Pim Bongaerts

The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts.

Despite being one of the simplest metazoans, corals harbor some of the most highly diverse and abundant microbial communities. Differentiating core, symbiotic bacteria from this diverse host-associated consortium is essential for characterizing the functional contributions of bacteria but has not been possible yet. Here we characterize the coral core microbiome and demonstrate clear phylogenetic and functional divisions between the micro-scale, niche habitats within the coral host. In doing so, we discover seven distinct bacterial phylotypes that are universal to the core microbiome of coral species, separated by thousands of kilometres of oceans. The two most abundant phylotypes are co-localized specifically with the corals’ endosymbiotic algae and symbiont-containing host cells. These bacterial symbioses likely facilitate the success of the dinoflagellate endosymbiosis with corals in diverse environmental regimes.

Genetic Divergence across Habitats in the Widespread Coral Seriatopora hystrix and Its Associated Symbiodinium

Background Coral reefs are hotspots of biodiversity, yet processes of diversification in these ecosystems are poorly understood. The environmental heterogeneity of coral reef environments could be an important contributor to diversification, however, evidence supporting ecological speciation in corals is sparse. Here, we present data from a widespread coral species that reveals a strong association of host and symbiont lineages with specific habitats, consistent with distinct, sympatric gene pools that are maintained through ecologically-based selection. Methodology/Principal Findings Populations of a common brooding coral, Seriatopora hystrix, were sampled from three adjacent reef habitats (spanning a ∼30 m depth range) at three locations on the Great Barrier Reef (n = 336). The populations were assessed for genetic structure using a combination of mitochondrial (putative control region) and nuclear (three microsatellites) markers for the coral host, and the ITS2 region of the ribosomal DNA for the algal symbionts (Symbiodinium). Our results show concordant genetic partitioning of both the coral host and its symbionts across the different habitats, independent of sampling location. Conclusions/Significance This study demonstrates that coral populations and their associated symbionts can be highly structured across habitats on a single reef. Coral populations from adjacent habitats were found to be genetically isolated from each other, whereas genetic similarity was maintained across similar habitat types at different locations. The most parsimonious explanation for the observed genetic partitioning across habitats is that adaptation to the local environment has caused ecological divergence of distinct genetic groups within S. hystrix.

The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia.

Approximately one quarter of zooxanthellate coral species have a depth distribution from shallow waters (<30 m) down to mesophotic depths of 30–60 m. The deeper populations of such species are less likely to be affected by certain environmental perturbations, including high temperature/high irradiance causing coral bleaching. This has led to the hypothesis that deep populations may serve as refuges and a source of recruits for shallow reef habitats. The extent of vertical connectivity of reef coral species, however, is largely unquantified. Using 10 coral host microsatellite loci and sequences of the host mtDNA putative control region, as well as ribosomal DNA (rDNA) ITS2 sequences of the coral’s algal endosymbionts (Symbiodinium), we examine population structure, connectivity and symbiont specificity in the brooding coral Seriatopora hystrix across a depth profile in both northwest (Scott Reef) and northeast Australia (Yonge Reef). Strong genetic structuring over depth was observed in both regions based on the microsatellite loci; however, Yonge Reef exhibited an additional partitioning of mtDNA lineages (associated with specific symbiont ITS2 types), whereas Scott Reef was dominated by a single mtDNA lineage (with no apparent host‐symbiont specificity). Evidence for recruitment of larvae of deep water origin into shallow habitats was found at Scott Reef, suggesting that recovery of shallow water habitats may be aided by migration from deep water refuges. Conversely, no migration from the genetically divergent deep slope populations into the shallow habitats was evident at Yonge Reef, making recovery of shallow habitats from deeper waters at this location highly unlikely.

Deep down on a Caribbean reef: lower mesophotic depths harbor a specialized coral-endosymbiont community

The composition, ecology and environmental conditions of mesophotic coral ecosystems near the lower limits of their bathymetric distributions remain poorly understood. Here we provide the first in-depth assessment of a lower mesophotic coral community (60–100 m) in the Southern Caribbean through visual submersible surveys, genotyping of coral host-endosymbiont assemblages, temperature monitoring and a growth experiment. The lower mesophotic zone harbored a specialized coral community consisting of predominantly Agaricia grahamae, Agaricia undata and a “deep-water” lineage of Madracis pharensis, with large colonies of these species observed close to their lower distribution limit of ~90 m depth. All three species associated with “deep-specialist” photosynthetic endosymbionts (Symbiodinium). Fragments of A. grahamae exhibited growth rates at 60 m similar to those observed for shallow Agaricia colonies (~2–3 cm yr−1), but showed bleaching and (partial) mortality when transplanted to 100 m. We propose that the strong reduction of temperature over depth (Δ5°C from 40 to 100 m depth) may play an important contributing role in determining lower depth limits of mesophotic coral communities in this region. Rather than a marginal extension of the reef slope, the lower mesophotic represents a specialized community, and as such warrants specific consideration from science and management.

The Microbial Signature Provides Insight into the Mechanistic Basis of Coral Success across Reef Habitats

ABSTRACT For ecosystems vulnerable to environmental change, understanding the spatiotemporal stability of functionally crucial symbioses is fundamental to determining the mechanisms by which these ecosystems may persist. The coral Pachyseris speciosa is a successful environmental generalist that succeeds in diverse reef habitats. The generalist nature of this coral suggests it may have the capacity to form functionally significant microbial partnerships to facilitate access to a range of nutritional sources within different habitats. Here, we propose that coral is a metaorganism hosting three functionally distinct microbial interactions: a ubiquitous core microbiome of very few symbiotic host-selected bacteria, a microbiome of spatially and/or regionally explicit core microbes filling functional niches (<100 phylotypes), and a highly variable bacterial community that is responsive to biotic and abiotic processes across spatial and temporal scales (>100,000 phylotypes). We find that this coral hosts upwards of 170,000 distinct phylotypes and provide evidence for the persistence of a select group of bacteria in corals across environmental habitats of the Great Barrier Reef and Coral Sea. We further show that a higher number of bacteria are consistently associated with corals on mesophotic reefs than on shallow reefs. An increase in microbial diversity with depth suggests reliance by this coral on bacteria for nutrient acquisition on reefs exposed to nutrient upwelling. Understanding the complex microbial communities of host organisms across broad biotic and abiotic environments as functionally distinct microbiomes can provide insight into those interactions that are ubiquitous niche symbioses and those that provide competitive advantage within the hosts’ environment. IMPORTANCE Corals have been proposed as the most diverse microbial biosphere. The high variability of microbial communities has hampered the identification of bacteria playing key functional roles that contribute to coral survival. Exploring the bacterial community in a coral with a broad environmental distribution, we found a group of bacteria present across all environments and a higher number of bacteria consistently associated with mesophotic corals (60 to 80 m). These results provide evidence of consistent and ubiquitous coral-bacterial partnerships and support the consideration of corals as metaorganisms hosting three functionally distinct microbiomes: a ubiquitous core microbiome, a microbiome filling functional niches, and a highly variable bacterial community. Corals have been proposed as the most diverse microbial biosphere. The high variability of microbial communities has hampered the identification of bacteria playing key functional roles that contribute to coral survival. Exploring the bacterial community in a coral with a broad environmental distribution, we found a group of bacteria present across all environments and a higher number of bacteria consistently associated with mesophotic corals (60 to 80 m). These results provide evidence of consistent and ubiquitous coral-bacterial partnerships and support the consideration of corals as metaorganisms hosting three functionally distinct microbiomes: a ubiquitous core microbiome, a microbiome filling functional niches, and a highly variable bacterial community.

Habitat-specific environmental conditions primarily control the microbiomes of the coral Seriatopora hystrix

Reef-building corals form complex relationships with a range of microorganisms including bacteria, archaea, fungi and the unicellular microalgae of the genus Symbiodinium, which together form the coral holobiont. These symbionts are known to have both beneficial and deleterious effects on their coral host, but little is known about what the governing factors of these relationships are, or the interactions that exist between the different members of the holobiont and their environment. Here we used 16S ribosomal RNA gene amplicon sequencing to investigate how archaeal and bacterial communities associated with the widespread scleractinian coral Seriatopora hystrix are influenced by extrinsic (reef habitat and geographic location) and intrinsic (host genotype and Symbiodinium subclade) factors. Bacteria dominate the microbiome of S. hystrix, with members of the Alphaproteobacteria, Gammaproteobacteria and Bacteriodetes being the most predominant in all samples. The richness and evenness of these communities varied between reef habitats, but there was no significant difference between distinct coral host lineages or corals hosting distinct Symbiodinium subclades. The coral microbiomes correlated to reef habitat (depth) and geographic location, with a negative correlation between Alpha- and Gammaproteobacteria, driven by the key members of both groups (Rhodobacteraceae and Hahellaceae, respectively), which showed significant differences between location and depth. This study suggests that the control of microbial communities associated with the scleractinian coral S. hystrix is driven primarily by external environmental conditions rather than by those directly associated with the coral holobiont.

Deep reefs are not universal refuges: Reseeding potential varies among coral species

Genome-wide assessment reveals opposing patterns of vertical connectivity in two depth-generalist coral species. Deep coral reefs (that is, mesophotic coral ecosystems) can act as refuges against major disturbances affecting shallow reefs. It has been proposed that, through the provision of coral propagules, such deep refuges may aid in shallow reef recovery; however, this “reseeding” hypothesis remains largely untested. We conducted a genome-wide assessment of two scleractinian coral species with contrasting reproductive modes, to assess the potential for connectivity between mesophotic (40 m) and shallow (12 m) depths on an isolated reef system in the Western Atlantic (Bermuda). To overcome the pervasive issue of endosymbiont contamination associated with de novo sequencing of corals, we used a novel subtraction reference approach. We have demonstrated that strong depth-associated selection has led to genome-wide divergence in the brooding species Agaricia fragilis (with divergence by depth exceeding divergence by location). Despite introgression from shallow into deep populations, a lack of first-generation migrants indicates that effective connectivity over ecological time scales is extremely limited for this species and thus precludes reseeding of shallow reefs from deep refuges. In contrast, no genetic structuring between depths (or locations) was observed for the broadcasting species Stephanocoenia intersepta, indicating substantial potential for vertical connectivity. Our findings demonstrate that vertical connectivity within the same reef system can differ greatly between species and that the reseeding potential of deep reefs in Bermuda may apply to only a small number of scleractinian species. Overall, we argue that the “deep reef refuge hypothesis” holds for individual coral species during episodic disturbances but should not be assumed as a broader ecosystem-wide phenomenon.

SymbioGBR: a web-based database of Symbiodinium associated with cnidarian hosts on the Great Barrier Reef

BackgroundThe algal endosymbionts (genus Symbiodinium) associated with scleractinian corals (and other reef invertebrates) have received a lot of research attention in the past decade, particularly as certain host-symbiont associations appear more affected by increasing seawater temperatures than others. With the rapid accumulation of information on the diversity of Symbiodinium, it is becoming increasingly difficult to compare newly acquired Symbiodinium data with existing data to detect patterns of host-symbiont specificity on broader spatial scales. The lack of a general consensus on the classification of Symbiodinium species coupled with the variety of different markers used to identify the genus Symbiodinium (ITS1, ITS2, LSU D1/D2, chloroplast 23S rDNA and psbA minicircle) further complicate direct comparison.DescriptionThe SymbioGBR database compiles all currently available Symbiodinium sequences and associated host information of data collected from the Great Barrier Reef into a single relational database that is accessible via a user-friendly, searchable web-based application (http://www.SymbioGBR.org). SymbioGBR allows users to query Symbiodinium types or sequences sourced from various genetic markers (e.g. ITS1, ITS2, LSU D1/D2 and chloroplast 23S) and invertebrate host species to explore their reported associations. In addition, as the database includes sequence information of multiple genetic markers, it allows cross-referencing between conventional (e.g. ITS2 region) and novel markers that exhibit low intragenomic variability (e.g. psbA region). Finally, the database is based on the collection details of individual specimens. Such host-symbiont associations can be assessed quantitatively and viewed in relation to their environmental and geographic context.ConclusionsThe SymbioGBR database provides a comprehensive overview of Symbiodinium diversity and host-associations on the Great Barrier Reef. It provides a quick, user-friendly means to compare newly acquired data on Symbiodinium (e.g. raw sequences or characterized Symbiodinium types) with previous data on the diversity of invertebrate host-symbiont associations on the GBR. The inclusion of psbAncr sequence information allows for validation of widely used ITS1/ITS2 markers and their ability to accurately identify relevant sequences. Most importantly, centralization of sequence information from multiple genetic markers will aid the classification of Symbiodinium species diversity and allow researchers to easily compare patterns of host-Symbiodinium associations.

Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species.

Bathymetric distributions of photosynthetic marine invertebrate species are relatively well studied, however the importance of symbiont zonation (i.e. hosting of distinct algal endosymbiont communities over depth) in determining these depth distributions still remains unclear. Here, we assess the prevalence of symbiont zonation in tropical scleractinian corals by genotyping the Symbiodinium of the 25 most common species over a large depth range (down to 60 m) on a Caribbean reef. Symbiont depth zonation was found to be common on a reef-wide scale (11 out of 25 coral species), and a dominant feature in species with the widest depth distributions. With regards to reproductive strategy, symbiont zonation was more common in broadcasting species, which also exhibited a higher level of polymorphism in the symbiont zonation (i.e. number of different Symbiodinium profiles involved). Species with symbiont zonation exhibited significantly broader depth distributions than those without, highlighting the role of symbiont zonation in shaping the vertical distributions of the coral host. Overall, the results demonstrate that coral reefs can consist of highly structured communities over depth when considering both the coral host and their obligate photosymbionts, which probably has strong implications for the extent of connectivity between shallow and mesophotic habitats.

Mesophotic coral ecosystems on the walls of Coral Sea atolls

A research cruise was undertaken in October 2010 to explore potential mesophotic coral communities (30–150 m) in the recently established Coral Sea Conservation Zone (CSCZ). The CSCZ covers an area of almost one million square kilometres east of the Great Barrier Reef (Australia), with its reefs and atolls located hundreds of kilometres from the nearest landmass and surrounded by deep oceanic water. Three of the atolls in the CSCZ (West Holmes Reef [16.243°S, 147.874°E], East Holmes Reef [16.459°S, 148.024°E] and Flora Reef [16.755°S, 147.738°E]) were assessed using SCUBA and a Seabotix ROV. Shallow reef areas (<30 m) consisted largely of bare substrate with predominantly juvenile corals and very low coral cover due to past cyclone damage and thermal bleaching events. In contrast, the steep walls in 40–100 m depth were covered by extensive Halimeda curtains (Fig. 1a), which harboured diverse scleractinian coral communities, including Acropora, Astreopora, Fungia, Galaxea, Goniastrea, Porites, Mycedium (Fig. 1c), Seriatopora and Turbinaria spp., with Pachyseris (Fig. 1d), Leptoseris and Montipora spp. recorded to 102 m depth. At least one of the collected specimens represents a new species record for Australia: Echino- morpha nishihirai (Fig. 1b). Diverse communities of azooxanthellate octocorals were also observed to 150 m, the maximum depth of the ROV. These observations confirm the presence of mesophotic coral ecosystems (MCEs) along the walls of Coral Sea atolls and indicate that MCEs may form extensive features in the CSCZ. The deep-water coral communities may play an important role in the recovery of shallow reef areas on these isolated atolls by functioning as refugia from the repeated disturbances that have affected these reefs.