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Home , Coral disease, Eugene Rosenberg, Zooxanthellae

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> Section V. Ex amples of Diversit y

> Chapter 10. Microbial Communities Oceanography > C. Cor al Reef Microbiology , Volume 2, a quarterly 20, Number The O journal of by Eugene Rosenberg, Christina A . Kellogg, and Forest Rohwer

In the last 30 years, there has been their effects by altering the microbial tains multiple “taxa” (Baker, 2003). A approximately a 30% loss of population and causing certain microbes single species of coral can multiple worldwide, largely due to emerging dis- to become . types of , often contain- ceanography S eases (Harvell et al., 2002, 2007; Hughes ing different clades at different depths et al., 2003). Coral microbiology is a new Associated (Rowan and Knowlton, 1995). Reviews ociety. Copyright 2007 by The O field, driven largely by a desire to under- with Healthy Corals of Symbiodinium diversity, systematics, stand the interactions between corals The coral (host organism plus and relationships to coral diseases are and their symbiotic microorganisms and all of its associated microorganisms) is presented by Baker (2003, 2004). to use this knowledge to eventually pre- a complex system containing microbial vent the spread of coral diseases. representatives of all three domains: The last decade has brought substan- Eucarya, Bacteria, and Archaea, as well Corals provide three general habitats for ceanography S ceanography S tial progress in determining the abun- as numerous (Figure 1). We dis- bacteria: the surface mucus layer, coral

dance and diversity of microorganisms cuss the microorganisms associated with tissue, and the calcium carbonate skel- ociety. A associated with healthy and diseased healthy coral communities in the next eton, each of which has a distinct bac- ociety. S ll rights reserved. P reserved. ll rights corals. Much of this progress is the result few sections, and then turn to the coral terial population (Bourne and Munn, end all correspondence to: [email protected] Th e O or of the introduction of culture-indepen- diseases related to microbes. 2005; Koren and Rosenberg, 2006). It is dent molecular techniques into coral likely that within each of these habitats microbiology (Rohwer et al., 2001). Eucarya (Zooxanthellae) there are microniches. Initially, research ermission is granted to in teaching copy this and research. for use article Republication, systemmatic reproduction, Consideration of the data published to Corals contain endosymbiotic dino- in coral microbiology concentrated on date leads to the hypothesis that envi- flagellates (algae) of the genus the mucus fraction, using culturing tech- ronmental stress factors contributing Symbiodinium, commonly referred to niques. These studies demonstrated that to coral disease, such as climate change, as zooxanthellae. Zooxanthellae pro- the mucus harbors a diverse and abun- water pollution, and overfishing, exert vide a large part of their hosts’ energy dant bacterial community (Ducklow and ceanography S requirements by transferring photo- Mitchell, 1979; Ritchie and Smith, 1997), Eugene Rosenberg ([email protected]) synthetically fixed carbon to the coral including nitrogen fixers (Shashar et al., is Professor, Department of Microbiology, (Fallowski et al., 1984). The algae also 1994; Lesser et al., 2004). The concen- ociety, B PO Tel Aviv University, Tel Aviv, Israel. produce large amounts of molecular tration of colony-forming bacteria in 5 6 Christina A. Kellogg is Microbiologist, oxygen, which allow for efficient respi- the mucus is 10 –10 per ml (Koren and M D 20849-1931, USA ox 1931, Rockville, U.S. Geological Survey Center for Coastal ration by the coral and associated pro- Rosenberg, 2006; Ducklow and Mitchell, and Watershed Studies, St. Petersburg, karyotes. We now know from molecular 1979), about 0.2% of the total counts FL, USA. Forest Rohwer is Assistant evidence that the genus Symbiodinium determined microscopically using a Professor, San Diego State University, San is diverse, containing more than seven common technique for detecting micro- Diego, CA, USA. principal clades, each of which con- organisms called SYBR Gold Staining .

146 Oceanography Vol. 20, No. 2 Figure 1. The coral holobiont consists of Zooxanthellae the coral animal and associated viruses, microbes (both bacteria and archaea), zooxanthellae, and endolithic organisms. Most of the viruses are phages, which attack the microbes. The endolithic organisms include algae, fungi, , and microbes that bore into the coral skeleton. The holobiont likely occupies different niches by mixing and matching different components (i.e., the Hypothesis). Zooxanthellae and protist micrographs by Linda Wegley and Ian Hewson, respectively

Endolithic Algae

Viruses, Bacteria, & Archaea

(Koren and Rosenberg, 2006). Culture-free, DNA-based techniques found on the same coral species that are Bacteria can also be found in coral first applied by Rohwer et al. (2001) geographically separated, while different tissue after removal of the mucus and to the study of coral bacteria provide populations are found on different coral skeleton. The numbers of culturable and useful data on the bacterial commu- species; and (5) different populations total tissue bacteria are similar to those nity associated with different corals are found in mucus and tissue from the found in mucus. However, the abundant (Bourne and Munn, 2005; Koren and same coral fragment. bacterial species associated with coral tis- Rosenberg, 2006; Pantos et al., 2003; sue is very different from those found in Rohwer et al., 2001, 2002; Frias-Lopez Archaea mucus (Bourne and Munn, 2005; Koren et al., 2002; Cooney et al., 2002; Sekar Previously pigeonholed as extremo- and Rosenberg, 2006). et al., 2006; Casas et al., 2004). Certain philes, archaea have been found in a Coral skeletons are porous struc- generalizations are beginning to emerge: number of mesophilic marine niches: tures inhabited by a variety of bacteria. (1) the diversity of bacterial species asso- coastal waters (DeLong 1992; Fuhrman This endolithic community may sat- ciated with a particular coral species is et al., 1992), marsh sediments (Munson isfy 50% of the nitrogen required by high, including a majority of novel spe- et al., 1997), fishes (van der Maarel et the coral (Ferrer and Szmant, 1988). cies; (2) bacteria in a particular coral al., 1998, 1999), sponges (Preston et al., in the skeleton of Oculina community are different from those 1996; Margot et al., 2002; Webster et al., patagonica provide photoassimilates to in the seawater surrounding the coral, 2001), a sea cucumber (McInerney et the coral tissue (Fine and Loya, 2002). suggesting the association is specific; al., 1995), and several species of corals These may be critical for the survival of (3) the species composition of the uncul- (Kellogg, 2004; Wegley et al., 2004). Like the coral during times when it loses its tured bacterial population is completely coral-associated bacterial communities, endosymbiotic algae, a disease referred different from the cultured population; these archaeal communities are distinct to as . (4) similar bacterial populations are from those in surrounding seawater,

Oceanography June 2007 147 they consist of undescribed species, and particles (VLP) in the water above corals. nism by which viruses might be involved different populations appear to inhabit Microscale profiles show that VLP abun- in coral bleaching. However, the field of the mucus and the tissue. The mucus dance is significantly higher closest to coral virology is still extremely under- samples were dominated by euryar- the coral surface. It also appears that studied and a major effort to uncover chaeotes (Kellogg, 2004) and the tissue VLP concentrations are highest above the diversity and identity of coral viruses samples by crenarchaeotes (Wegley et al., healthy and diseased corals, in compari- present in healthy versus stressed corals 2004). Unlike zooxanthellae and bacteria, son to coral rubble (Patten et al., 2006). is desperately needed (Davy et al., 2006). however, there is no evidence of species- The authors suggest that there are fun- specific associations between particular damental shifts in the VLP and bacterial Infectious Diseases of Corals archaea and individual corals. In fact, community in the water associated with Of more than twenty coral diseases there appear to be archaeal generalists; diseased corals. Most of the coral reef- described by coral biologists, the caus- two independent studies found major associated VLPs are phages—viruses that ative agent for only six of the diseases archaeal ribotypes present in multiple infect bacteria (recent work of author has been isolated and characterized species of coral (Kellogg, 2004; Wegley Rohwer and Rebecca Thurber, San Diego (Table 1, Figure 2). et al., 2004). Although both studies State University). However, the effects of included the coral strigosa, they phages on the food-web structure of the Coral Bleaching had no archaea in common. This may be coral reef and coral holobiont still need At the global scale, coral bleaching is the due to a population difference between to be determined. most serious disease threatening coral mucus and tissue or it may indicate a Wilson et al. (2001) show that there is reefs. Coral bleaching is the disruption biogeographical distinction between the a transferable infectious agent, probably of symbioses between coral hosts and study sites (U.S. Virgin Islands versus a , that can cause bleaching in a sea their endosymbiotic Symbiodinium. The Panama and Bermuda). anemone. In a follow-up study, the cor- loss of the microalgae and/or its photo- als Pavona danai, formosa, and synthetic pigments causes the coral to Viruses were shown to pro- lose color in this bleaching process. If Viruses are common components of duce numerous VLPs when heat shocked the process is not reversed within a few the coral reef environment. Seymour (Wilson et al., 2005). VLPs were also weeks or months, depending on the spe- et al. (2005) used flow cytometry to observed in heat-shocked zooxanthellae. cific coral species and the environmental show that there are ~ 5 x 105 virus-like Together, these results suggest a mecha- conditions, the coral will die. In general,

Table 1. Coral Pathogens Disease Coral Host Reference Bleaching Vibrio shiloi Oculina patagonica Kushmaro et al., 1996, 1997 Bleaching and lysis Vibrio coralliilyticus Pocillopora damicornis Ben-Haim and Rosenberg, 2002; Ben-Haim et al., 2003 Aspergillosis Aspergillus sidowii Gorgonians (sea fans) Smith et al., 1996, Geiser et al., 1998 White band Vibrio carchariae* Acropora sp. Ritchie and Smith, 1995 White plague Aurantimonas coralicida Several Denner et al., 2003 White plague (Eilat) Thalassomonas loyana Several Barash et al., 2005; Thompson et al., 2006; Efrony et al., 2007 White pox Serratia marcenscens Acropora palmata Patterson et al., 2002 Yellow blotch Vibrio alginolyticus Monastraea sp. Cervinio et. al., 2004 Black band Consortium* (?) Several Richardson, 2004 * Presumed pathogens, but Koch’s postulates not demonstrated

148 Oceanography Vol. 20, No. 2 coral bleaching coincides with the hottest (Sussman et al., 2003). tion of vibrios. These disease-associated period of the year (Goreau et al., 1997; Vibrio coralliilyticus is an etio- vibrios clustered most closely to Vibrio Hayes and Goreau, 1998) and is most logical agent of bleaching of the coral carchariae. Because infection experi- severe at times of warmer-than-normal Pocillopora damicornis on coral reefs ments with isolated V. carchariae were conditions (Hoegh-Guldberg, 1999). in the Indian Ocean and Red Sea not reported, it is not clear whether or Shortly after bleaching of O. pata- (Ben-Haim and Rosenberg, 2002; not it is the causative agent or the result gonica in the Mediterranean was first Ben-Haim et al., 2003). The infection of of the disease. Culture-independent reported in 1995, the causative agent of P. damicornis by V. coralliilyticus shows analyses of type I and the disease was identified asVibrio shiloi strong temperature dependence. Below healthy Acropora species showed that (Kushmaro et al., 1996; Kushmaro et 22°C, no infection occurs. At 24–26°C, the microbial community was domi- al., 1997). Increased seawater tempera- the infection results in bleaching, nated by a single bacterial species related ture was the environmental factor that whereas at 27–29°C the infection causes to Rickettsiales. However, there were triggered the disease (Kushmaro et al., rapid tissue lysis and death of the coral. no dramatic differences in the bacterial 1998). Infection and resulting bleach- communities associated with white band ing only occurred at summer seawater White Band Disease disease. These results suggest that a non- temperatures (25–30°C) and not at White band disease is characterized by bacterial pathogen might be the cause of winter temperatures (16–20°C). The a progressive lesion starting from the the disease (Casas et al., 2004). mode of infection and the tempera- base of the coral and moving to the tip ture dependence of many steps in the (Figure 2c). Ritchie and Smith (1995) White Plague Disease process have been studied extensively compared the microbial community In the summer of 1995, a devastating (Rosenberg and Falkowitz, 2004). The structure of diseased and healthy corals disease occurred on reefs of the northern winter reservoir and summer vec- using carbon source utilization pattern Florida Keys, spreading rapidly to infect tor for transmitting the disease is the analyses. They found that diseased cor- 17 different coral species. The disease, marine firewormHermodice carunculata als contained a much higher propor- designated white plague, was charac-

Figure 2. Photographs of dis- eased corals. (a) Bleaching of Oculina patagonica. (b) Aspergillosis of Gorgonia ventalina. (c) White band disease of Acropora cervicor- nis. (d) White plague disease of Diploria strigosa. (e) White plague disease of Favia favius. a. Oc ulina patagonica b. Gorgonia ventalin a c. Acropora ce rvicornis d. Diplor ia stri gosa (f) of Acropora palmata. (g) Yellow blotch disease of Monastraea faveolata. (h) of Diploria strigosa. L. Richardson and NOAA provided photographs b, c, d, f, g, and h

e. Fa via favius f. Acropora palmat a g. Montastraea faveolata h. Diploria stri gosa

Oceanography June 2007 149 terized by a sharp line between freshly White Pox Disease gesting a close similarity to the above- exposed coral skeleton and apparently Serratia marcescens causes white pox described coral bleaching by V. shiloi and healthy tissue (Figure 2d). The lesion disease (Figure 2f) in the common V. coralliilyticus. progressed rapidly (up to 2 cm/day), Caribbean reef-building coral, Acropora leading to mortality within 10 weeks. palmata (Patterson et al., 2002). Black Band Disease Microbiological studies indicated that S. marcescens, a Gram-negative coli- Black band disease can be recognized as a dark band that moves across coral colonies, destroying coral tissue (Figure 2h). The disease is most active Coral microbiology is a new field, during the warm summer months (Kuta driven largely by a desire to understand and Richardson, 2002). Although this the interactions between corals and disease has been studied extensively, the causative agent remains elusive (Cooney their symbiotic microorganisms and to et al., 2002; Frais-Lopez et al., 2002). use this knowledge to eventually prevent Microscopic observation of diseased tis- sue reveals the presence of heterotrophic the spread of coral diseases. and photosynthetic bacteria. Richardson (2004) argues for the concept that black band disease is not caused by a single the causative agent was a single Gram- form bacterium and a member of the primary pathogen, but rather results negative bacterium. Subsequently, Enterobacteriacae family, is a known from a pathogenic consortium behaving this pathogen was classified as a rep- pathogen of humans, cows, goats, chick- as a microbial mat. resentative of a hitherto unknown ens, fish, insects, and plants. This is the marine taxon of the order Rhizobiales first example of a coral pathogen with a Fungal Infections of the class alpha-Proteobacteria possible link to human sewage pollution. During the 1980s, certain areas of the and called Aurantimonas coralicida Caribbean experienced mass mortalities (Denner et al., 2003). Yellow Blotch Disease of sea fans (Garzon-Ferreira and Zea, Starting in 2003, a white plague- During the early stages of yellow blotch 1992), but microbiological studies were like disease (Figure 2e) spread over the disease, pale yellow blotches appear on not performed. In 1995, sea fans showing Eilat coral reef, Gulf of Aqaba, Red Sea, the coral tissue. The blotches expand and disease signs (Figure 2b) similar to those affecting approximately 10% of the form bands (Figure 2g) that can spread reported in the 1980s were observed major reef-building coral genera. The slowly across the colony at rates of throughout the Caribbean (Nagelkerken pathogen was identified as a new spe- 0.5–1.0 cm/month (Santavy et al., 1999). et al., 1997). The causative agent of this cies, Thalassomonas loyana (Barash et al., After a series of infection/reisolation disease was isolated and identified by 2005; Thompson et al., 2006). To dem- experiments, four Vibrio strains were classical and molecular methods as a onstrate unequivocally that T. loyana is obtained that induced the disease in con- strain of the Aspergillis sydowii the causative agent of the white plague- trolled aquarium experiments (Cervino (Smith et al., 1996; Geiser et al., 1998). like disease on the Eilat coral reef, an et al., 2004). One of the strains was iden- Aspergilli are considered terrestrial indirect, but powerful, novel method tified asVibrio alginolyticus. The rate of fungi and do not sporulate in seawater. was employed— (Efrony spread of the disease was proportional to Two hypotheses have been put forth to et al., 2007). A bacteriophage specific temperature from 25–33°C. The Vibrio explain the source of the coral pathogen for T. loyana was isolated and shown to infection targets the endosymbiotic (Smith and Weil, 2004): runoff from the block the disease. algae rather than the coral tissue, sug- land and African dust events.

150 Oceanography Vol. 20, No. 2 The presence of endolithic fungi in lence (Gophna et al., 2004). A link has more rapidly in warm summer months. scleractinian corals has been known been made between the relative abun- In the two documented examples of since the 1800s (Kölliker, 1859). These dance of methanogenic archaea in the bacterial bleaching of corals, the mecha- fungal associates have been described subgingival crevice and the severity of nisms by which temperatures affect the from many geographic areas and spe- periodontal disease in humans (Lepp et process were established. As noted above, cies, and seem to infect the coral at an al., 2004). The methogens do not cause expression of critical bacterial virulence early stage of development (Bentis et al., the disease, but their metabolism pro- genes is temperature dependent. 2000). Although healthy corals appear to duces a conducive environment for cer- be able to keep endolithic fungal attacks tain bacteria. Considering how little we Water Pollution on polyps in check by walling them off know about archaeal metabolic capabili- Elevated nutrients (e.g., phosphate, (Le Campion-Alsumard et al., 1995), ties, and that corals have > 107 archaea nitrate, ammonia, and dissolved organic stresses such as increased water tempera- per cm2 in addition to at least as many carbon) in coastal waters have been sug- ture, bleaching, or disease provide an bacteria (Wegley et al., 2004), corals gested as a cause of reef decline. Field opportunity for secondary infection, for would seem to be an excellent laboratory experiments using a slow-release fertil- example, fungal infection associated with to begin studying these interactions and izer in nylon bags demonstrated that black band disease (Ramos-Flores, 1983) the possible pathogenicity of archaea. increasing inorganic nitrogen and phos- and pink line syndrome (Ravindran et phate by two to five times increased al., 2001). Most of these fungi remain Stress Factors that the severity of aspergillosis and yellow partially or completely unidentified Contribute to Coral Disease blotch diseases (Bruno et al., 2003). because characterization is based on Climate change (Harvell et al., 2002, Addition of small quantities of car- histological and microscopic examina- 2007), water pollution (Szmant, 2002), bohydrates to corals in a flow-though tion of the hyphae that is hampered by a and overfishing (Jackson et al., 2001) system caused substantial coral mortal- lack of sporulation in cultured isolates. are the three most frequently cited envi- ity and an order of magnitude increase Molecular techniques have not yet been ronmental stress factors responsible for in the growth rate of microorganisms successfully applied to this task because the rise in coral disease. Until recently, in the coral mucus (Kline et al., 2006). nominally fungal-specific primer sets evidence supporting these claims has The latter study suggests that mortal- also amplify the 18S rDNA gene from been largely circumstantial, namely, cor- ity results from a disruption of the bal- the coral host. relations between these stress factors and ance between the coral and its associated the frequency of disease. However, recent microbiota. These studies should be Archaeal Pathogens? studies provide direct experimental evi- valuable in implementing coral monitor- As studies increasingly reveal the diver- dence demonstrating how each of these ing and management plans. sity of archaea and the varied environ- factors contributes to coral disease. ments they inhabit, it is interesting that Overfishing no archaea have been characterized as Climate Change Overfishing reduces the number of fish pathogens. Archaea have been shown to Earth is undergoing accelerating climate that graze on algae, thus increasing the colonize metazoans, including all rumi- change that is being driven by increas- concentration of algae present on coral nants, humans (Kulik et al., 2001; Miller ing concentrations of greenhouse gases. reefs. Numerous studies show that vari- and Wolin, 1982), fish (van der Maarel During the last century, the average ous species of algae can influence cor- et al., 1998, 1999), and corals (Kellogg, global temperature increased 0.6 ± 0.2°C, als negatively (reviewed by McCook 2004; Wegley et al., 2004). It has been and it is predicted to rise another et al., 2001). Suggested mechanisms suggested that horizontal transfer of 1.5–4.5°C this century (IPCC, 2007). All include alleopathy, smothering, shad- genes from archaea to bacterial patho- of the coral diseases shown in Figure 2 ing, abrasion, overgrowth, and harboring gens may have enhanced bacterial viru- occur more frequently and progress potential pathogens. Smith et al. (2006)

Oceanography June 2007 151 demonstrate that algae can cause For example, A. coralicida (Denner et lacking an adaptive immune system (no coral mortality by enhancing micro- al., 2003), the bacterium responsible antibodies), corals can develop resis- bial activity via the release of dissolved for the white plague disease on reefs off tance to pathogens. The Coral Probiotic compounds. Coral mortality can be the Florida Keys in 1995, can no longer Hypothesis may help explain the evolu- completely prevented by addition of infect these corals (Richardson and tionary success of corals and moderate antibiotics, thus supporting the hypoth- Aronson, 2002). predictions of their demise. esis that the microbial community is the agent of coral death under conditions of The Coral Holobiont and Acknowledgements abundant algal growth. Probiotic Hypothesis This research was supported by grants The ability to adapt to stresses, such from the Israel Center for the Study Coral Resistance to Stress as high temperature and infection by of Emerging Diseases, the World Bank and the Coral Probiotic specific pathogens, has led to the Coral Coral Disease and Bleaching Groups, Hypothesis Probiotic Hypothesis (Reshef et al., and the Pasha Gol Chair for Applied Although corals contain innate or non- 2006). This hypothesis posits that a Microbiology. Archaeal research was specific immunity systems, they do not dynamic relationship exists between supported by the U.S. Geological produce antibodies and are considered symbiotic microorganisms and corals Survey (CAK) and the National Science to lack an adaptive immune system. at different environmental conditions, Foundation (FR). The Gordon and Betty However, recent data demonstrate that which bring about a selection for the Moore Foundation Marine Microbial corals can develop resistance to specific most advantageous coral holobiont. The Initiative provided support for research pathogens and adapt to higher tempera- hypothesis is similar to the Adaptive on coral-algae interactions and coral- tures. The Coral Probiotic Hypothesis Bleaching Hypothesis for zooxanthel- associated viruses (FR). (Reshef et al., 2006), discussed below, lae but more inclusive because the coral explains these findings within the con- holobiont is defined as the host organ- References text of what is currently known about ism plus all of the associated micro- Baker, A.C. 2003. Flexibility and specificity in coral- algal : Diversity, ecology and bioge- coral microbiology. organisms. By changing its microbial ography of Symbiodinium. Annual Review of community, the holobiont can adapt Ecology and Systematics 34:661–689. Adaptation of Corals to Stress to changing environmental conditions Baker, A.C. 2004. Symbiont diversity on coral reefs and its relationship to bleaching resistance and From 1995 to 2002, bacterial bleaching more rapidly (weeks to years) than it resilience. Pp. 177–194 in Coral Health and of the coral O. patagonica in the eastern can via mutation and selection of the Disease. E. Roseberg and Y. Loya, eds, Springer- Mediterranean occurred every sum- coral host itself (thousands of years). Verlag, Berlin. Barash, Y., R. Sulam, Y. Loya, and E. Rosenberg. mer. During that time period, V. shiloi Four key observations discussed in 2005. Bacterial strain BA-3 and a filterable fac- was repeatedly isolated from bleached this article support the Coral Probiotic tor cause a white plague-like disease in corals corals and shown to cause bleaching of Hypothesis: (1) corals contain a large from the Eilat coral reef. Aquatic 40:183–189. healthy corals in controlled aquarium and diverse microbial population asso- Ben-Haim, Y., and E. Rosenberg. 2002. A novel experiments. However, since 2003, it ciated with their mucus and tissues; Vibrio sp. pathogen of the coral Pocillopora has not been possible to isolate V. shiloi (2) coral-associated microorganisms damicornis. 141:47–55. Ben-Haim, Y., M. Zicherman-Keren, and E. from bleached or healthy corals, and all can benefit their host by a variety of dif- Rosenberg. 2003. Temperature-regulated laboratory stocks of V. shiloi failed to ferent mechanisms (e.g., nitrogen fixa- bleaching and lysis of the coral Pocillopora dam- cause bleaching of fresh, healthy corals tion, , and production icornis by the novel pathogen Vibrio coralliilyti- cus. Applied and Environmental Microbiology taken from the sea (Reshef et al., 2006). of antimicrobials); (3) the coral-associ- 69:4,236–4,242. There are other, less-well-documented ated microbial population undergoes Bentis, C.J., L. Kaufman, and S. Golubic. 2000. examples of coral communities that have a rapid change when environmental Endolithic fungi in reef-building corals (order: ) are common, cosmopolitan, and become resistant to specific pathogens. conditions are altered; and (4) although potentially pathogenic. Biological Bulletin

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