Cornelia Roder

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.

In-situ Effects of Eutrophication and Overfishing on Physiology and Bacterial Diversity of the Red Sea Coral Acropora hemprichii

Coral reefs of the Central Red Sea display a high degree of endemism, and are increasingly threatened by anthropogenic effects due to intense local coastal development measures. Overfishing and eutrophication are among the most significant local pressures on these reefs, but there is no information available about their potential effects on the associated microbial community. Therefore, we compared holobiont physiology and 16S-based bacterial communities of tissue and mucus of the hard coral Acropora hemprichii after 1 and 16 weeks of in-situ inorganic nutrient enrichment (via fertilizer diffusion) and/or herbivore exclusion (via caging) in an offshore reef of the Central Red Sea. Simulated eutrophication and/or overfishing treatments did not affect coral physiology with respect to coral respiration rates, chlorophyll a content, zooxanthellae abundance, or δ 15N isotopic signatures. The bacterial community of A. hemprichii was rich and uneven, and diversity increased over time in all treatments. While distinct bacterial species were identified as a consequence of eutrophication, overfishing, or both, two bacterial species that could be classified to the genus Endozoicomonas were consistently abundant and constituted two thirds of bacteria in the coral. Several nitrogen-fixing and denitrifying bacteria were found in the coral specimens that were exposed to experimentally increased nutrients. However, no particular bacterial species was consistently associated with the coral under a given treatment and the single effects of manipulated eutrophication and overfishing could not predict the combined effect. Our data underlines the importance of conducting field studies in a holobiont framework, taking both, physiological and molecular measures into account.

Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences

The significance of bacteria for eukaryotic functioning is increasingly recognized. Coral reef ecosystems critically rely on the relationship between coral hosts and their intracellular photosynthetic dinoflagellates, but the role of the associated bacteria remains largely theoretical. Here, we set out to relate coral‐associated bacterial communities of the fungid host species Ctenactis echinata to environmental settings (geographic location, substrate cover, summer/winter, nutrient and suspended matter concentrations) and coral host abundance. We show that bacterial diversity of C. echinata aligns with ecological differences between sites and that coral colonies sampled at the species’ preferred habitats are primarily structured by one bacterial taxon (genus Endozoicomonas) representing more than 60% of all bacteria. In contrast, host microbiomes from lower populated coral habitats are less structured and more diverse. Our study demonstrates that the content and structure of the coral microbiome aligns with environmental differences and denotes habitat adequacy. Availability of a range of coral host habitats might be important for the conservation of distinct microbiome structures and diversity.

Bacterial profiling of White Plague Disease across corals and oceans indicates a conserved and distinct disease microbiome.

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.

Metabolic plasticity of the corals Porites lutea and Diploastrea heliopora exposed to large amplitude internal waves

The metabolic plasticity of the two mounding coral species Porites lutea (Milne-Edwards and Haime, 1860) and Diploastrea heliopora (Lamarck, 1816) was investigated in the Similan Islands (Thailand), an offshore Andaman Sea island group subjected to large amplitude internal waves (LAIW). Nutrient concentrations were highly correlated with LAIW intensity and contributed to 3- and 10-fold higher symbiont densities in P. lutea and D. heliopora, respectively, along with elevated pigment concentrations, protein content, host tissue, and symbiont biomass. The comparison of LAIW-exposed and LAIW-sheltered island faces, and LAIW-intense and LAIW-weak years suggests a species-specific metabolic plasticity to LAIW, where D. heliopora benefits more from increased nutrient and organic matter availability than P. lutea. The ubiquitous LAIW in Southeast Asia and beyond may provide so far unexplored clues to coral acclimatization to disturbances on various scales, and hence, a potential key to coral resilience to climate change.

Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula

Abstract Aim Coral reefs rely on the symbiosis between scleractinian corals and intracellular, photosynthetic dinoflagellates of the genus Symbiodinium making the assessment of symbiont diversity critical to our understanding of ecological resilience of these ecosystems. This study characterizes Symbiodinium diversity around the Arabian Peninsula, which contains some of the most thermally diverse and understudied reefs on Earth. Location Shallow water coral reefs throughout the Red Sea (RS), Sea of Oman (SO), and Persian/Arabian Gulf (PAG). Methods Next‐generation sequencing of the ITS2 marker gene was used to assess Symbiodinium community composition and diversity comprising 892 samples from 46 hard and soft coral genera. Results Corals were associated with a large diversity of Symbiodinium, which usually consisted of one or two prevalent symbiont types and many types at low abundance. Symbiodinium communities were strongly structured according to geographical region and to a lesser extent by coral host identity. Overall symbiont communities were composed primarily of species from clade A and C in the RS, clade A, C, and D in the SO, and clade C and D in the PAG, representing a gradual shift from C‐ to D‐dominated coral hosts. The analysis of symbiont diversity in an Operational Taxonomic Unit (OTU)‐based framework allowed the identification of differences in symbiont taxon richness over geographical regions and host genera. Main conclusions Our study represents a comprehensive overview over biogeography and molecular diversity of Symbiodinium in the Arabian Seas, where coral reefs thrive in one of the most extreme environmental settings on the planet. As such our data will serve as a baseline for further exploration into the effects of environmental change on host–symbiont pairings and the identification and ecological significance of Symbiodinium types from regions already experiencing ‘Future Ocean’ conditions.

Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease

White Plague Disease (WPD) is implicated in coral reef decline in the Caribbean and is characterized by microbial community shifts in coral mucus and tissue. Studies thus far have focused on assessing microbial communities or the identification of specific pathogens, yet few have addressed holobiont response across metaorganism compartments in coral disease. Here, we report on the first metatranscriptomic assessment of the coral host, algal symbiont, and microbial compartment in order to survey holobiont structure and function in healthy and diseased samples from Orbicella faveolata collected at reef sites off Puerto Rico. Our data indicate metaorganism-wide as well as compartment-specific responses to WPD. Gene expression changes in the diseased coral host involved proteins playing a role in innate immunity, cytoskeletal integrity, cell adhesion, oxidative stress, chemical defense, and retroelements. In contrast, the algal symbiont showed comparatively few expression changes, but of large magnitude, of genes related to stress, photosynthesis, and metal transport. Concordant with the coral host response, the bacterial compartment showed increased abundance of heat shock proteins, genes related to oxidative stress, DNA repair, and potential retroelement activity. Importantly, analysis of the expressed bacterial gene functions establishes the participation of multiple bacterial families in WPD pathogenesis and also suggests a possible involvement of viruses and/or phages in structuring the bacterial assemblage. In this study, we implement an experimental approach to partition the coral holobiont and resolve compartment- and taxa-specific responses in order to understand metaorganism function in coral disease.

First biological measurements of deep-sea corals from the Red Sea

It is usually assumed that metabolic constraints restrict deep-sea corals to cold-water habitats, with ‘deep-sea’ and ‘cold-water’ corals often used as synonymous. Here we report on the first measurements of biological characters of deep-sea corals from the central Red Sea, where they occur at temperatures exceeding 20°C in highly oligotrophic and oxygen-limited waters. Low respiration rates, low calcification rates, and minimized tissue cover indicate that a reduced metabolism is one of the key adaptations to prevailing environmental conditions. We investigated four sites and encountered six species of which at least two appear to be undescribed. One species is previously reported from the Red Sea but occurs in deep cold waters outside the Red Sea raising interesting questions about presumed environmental constraints for other deep-sea corals. Our findings suggest that the present understanding of deep-sea coral persistence and resilience needs to be revisited.

Spatial and seasonal reef calcification in corals and calcareous crusts in the central Red Sea

The existence of coral reef ecosystems critically relies on the reef carbonate framework produced by scleractinian corals and calcareous crusts (i.e., crustose coralline algae). While the Red Sea harbors one of the longest connected reef systems in the world, detailed calcification data are only available from the northernmost part. To fill this knowledge gap, we measured in situ calcification rates of primary and secondary reef builders in the central Red Sea. We collected data on the major habitat-forming coral genera Porites, Acropora, and Pocillopora and also on calcareous crusts (CC) in a spatio-seasonal framework. The scope of the study comprised sheltered and exposed sites of three reefs along a cross-shelf gradient and over four seasons of the year. Calcification of all coral genera was consistent across the shelf and highest in spring. In addition, Pocillopora showed increased calcification at exposed reef sites. In contrast, CC calcification increased from nearshore, sheltered to offshore, exposed reef sites, but also varied over seasons. Comparing our data to other reef locations, calcification in the Red Sea was in the range of data collected from reefs in the Caribbean and Indo-Pacific; however, Acropora calcification estimates were at the lower end of worldwide rates. Our study shows that the increasing coral cover from nearshore to offshore environments aligned with CC calcification but not coral calcification, highlighting the potentially important role of CC in structuring reef cover and habitats. While coral calcification maxima have been typically observed during summer in many reef locations worldwide, calcification maxima during spring in the central Red Sea indicate that summer temperatures exceed the optima of reef calcifiers in this region. This study provides a foundation for comparative efforts and sets a baseline to quantify impact of future environmental change in the central Red Sea.

Mesophotic coral depth acclimatization is a function of host-specific symbiont physiology

Mesophotic coral ecosystems receive increasing attention owing to their potential as deep coral refuges in times of global environmental change. Here, the mechanisms of coral holobiont photoacclimatization over a 60 m depth gradient in the central Red Sea were examined for the four coral genera Porites, Leptoseris, Pachyseris, and Podabacia. General acclimatization strategies were common to all host-symbiont combinations, e.g. Symbiodinium cell densities and photoprotective to light-harvesting pigment ratios both significantly decreased with water depth. Porites harboured Symbiodinium type C15 over the whole 60 m depth range, while Pachyseris and Podabacia had limited vertical distributions and hosted mainly Symbiodinium type C1. Symbiodinium type C15 had generally higher xanthophyll de-epoxidation rates and lower maximum quantum yields than C1, and also exhibited a strong photoacclimatory signal over depth that relates to the large distribution range of Porites. Interestingly, the coral host had an effect on Symbiodinium pigment composition. When comparing Symbiodinium type C1 in Podabacia and Pachyseris, the s-carotene chl a-1, the peridinin chl a-1, and diadinoxanthin chl a-1 ratios were significantly different between host species. Our data support a view that depth acclimatization of corals in the mesophotics is supported by Symbiodinium physiology, which in turn is host-specific.