Macroalgae Decrease Growth and Alter Microbial Community Structure of the Reef-Building Coral, Porites astreoides

With the continued and unprecedented decline of coral reefs worldwide, evaluating the factors that contribute to coral demise is of critical importance. As coral cover declines, macroalgae are becoming more common on tropical reefs. Interactions between these macroalgae and corals may alter the coral microbiome, which is thought to play an important role in colony health and survival. Together, such changes in benthic macroalgae and in the coral microbiome may result in a feedback mechanism that contributes to additional coral cover loss. To determine if macroalgae alter the coral microbiome, we conducted a field-based experiment in which the coral Porites astreoides was placed in competition with five species of macroalgae. Macroalgal contact increased variance in the coral-associated microbial community, and two algal species significantly altered microbial community composition. All macroalgae caused the disappearance of a γ-proteobacterium previously hypothesized to be an important mutualist of P. astreoides. Macroalgal contact also triggered: 1) increases or 2) decreases in microbial taxa already present in corals, 3) establishment of new taxa to the coral microbiome, and 4) vectoring and growth of microbial taxa from the macroalgae to the coral. Furthermore, macroalgal competition decreased coral growth rates by an average of 36.8%. Overall, this study found that competition between corals and certain species of macroalgae leads to an altered coral microbiome, providing a potential mechanism by which macroalgae-coral interactions reduce coral health and lead to coral loss on impacted reefs.     

The impact of reduced pH on the microbial community of the coral Acropora eurystoma

Rising concentrations of atmospheric carbon dioxide are acidifying the world''s oceans. Surface seawater pH is 0.1 units lower than pre-industrial values and is predicted to decrease by up to 0.4 units by the end of the century. This change in pH may result in changes in the physiology of ocean organisms, in particular, organisms that build their skeletons/shells from calcium carbonate, such as corals. This physiological change may also affect other members of the coral holobiont, for example, the microbial communities associated with the coral, which in turn may affect the coral physiology and health. In the present study, we examined changes in bacterial communities in the coral mucus, tissue and skeleton following exposure of the coral Acropora eurystoma to two different pH conditions: 7.3 and 8.2 (ambient seawater). The microbial community was different at the two pH values, as determined by denaturing gradient gel electrophoresis and 16S rRNA gene sequence analysis. Further analysis of the community in the corals maintained at the lower pH revealed an increase in bacteria associated with diseased and stressed corals, such as Vibrionaceae and Alteromonadaceae. In addition, an increase in the number of potential antibacterial activity was recorded among the bacteria isolated from the coral maintained at pH 7.3. Taken together, our findings highlight the impact that changes in the pH may have on the coral-associated bacterial community and their potential contribution to the coral host.     

Regulation of Bacterial Communities Through Antimicrobial Activity by the Coral Holobiont

Interactions between corals and associated bacteria and amongst these bacterial groups are likely to play a key role in coral health. However, the complexity of these interactions is poorly understood. We investigated the functional role of specific coral-associated bacteria in maintaining microbial communities on the coral Acropora millepora (Ehrenberg 1834) and the ability of coral mucus to support or inhibit bacterial growth. Culture-independent techniques were used to assess bacterial community structures whilst bacterial culture was employed to assess intra- and inter-specific antimicrobial activities of bacteria. Members of Pseudoalteromonas and ribotypes closely related to Vibrio coralliilyticus displayed potent antimicrobial activity against a range of other cultured isolates and grew readily on detached coral mucus. Although such bacterial ribotypes would be expected to have a competitive advantage, they were rare or absent on intact and healthy coral colonies growing in situ (analysed using denaturing gradient gel electrophoresis and 16S rRNA gene sequencing). The most abundant bacterial ribotypes found on healthy corals were Gammaproteobacteria, previously defined as type A coral associates. Our results indicate that this group of bacteria and specific members of the Alphaproteobacteria described here as ‘type B associates’ may be important functional groups for coral health. We suggest that bacterial communities on coral are kept in check by a combination of host-derived and microbial interactions and that the type A associates in particular may play a key role in maintaining stability of microbial communities on healthy coral colonies.     

Coral-associated bacterial communities on Ningaloo Reef, Western Australia

Coral-associated microbial communities from three coral species (Pocillopora damicornis, Acropora tenuis and Favites abdita) were examined every 3 months (January, March, June, October) over a period of 1 year on Ningaloo Reef, Western Australia. Tissue from corals was collected throughout the year and additional sampling of coral mucus and seawater samples was performed in January. Tissue samples were also obtained in October from P. damicornis coral colonies on Rottnest Island off Perth, 1200 km south of Ningaloo Reef, to provide comparisons between coral-microbial associates in different locations. The community structures of the coral-associated microorganisms were analysed using phylogenetic analysis of 16S rRNA gene clone libraries, which demonstrated highly diverse microbial profiles among all the coral species sampled. Principal component analysis revealed that samples grouped according to time and not species, indicating that coral-microbial associations may be a result of environmental drivers such as oceanographic characteristics, benthic community structure and temperature. Tissue samples from P. damicornis at Rottnest Island revealed similarities in bacteria to the samples at Ningaloo Reef. This study highlights that coral-associated microbial communities are highly diverse; however, the complex interactions that determine the stability of these associations are not necessarily dependent on coral host specificity.     

Metagenomic analysis of stressed coral holobionts

The coral holobiont is the community of metazoans, protists and microbes associated with scleractinian corals. Disruptions in these associations have been correlated with coral disease, but little is known about the series of events involved in the shift from mutualism to pathogenesis. To evaluate structural and functional changes in coral microbial communities, Porites compressa was exposed to four stressors: increased temperature, elevated nutrients, dissolved organic carbon loading and reduced pH. Microbial metagenomic samples were collected and pyrosequenced. Functional gene analysis demonstrated that stressors increased the abundance of microbial genes involved in virulence, stress resistance, sulfur and nitrogen metabolism, motility and chemotaxis, fatty acid and lipid utilization, and secondary metabolism. Relative changes in taxonomy also demonstrated that coral-associated microbiota ( Archaea , Bacteria , protists) shifted from a healthy-associated coral community (e.g. Cyanobacteria , Proteobacteria and the zooxanthellae Symbiodinium ) to a community (e.g. Bacteriodetes , Fusobacteria and Fungi ) of microbes often found on diseased corals. Additionally, low-abundance Vibrio spp. were found to significantly alter microbiome metabolism, suggesting that the contribution of a just a few members of a community can profoundly shift the health status of the coral holobiont.     

PhyloChip™ microarray comparison of sampling methods used for coral microbial ecology

Interest in coral microbial ecology has been increasing steadily over the last decade, yet standardized methods of sample collection still have not been defined. Two methods were compared for their ability to sample coral-associated microbial communities: tissue punches and foam swabs, the latter being less invasive and preferred by reef managers. Four colonies of star coral, Montastraea annularis, were sampled in the Dry Tortugas National Park (two healthy and two with white plague disease). The PhyloChip™ G3 microarray was used to assess microbial community structure of amplified 16S rRNA gene sequences. Samples clustered based on methodology rather than coral colony. Punch samples from healthy and diseased corals were distinct. All swab samples clustered closely together with the seawater control and did not group according to the health state of the corals. Although more microbial taxa were detected by the swab method, there is a much larger overlap between the water control and swab samples than punch samples, suggesting some of the additional diversity is due to contamination from water absorbed by the swab. While swabs are useful for noninvasive studies of the coral surface mucus layer, these results show that they are not optimal for studies of coral disease.     

The dynamics of microbial partnerships in the coral Isopora palifera

Both bacteria and algal symbionts (genus Symbiodinium), the two major microbial partners in the coral holobiont, respond to fluctuations in the environment, according to current reports; however, little evidence yet indicates that both populations have any direct interaction with each other in seasonal fluctuation. In this study, we present field observations of a compositional change in bacteria and Symbiodinium in the coral Isopora palifera in three separate coral colonies following monthly sampling from February to November in 2008. Using massively parallel pyrosequencing, over 200 000 bacterial V6 sequences were classified to build the bacterial community profile; in addition, the relative composition and quantity of Symbiodinium clades C and D were determined by real-time PCR. The results showed that coral-associated bacterial and Symbiodinium communities were highly dynamic and dissimilar among the tagged coral colonies, suggesting that the effect of host specificity was insignificant. The coral-associated bacterial community was more diverse (Shannon index up to 6.71) than previous estimates in other corals and showed rapid seasonal changes. The population ratios between clade C and D groups of Symbiodinium varied in the tagged coral colonies through the different seasons; clade D dominated in most of the samples. Although significant association between bacteria and symbiont was not detected, this study presents a more detailed picture of changes in these two major microbial associates of the coral at the same time, using the latest molecular approaches.     

Bacterial profiling of White Plague Disease in a comparative coral species framework

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.     

Algae as Reservoirs for Coral Pathogens

Benthic algae are associated with coral death in the form of stress and disease. It''s been proposed that they release exudates, which facilitate invasion of potentially pathogenic microbes at the coral-algal interface, resulting in coral disease. However, the original source of these pathogens remains unknown. This study examined the ability of benthic algae to act as reservoirs of coral pathogens by characterizing surface associated microbes associated with major Caribbean and Indo-Pacific algal species/types and by comparing them to potential pathogens of two dominant coral diseases: White Syndrome (WS) in the Indo-Pacific and Yellow Band Disease (YBD) in the Caribbean. Coral and algal sampling was conducted simultaneously at the same sites to avoid spatial effects. Potential pathogens were defined as those absent or rare in healthy corals, increasing in abundance in healthy tissues adjacent to a disease lesion, and dominant in disease lesions. Potentially pathogenic bacteria were detected in both WS and YBD and were also present within the majority of algal species/types (54 and 100% for WS and YBD respectively). Pathogenic ciliates were associated only with WS and not YBD lesions and these were also present in 36% of the Indo-Pacific algal species. Although potential pathogens were associated with many algal species, their presence was inconsistent among replicate algal samples and detection rates were relatively low, suggestive of low density and occurrence. At the community level, coral-associated microbes irrespective of the health of their host differed from algal-associated microbes, supporting that algae and corals have distinctive microbial communities associated with their tissue. We conclude that benthic algae are common reservoirs for a variety of different potential coral pathogens. However, algal-associated microbes alone are unlikely to cause coral death. Initial damage or stress to the coral via other competitive mechanisms is most likely a prerequisite to potential transmission of these pathogens.     

Quorum Sensing Signal Production and Microbial Interactions in a Polymicrobial Disease of Corals and the Coral Surface Mucopolysaccharide Layer

Black band disease (BBD) of corals is a complex polymicrobial disease considered to be a threat to coral reef health, as it can lead to mortality of massive reef-building corals. The BBD community is dominated by gliding, filamentous cyanobacteria with a highly diverse population of heterotrophic bacteria. Microbial interactions such as quorum sensing (QS) and antimicrobial production may be involved in BBD disease pathogenesis. In this study, BBD (whole community) samples, as well as 199 bacterial isolates from BBD, the surface mucopolysaccharide layer (SML) of apparently healthy corals, and SML of apparently healthy areas of BBD-infected corals were screened for the production of acyl homoserine lactones (AHLs) and for autoinducer-2 (AI-2) activity using three bacterial reporter strains. AHLs were detected in all BBD (intact community) samples tested and in cultures of 5.5% of BBD bacterial isolates. Over half of a subset (153) of the isolates were positive for AI-2 activity. AHL-producing isolates were further analyzed using LC-MS/MS to determine AHL chemical structure and the concentration of (S)-4,5-dihydroxy-2,3-pentanedione (DPD), the biosynthetic precursor of AI-2. C6-HSL was the most common AHL variant detected, followed by 3OC4-HSL. In addition to QS assays, 342 growth challenges were conducted among a subset of the isolates, with 27% of isolates eliciting growth inhibition and 2% growth stimulation. 24% of BBD isolates elicited growth inhibition as compared to 26% and 32% of the bacteria from the two SML sources. With one exception, only isolates that exhibited AI-2 activity or produced DPD inhibited growth of test strains. These findings demonstrate for the first time that AHLs are present in an active coral disease. It is possible that AI-2 production among BBD and coral SML bacteria may structure the microbial communities of both a polymicrobial infection and the healthy coral microbiome.     

PCR Primers with Enhanced Specificity for Nematode-Trapping Fungi (<Emphasis Type="Italic">Orbiliales</Emphasis>)

In search for microbiological indicators of coral health and coral diseases, community profiles of coral-associated epizoic prokaryotes were investigated because of their dual potential as a source of coral pathogens and their antagonists. In pairwise samples of visually healthy and diseased coral specimens from Bolinao Bay (Pangasinan, Philippines), mixed biofilm communities of ectoderm- and mucus-colonizing epizoic prokaryotes were compared using fluorescent in situ hybridization (FISH). Oligonucleotide probes targeted 13 phylotypes representing the main taxonomic groups of marine prokaryotes. Coral taxa tended to show specific community profiles. An attempt to separate the profiles of healthy and diseased specimens by applying principal component analysis (PCA) to a (nonselective) collection of corals (affected by various diseases) proved unsuccessful. On the other hand, separate PCA clusters were obtained from healthy and diseased corals belonging to a single species (Pocillopora damicornis) only. This cluster formation was dominated by principal component 1 with the genus Vibrio accounting for 18%. At the same time, reef-site-specific clusters were formed as well. At a reef site exposed to pollution from intensive fish cage (Chanos chanos) farming, healthy P. damicornis were mainly (93%) colonized by unicellular cyanobacteria. The formal calculation of diversity parameters suggested that evenness in particular was driven by both health status and reef site location. Despite the low resolution of taxonomic levels achieved with FISH probes targeting only large phylotype groups, significant differences between healthy and diseased corals and also between polluted and nonpolluted reef sites were observed.     

Coral bleaching: the winners and the losers

Sea surface temperatures were warmer throughout 1998 at Sesoko Island, Japan, than in the 10 preceding years. Temperatures peaked at 2.8 °C above average, resulting in extensive coral bleaching and subsequent coral mortality. Using random quadrat surveys, we quantitatively documented the coral community structure one year before and one year after the bleaching event. The 1998 bleaching event reduced coral species richness by 61% and reduced coral cover by 85%. Colony morphology affected bleaching vulnerability and subsequent coral mortality. Finely branched corals were most susceptible, while massive and encrusting colonies survived. Most heavily impacted were the branched Acropora and pocilloporid corals, some of which showed local extinction. We suggest two hypotheses whose synergistic effect may partially explain observed mortality patterns (i.e. preferential survival of thick-tissued species, and shape-dependent differences in colony mass-transfer efficiency). A community-structural shift occurred on Okinawan reefs, resulting in an increase in the relative abundance of massive and encrusting coral species.     

Viral communities associated with healthy and bleaching corals

The coral holobiont is the integrated assemblage of the coral animal, its symbiotic algae, protists, fungi and a diverse consortium of Bacteria and Archaea . Corals are a model system for the study of symbiosis, the breakdown of which can result in disease and mortality. Little is known, however, about viruses that infect corals and their symbionts. Here we present metagenomic analyses of the viral communities associated with healthy and partially bleached specimens of the Caribbean reef-building coral Diploria strigosa . Surprisingly, herpes-like sequences accounted for 4–8% of the total sequences in each metagenome; this abundance of herpes-like sequences is unprecedented in other marine viral metagenomes. Viruses similar to those that infect algae and plants were also present in the coral viral assemblage. Among the phage identified, cyanophages were abundant in both healthy and bleaching corals and vibriophages were also present. Therefore, coral-associated viruses could potentially infect all components of the holobiont – coral, algal and microbial. Thus, we expect viruses to figure prominently in the preservation and breakdown of coral health.     

Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts

The importance of associations between microorganisms and their invertebrate hosts is becoming increasingly apparent. An emerging field, driven by the necessity to understand the microbial relationships that both maximize coral health and cause coral disease, is the study of coral-bacteria interactions. In this article, we review our current understanding of the diversity, specificity, development, and functions of coral-associated bacteria. We also summarize what is known regarding the role of coral microbiota in the health and disease of coral. We conduct a meta-analysis to determine whether the presence of unique taxa correlates with the state of coral health (i.e. healthy, diseased or bleached), as well as whether coral reef habitats harbor clusters of distinct taxa. We find that healthy and bleached corals harbor similar dominant taxa, although bleached corals had higher proportions of Vibrio and Acidobacteria. Diseased corals generally had more Rhodobacter, Clostridia, and Cyanobacteria sequences, and fewer Oceanospirillum sequences. We caution, however, that while 16S rRNA is useful for microbial species identification, it is a poor predictor of habitat or lifestyle, and care should be taken in interpretation of 16S rRNA surveys to identify potential pathogens amongst complex coral-microbial assemblages. Finally, we highlight evidence that coral-bacterial assemblages could be sensitive to the effects of climatic change. We suggest that the relationship between coral and their bacterial associates represents a valuable model that can be applied to the broader discipline of invertebrate-microbial interactions.     

Specificity is rarely absolute in coral-algal symbiosis: implications for coral response to climate change

Some reef-building corals have been shown to respond to environmental change by shifting the composition of their algal symbiont (genus Symbiodinium) communities. These shifts have been proposed as a potential mechanism by which corals might survive climate stressors, such as increased temperatures. Conventional molecular methods suggest this adaptive capacity may not be widespread because few (～25%) coral species have been found to associate with multiple Symbiodinium clades. However, these methods can fail to detect low abundance symbionts (typically less than 10-20% of the total algal symbiont community). To determine whether additional Symbiodinium clades are present, but are not detected using conventional techniques, we applied a high-resolution, real-time PCR assay to survey Symbiodinium (in clades A-D) from 39 species of phylogenetically and geographically diverse scleractinian corals. This survey included 26 coral species thought to be restricted to hosting a single Symbiodinium clade ('symbiotic specialists'). We detected at least two Symbiodinium clades (C and D) in at least one sample of all 39 coral species tested; all four Symbiodinium clades were detected in over half (54%) of the 26 symbiotic specialist coral species. Furthermore, on average, 68 per cent of all sampled colonies within a given coral species hosted two or more symbiont clades. We conclude that the ability to associate with multiple symbiont clades is common in scleractinian (stony) corals, and that, in coral-algal symbiosis, 'specificity' and 'flexibility' are relative terms: specificity is rarely absolute. The potential for reef corals to adapt or acclimatize to environmental change via symbiont community shifts may therefore be more phylogenetically widespread than has previously been assumed.     

Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis

The coral reef benthos is primarily colonized by corals and algae, which are often in direct competition with one another for space. Numerous studies have shown that coral-associated Bacteria are different from the surrounding seawater and are at least partially species specific (i.e. the same bacterial species on the same coral species). Here we extend these microbial studies to four of the major ecological functional groups of algae found on coral reefs: upright and encrusting calcifying algae, fleshy algae, and turf algae, and compare the results to the communities found on the reef-building coral Montastraea annularis. It was found using 16S rDNA tag pyrosequencing that the different algal genera harbour characteristic bacterial communities, and these communities were generally more diverse than those found on corals. While the majority of coral-associated Bacteria were related to known heterotrophs, primarily consuming carbon-rich coral mucus, algal-associated communities harboured a high percentage of autotrophs. The majority of algal-associated autotrophic Bacteria were Cyanobacteria and may be important for nitrogen cycling on the algae. There was also a rich diversity of photosynthetic eukaryotes associated with the algae, including protists, diatoms, and other groups of microalgae. Together, these observations support the hypothesis that coral reefs are a vast landscape of distinctive microbial communities and extend the holobiont concept to benthic algae.     

Macroalgal Extracts Induce Bacterial Assemblage Shifts and Sublethal Tissue Stress in Caribbean Corals

Benthic macroalgae can be abundant on present-day coral reefs, especially where rates of herbivory are low and/or dissolved nutrients are high. This study investigated the impact of macroalgal extracts on both coral-associated bacterial assemblages and sublethal stress response of corals. Crude extracts and live algal thalli from common Caribbean macroalgae were applied onto the surface of Montastraea faveolata and Porites astreoides corals on reefs in both Florida and Belize. Denaturing gradient gel electrophoresis (DGGE) of 16S rRNA gene amplicons was used to examine changes in the surface mucus layer (SML) bacteria in both coral species. Some of the extracts and live algae induced detectable shifts in coral-associated bacterial assemblages. However, one aqueous extract caused the bacterial assemblages to shift to an entirely new state (Lobophora variegata), whereas other organic extracts had little to no impact (e.g. Dictyota sp.). Macroalgal extracts more frequently induced sublethal stress responses in M. faveolata than in P. astreoides corals, suggesting that cellular integrity can be negatively impacted in selected corals when comparing co-occurring species. As modern reefs experience phase-shifts to a higher abundance of macroalgae with potent chemical defenses, these macroalgae are likely impacting the composition of microbial assemblages associated with corals and affecting overall reef health in unpredicted and unprecedented ways.     

Changes in coral microbial communities in response to a natural pH gradient

Surface seawater pH is currently 0.1 units lower than pre-industrial values and is projected to decrease by up to 0.4 units by the end of the century. This acidification has the potential to cause significant perturbations to the physiology of ocean organisms, particularly those such as corals that build their skeletons/shells from calcium carbonate. Reduced ocean pH could also have an impact on the coral microbial community, and thus may affect coral physiology and health. Most of the studies to date have examined the impact of ocean acidification on corals and/or associated microbiota under controlled laboratory conditions. Here we report the first study that examines the changes in coral microbial communities in response to a natural pH gradient (mean pH_T 7.3–8.1) caused by volcanic CO₂ vents off Ischia, Gulf of Naples, Italy. Two Mediterranean coral species, Balanophyllia europaea and Cladocora caespitosa, were examined. The microbial community diversity and the physiological parameters of the endosymbiotic dinoflagellates (Symbiodinium spp.) were monitored. We found that pH did not have a significant impact on the composition of associated microbial communities in both coral species. In contrast to some earlier studies, we found that corals present at the lower pH sites exhibited only minor physiological changes and no microbial pathogens were detected. Together, these results provide new insights into the impact of ocean acidification on the coral holobiont.     

Bacterial community structure associated with the Antarctic soft coral, Alcyonium antarcticum

The structure and composition of microbial communities inhabiting the soft coral Alcyonium antarcticum were investigated across three differentially contaminated sites within McMurdo Sound, Antarctica. Diverse microbial communities were revealed at all sites using culture-based analysis, denaturing gradient gel electrophoresis (DGGE), 16S rRNA gene clone-library analysis, and FISH. Phylogenetic analysis of isolates and retrieved sequences demonstrated close affiliation with known psychrophiles from the Antarctic environment and high similarity to Gammaproteobacteria clades of sponge-associated microorganisms. The majority of bacteria detected with all techniques reside within the Gammaproteobacteria, although other phylogenetic groups including Alpha- and Betaproteobacteria, Bacteroidetes, Firmicutes, Actinomycetales, Planctomycetes, and Chlorobi and bacteria from the functional group of sulfate-reducing bacteria were also present. Multivariate (nMDS) analysis of DGGE banding patterns and principal component analysis of quantitative FISH data revealed no distinct differences in community composition between differentially contaminated sites. Rather, conserved coral-associated bacterial groups were observed within and between sites, providing evidence to support specific coral-microbial interactions. This is the first investigation of microbial communities associated with Antarctic soft corals, and the results suggest that spatially stable microbial associations exist across an environmental impact gradient.     

Resilience of Coral-Associated Bacterial Communities Exposed to Fish Farm Effluent

Background

The coral holobiont includes the coral animal, algal symbionts, and associated microbial community. These microbes help maintain the holobiont homeostasis; thus, sustaining robust mutualistic microbial communities is a fundamental part of long-term coral reef survival. Coastal pollution is one major threat to reefs, and intensive fish farming is a rapidly growing source of this pollution.

Methodology & Principal Findings

We investigated the susceptibility and resilience of the bacterial communities associated with a common reef-building coral, Porites cylindrica, to coastal pollution by performing a clonally replicated transplantation experiment in Bolinao, Philippines adjacent to intensive fish farming. Ten fragments from each of four colonies (total of 40 fragments) were followed for 22 days across five sites: a well-flushed reference site (the original fragment source); two sites with low exposure to milkfish (Chanos chanos) aquaculture effluent; and two sites with high exposure. Elevated levels of dissolved organic carbon (DOC), chlorophyll a, total heterotrophic and autotrophic bacteria abundance, virus like particle (VLP) abundances, and culturable Vibrio abundance characterized the high effluent sites. Based on 16S rRNA clone libraries and denaturing gradient gel electrophoresis (DGGE) analysis, we observed rapid, dramatic changes in the coral-associated bacterial communities within five days of high effluent exposure. The community composition on fragments at these high effluent sites shifted towards known human and coral pathogens (i.e. Arcobacter, Fusobacterium, and Desulfovibrio) without the host corals showing signs of disease. The communities shifted back towards their original composition by day 22 without reduction in effluent levels.

Significance

This study reveals fish farms as a likely source of pathogens with the potential to proliferate on corals and an unexpected short-term resilience of coral-associated bacterial communities to eutrophication pressure. These data highlight a need for improved aquaculture practices that can achieve both sustainable industry goals and long-term coral reef survival.