considered “simple” animals, are able to mount an innate immune response by employing the functional plasticity of amebocytes, which seem to represent the primary immune population of phagocytic cells.

Increased apoptosis in WBD infected corals was indicated by the differential expression of TNFRSF1A and CASP-3. During apoptosis, TNFRSF1A binds to tumor necrosis factor (TNF), which then recruits CASP-8 initiating the downstream activation of CASP-3, the main effector caspase of the apoptotic pathway [57,58]. While both TNFRSF1A and CASP-3 are up-regulated, CASP-8 is down-regulated which may suggest that CASP-3 is activated by some alternative pathway. Active programmed cell death was also suggested by disruption of calcium homeostasis as indicated by the strong up-regulation of CaM and other calcium binding proteins. In both plants and animals [59,60], apoptosis can be triggered by LPS from gram-negative bacteria via alteration of TNFRSF1A expression [61]. Some bacterial pathogens are also able to induce or inhibit apoptosis in their host [60,62,63] via alteration of membrane permeability and disruption of Ca2+ homeostasis [64], direct activation of TNF-α [65], TLR2 [66,67]or CASP-3 [68]. In corals, apoptosis occurs normally during metamorphosis [69] and the onset of symbiosis [70], but it has also been observed during bleaching as a possible mechanism to expel zooxanthellae in response to thermal stress [71-73]. Apoptosis has also been detected in the lesions of three Pacific species of Acropora infected by White Syndrome (WS), suggesting that it is a mechanism of tissue loss in WS [74].

Another key, yet unexpected, finding of this study is the potential role of the arachidonic acid (AA) pathway in the coral immune response. Genes involved in AA synthesis increased dramatically in WBD infected corals. The role of AA as an inflammation regulator is well-known in metazoans [75] , but has not been described in Cnidaria or in association with any coral disease. In metazoans, AA is released by apoptotic cells as chemotactic factor to promote clearance by phagocytes [76], but it can also induce apoptosis via rapid increase of calcium concentration and activation of CASP-3 in a CASP-8-independent way [77]. These findings are consistent with our data showing up-regulation of CASP-3, but not CASP-8, suggesting that AA may act similarly as immunomodulator in A. cervicornis. The five transcripts matching allene oxide synthase-lypoxigenases (AOSL) from the soft coral Plexaura homomalla, on the other hand, indicated that AA is converted into allene oxide, an intermediate compound of prostanoid synthesis in plants and soft corals [78-82].

Allene oxide has received considerable attention as a putative precursor of clavulones [83], a class of unique marine prostanoids known for their anti-viral and anti-cancer activity [84,85]. The link between the AOSL pathway and clavulones synthesis in corals, although still under debate, was suggested by the similarities with the biosynthetic pathway of jasmonic acid [83] a plant hormone that is produced via an allene oxide intermediate upon mechanical injury [86] and herbivore attack [87]. Although further study is needed to understand the role allene oxide in corals, our data represent the first evidence implicating AOSL in coral immunity and suggest that AOSL may be involved in controlling levels of free AA produced by apoptotic cells.

Several other immune related genes exhibited altered expression in infected corals. The majority were anti-oxidants including PXDN, peroxidasin-like proteins and GLRX – a glutathione-dependent enzyme. PXDN has been shown to be DE in some thermally stressed corals, but not in a consistent manner. For example, in Montastraea faveolata, PXDN was up-regulated in thermally-stressed larvae [88], but was down-regulated in thermally-bleached adult colonies [89]. Active cell remodeling and cell matrix degradation was indicated by several DE cytoskeletal proteins, metalloproteases and cell adhesion proteins, probably associated with cellular and cytoskeletal rearrangements linked to phagocytosis and apoptosis. CASP-3 activation, in particular, initiates apoptosis by altering the expression of metalloproteases and hydrolytic enzymes such as cathepsins that degrade extracellular matrix components [90]. Interestingly, WBD infected corals up-regulated three transcripts encoding polydom, a cell adhesion protein belonging to the pentraxin family of lectins. Recent studies suggest an immune function for polydom based on its similarities in its protein domains to complement proteins and C-type lectins with antimicrobial activity [91]. In cnidarians, the potential immune role for polydom is bolstered by its up-regulation in the hydroid Hydractinia symbiolongicarpus after fungal and bacterial exposure [92].

Surprisingly, none of the three main innate immune pathways – TLR, complement and PO – played a prominent role in the immune signature of A. cervicornis infected with WBD, even though transcripts from these pathways are well-represented in our transcriptome. Only three transcripts in the TLR pathway were differentially expressed: two TLRs matching to human TLR2 and TRAF3. In the lectin complement pathway, the only two DE transcripts were two proteins matching MPEG1, a MAC/PF (membrane attack complex/perforin) containing protein that is involved in the response against Gram negative bacteria in sponges and is up-regulated upon LPS exposure [93]. None of the transcripts belonging to the PO pathway were differentially expressed during WBD infection, even though in other corals PO activity acts as an important defense against invading pathogens and tissue damage [16-18].
Non-coral transcripts

The taxonomic distribution of non-coral transcripts highlighted the presence of several members of the coral holobiont, i.e. the coral host and associated symbiotic microorganisms, including zooxanthellae, fungi and protozoa. The majority of these non-coral transcripts matched metazoan and putative zooxanthaellae proteins, while the remaining transcripts matched fungi, protozoa and bacteria. GO term analysis revealed that most of these non-coral transcripts encoded mediators of cell homeostasis and general metabolism. Transcripts with metazoan identities were likely coral transcripts that did not have identities in the coral reference genomes and may thus represent transcripts unique to A. cervicornis. Putative zooxanthellae transcripts were identified as transcripts annotating to Viridiplantae, Heterokontophyta (i.e. algae), cyanobacteria and the superphylum Alveolata. Interestingly, no genetic signature of immune activity from the algal symbionts was evident in our transcriptome. Instead, our data suggest drastic changes in photosynthesis and cell metabolism of the zooxanthellae; this is consistent with a previous study showing that Symbiodinum undergo major alteration of carbon metabolism in response to stress [94].
Conclusions

Our data reveal that the coral host, but not its algal symbionts, undergoes dramatic alterations in gene expression during response to WBD infection. Transcriptional changes affected mediators of innate immunity, in particular receptors on the surface of phagocytic cells, enzymes involved in ROS production and modulators of apoptosis. Taken together, our data suggest that WBD infection in A. cervicornis is associated with apoptosis, and that WBD pathogen triggers a powerful immune response driven by phagocytic cells that encapsulate and degrade apoptotic cells. This study also indicates a key role for arachidonic acid and in particular the enzyme AOSL in A. cervicornis immunity.
Materials and Methods

Total RNA was extracted from diseased and healthy Acropora cervicornis sampled from Crawl Cay reef in Bocas del Toro, Panama under Autoridad Nacional del Ambiente (ANAM) Collecting permit SE/A-71-08. For the diseased samples, corals with active mobile WBD interfaces were identified by monitoring the mobility of disease interfaces for two days, and then sampling a 2 cm region of tissue at and above the disease interface. A comparably sized and located tissue sample was taken from healthy (i.e. asymptomatic) corals. The coral tissues were flash frozen in liquid nitrogen and stored at -80°C. Total RNA was extracted in TriReagent (Molecular Research Center, Inc.) following the manufacturer’s protocol. Total RNA quality was assessed using the RNA Pico Chips on an Agilent Bioanalyzer 2100, and only extractions showing distinctive 28S and 18S bands and RIN values of 6 or higher were prepped for RNA sequencing.

RNA sequencing was performed on five diseased and six healthy coral samples using a multiplexed Illumina mRNA-seq protocol [95] with the following modifications. Instead of fragmenting the mRNA prior to cDNA synthesis, we obtained much better success fragmenting the double stranded cDNA using DNA fragmentase (New England Biolabs) for 30 minutes at 37°C. RNA-seq libraries were then prepared using next-generation sequencing modules (New England Biolabs) and custom paired-end adapters with 4bp barcodes. Multiplexed samples were run (2-3 samples per lane) on the Illumina GAII platform (Illumina, Inc, San Diego, California, USA) at the FAS Center for System Biology at Harvard University. Barcoded samples were de-multiplexed and raw sequencing reads were quality trimmed to remove sequences and regions with a Phred score of less than 30 and a read length less than 15bp long using custom Perl Scripts in the FASTX-Toolkit (http://hannonlab. cshl.edu/fastx_toolkit/).

A de novo transcriptome was assembled using Trinity [38] from 463.5 million single-end Illumina RNA-Seq reads from 39 A. cervicornis and 6 A. palmata samples, including the 11 A. cervicornis samples included in this paper. The assembled transcriptome produced 95,389 transcripts with a N50 of 363 and N75 of 696. RNA-seq data were produced using whole coral tissue, which putatively contains sequences from the coral host, its algal symbiont Symbiodinium, and other members of the coral holobiont (e.g. fungi, bacteria, and viruses).

In order to resolve the holobiont, and putatively classify the source of the transcripts that were assembled as either coral or non-coral, we utilized a multistep pipeline leveraging the existing genomes of two congener species – A. digitifera [39] and A. millepora [40]. RNA-seq reads were mapped against both Acropora reference genomes using Bowtie [96] to produce two exomes. Transcripts from our de novo assembly were aligned using BLAST [97] against each exome. Transcripts were assigned as putatively coral if they matched either exome with an e-value of less than 10-10. Transcripts without significant coral hits were assigned as non-coral and could potentially include novel coral and/or algal symbiont Symbiodinium transcripts, as well as other associated eukaryotes, like endolithic fungi. Bacterial and viral transcripts are possible, but less likely given that A-tail selection to isolate eukaryotic mRNAs was performed prior to cDNA synthesis.

Putative gene identities for each transcript were identified by performing homology searches against the Swiss-Prot and TReMBLE protein databases [98], using tBLASTx. Matches with an e-value of less than10-5 were considered homologous protein-coding genes. Subsequently, GenBank Flat Files corresponding to the hits’ Accession ID’s were downloaded and used to extract taxonomic data for each used as a second method to identify the putative source of the transcripts. GO terms and gene functions were obtained for the annotated transcripts on UniProt. The reference transcriptome sequences are available on Bioproject (accession number PRJNA222758).

Differences in gene expression between healthy and disease A.cervicornis specimens were estimated using the R package DESeq [38]. First, all contigs were separated into two datasets –i.e. coral and non-coral- based on their matches to the Acropora genomes. Size factor estimation and normalization were then performed separately on each dataset using the functions estimateSizeFactors and estimateDispersions, respectively. Differentially expressed contigs were detected by running a negative binomial test using the function nbinomTest. Only differentially expressed transcripts (adjusted p-value < 0.05) that were also annotated (e-values < 10-5) were used for this study. Supporting Information Table_S1.xlsx Table_S1

Table S2.

Dataset of annotated (E-val<10-5 ) non-coral transcripts exhibiting differential expression between healthy and diseased samples (adj p-val<0.05). Table s2

Acknowledgments

The authors would like to thank Elizabeth Hemond for helping with sample collection and library preparation, Laura Geyer and the Smithsonian Tropical Research Institute and the for field and logistical support and the members of the Vollmer lab for valuable comments. Collection permits were provided by Autoridad Nacional del Ambiente (ANAM) SE/A-71-08.
Author Contributions

Conceived and designed the experiments: SV. Performed the experiments: SL. Analyzed the data: SL STK. Contributed reagents/materials/analysis tools: SV. Wrote the manuscript: SL SV.
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ISME Journal via Coral-list: Bacterial profiling of White Plague Disease in a comparative coral species framework

The ISME Journal advance online publication 8 August 2013; doi: 10.1038/ismej.2013.127

Open–find complete paper with tables at:
http://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2013127a.html

Cornelia Roder1, Chatchanit Arif1, Till Bayer1, Manuel Aranda1, Camille Daniels1, Ahmed Shibl1, Suchana Chavanich2 and Christian R Voolstra1

1Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
2Department of Marine Science, Faculty of Science, Chulalongkorn University, Reef Biology Research Group, Bangkok, Thailand

Correspondence: CR Voolstra, Red Sea Research Center, King Abdullah University of Science and Technology, Building 2, Room 2226, Thuwal 23955, Saudi Arabia. E-mail: christian.voolstra@kaust.edu.sa

Received 23 January 2013; Revised 19 June 2013; Accepted 1 July 2013
Advance online publication 8 August 2013

Abstract

Coral reefs are threatened throughout the world. A major factor contributing to their decline is outbreaks and propagation of coral diseases. Due to the complexity of coral-associated microbe communities, little is understood in terms of disease agents, hosts and vectors. It is known that compromised health in corals is correlated with shifts in bacterial assemblages colonizing coral mucus and tissue. However, general disease patterns remain, to a large extent, ambiguous as comparative studies over species, regions, or diseases are scarce. Here, we compare bacterial assemblages of samples from healthy (HH) colonies and such displaying signs of White Plague Disease (WPD) of two different coral species (Pavona duerdeni and Porites lutea) from the same reef in Koh Tao, Thailand, using 16S rRNA gene microarrays. In line with other studies, we found an increase of bacterial diversity in diseased (DD) corals, and a higher abundance of taxa from the families that include known coral pathogens (Alteromonadaceae, Rhodobacteraceae, Vibrionaceae). In our comparative framework analysis, we found differences in microbial assemblages between coral species and coral health states. Notably, patterns of bacterial community structures from HH and DD corals were maintained over species boundaries. Moreover, microbes that differentiated the two coral species did not overlap with microbes that were indicative of HH and DD corals. This suggests that while corals harbor distinct species-specific microbial assemblages, disease-specific bacterial abundance patterns exist that are maintained over coral species boundaries.
Keywords:

16S rRNA gene microarray; Gulf of Thailand; Pavona duerdeni; Porites lutea; coral disease; White Plague Disease (WPD)

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