Coral holobiont functioning under global environmental change

The tropical scleractinian coral holobiont is comprised by the coral animal, dinoflagellate algae of the genus Symbiodinium, and a multitude of other microbes, specifically bacteria, archaea, viruses, and protists. These holobionts are the unit of ecological selection, and remarkably adapted to thrive under oligotrophic (nutrient-poor) conditions. The foundation for this adaptation is provided by the coral-algae symbiosis, a mutualistic nutrient exchange relationship between the coral and Symbiodinium, allowing for the high primary productivity and growth rates of tropical coral holobionts. The coral-algae symbiosis is maintained via nitrogen limitation by the host, and new nitrogen from heterotrophic feeding, dissolved nutrient uptake, or coral-associated nitrogen fixation activity is retained and taken up within the holobiont. This thesis highlights the importance of functional dependencies on nitrogen cycling, particularly the nitrogen fixation pathway, in coral holobiont functioning, and the importance of employing a large set of response parameters covering critical functions of the main holobiont members

Fish diversity patterns and trophic relationships in different types of tropical seagrass meadows in the Spermonde Archipelago, South Sulawesi, Indonesia

In dieser Studie wurden Biodiversität und trophische Beziehungen von Fischgemeinschaften in Seegraswiesen von kleinen Koralleninseln im indonesischen Spermonde-Archipel untersucht. Die gesamte Fischabundanz korrellierte nicht mit der Seegras-Sproßdichte. Diversität und Artenzusammensetzung der Fischgemeinschaften unterschied sich signifikant zwischen einzelnen Seegraswiesen, intertidalen und subtidalen Seegraswiesen und den beiden Inseln. Für die Gesamtabundanz von Fischen gab es keine signifikanten Unterschiede zwischen den Seegraswiesen. Für die sechs häufigsten Fischarten kamen signifikante Unterschiede zwischen Standorten zu tragen (Labridae: Cheilio inermis, Halichoeres argus, H. chloropterus; Hemirhamphidae: Hemirhamphus far; Siganidae: Siganus canaliculatus; Nemipteridae: Pentapodus trivittatus). Die Fischdiversität war an dem Standort mit dem stärksten anthropogenen Einfluss am höchsten. Seegraswiesen in einem späten Sukzessionsstadium (hohe strukturelle Komplexität) waren artenreicher als Seegraswiesen in frühen Stadien (niedrige Komplexität). Art-Akummulationskurven zeigten dennoch für keinen der beprobten Standorte Sättigung. Für zwei der drei artenreichsten Fischfamilien, den Labriden (Lippfischen) und den Pomacentriden (Riffbarschen), erreichten Art-Akummulationskurven keine Saturierung, während die Kurve für die dritt-artenreichste Familie, den Nemipteriden (Scheinschnappern) Sättigung erreicht. Wie erwartet zeigte die Stabile Isotopen-Analyse, dass Primärproduzenten eine geringere Anreicherung an δ15N und δ13C aufweisen als die meisten Tier-Taxa. Die Isotopen-Signaturen der Evertebraten hatten einen größeren Umfang als die der Fische, allerdings war die stärkste Anreicherung für schweren Stickstoff in der piscivoren Fischgilde zu finden. Die niedrigsten Isotopen-Signaturen für Tiere wurden bei drei Arten von Muscheln (Codakia tigerina, Solemya pusilla, Fimbria sp.) und bei zwei Krebs-Arten (Eucalliax panglaoensis und Calliaxina sp.) gefunden. Es wird vermutet, dass diese Taxa eine Symbiose mit chemoautotrophen Bakterien pflegen und dass aus dieser Symbiose der für diese Organismen notwendige Kohlenstoff und Stickstoff für Wachstum und Entwicklung stammt. Die höchsten trophischen Stufen basierend auf Stickstoffwerten aus der Stabilen Isotopen-Analyse waren 3.69 und 3.44 für zwei piscivore Fische, den Großen Barrakuda (Sphyraena barracuda) und den Krokodils-Hornhecht (Tylosurus crocodilus). Herbivore Fische finden sich dagegen auf der niedrigsten Stufe wieder: der Kaninchenfisch Siganus virgatus belegt eine trophische Stufe von lediglich 1.91 und kann dadurch als Primärkonsument identifiziert werden. Weder Seegras noch Phytoplankton konnte in der Isotopen-Analyse als wichtige Nahrungsquelle in der untersuchten Seegraswiese identifiziert werden, der Algenaufwuchs auf den Seegräsern dürfte jedoch eine große Rolle im beschriebenen Nahrungsnetz spielen. Darm-Inhalts-Analysen zeigten vier Nahrungsgilden (Zoobenthivore, Omnivore, Piscivore, Herbivore). Die Nahrungskategorien, die in den meisten Mägen oder Därmen gefunden wurden, waren die der Crustaceen, der Gastropoden und der Seegräser. Die trophische Zusammensetzung von Fischgemeinschaften in unterschiedlichen Seegraswiesen zeigt distinkte Muster zwischen intertidalen und subtidalen Standorten. Die Gilden-Zusammensetzung basierend auf Daten aus einem visuellen Fisch-Zensus enthüllte sechs Nahrungsgilden in den Seegraswiesen: Herbivore, Zooplanktivore, Corallivore, Omnivore, Zoobenthivore und Piscivore. Unterschiede zu den Ergebnissen der Darm-Inhalts-Analyse werden damit erklärt, dass nicht alle Fischarten in die Analyse miteinbezogen werden konnten. Die zoobenthivore Gilde weist die höchsten Taxon-Zahlen an allen Standorten auf. Die artenmäßig kleinsten Gilden sind die Corallivoren, Piscivoren und Zooplanktivoren. Die höchsten Abundanzen sind an den intertidalen Standorten für die Zooplanktivoren und für die subtidalen Standorte für die Omnivoren und Zoobenthivoren zu finden. Corallivore, Piscivore und Herbivore sind an allen Standorten nur in geringen Abundanzen anzutreffen.The present study investigated the nature and trophic relationships of fish assemblages in seagrass beds at small coral islands in the Indonesian Spermonde Archipelago. Total fish abundance did not correlate with seagrass shoot densities. Diversity and species composition of fish assemblages differed significantly among five examined seagrass beds, between intertidal and subtidal study sites, and between the two islands, while there was no significant difference for total fish abundance. Six common species, however, showed significant differences between study sites (Labridae: Cheilio inermis, Halichoeres argus, H. chloropterus; Hemirhamphidae: Hemirhamphus far; Siganidae: Siganus canaliculatus; Nemipteridae: Pentapodus trivittatus). Fish diversity was highest at the most impacted study site at Barrang Lompo South. Seagrass beds in a late stage of succession (high structural complexity) were more species-rich than seagrass beds in an early stage of succession (low structural complexity). Nonetheless, species-accumulation curves for total diversity did not show saturation for any of the study sites. For two of the most speciose fish families in the present study, the Labridae and Pomacentridae, species-accumulation curves did not exhibit saturation, whereas the curve for the third family, the Nemipteridae, clearly was saturated. As expected, primary producers were more depleted in stable δ15N and δ13C isotope values than most animal taxa. Isotopic values of invertebrates had a broader range than those of fish, although the highest stable nitrogen enrichment was found for piscivorous fish. Lowest isotopic signatures for animals were recorded for bivalves and two taxa of crustaceans that are assumed to have bacterial symbionts. Trophic levels calculated based on stable isotopes show values of 3.69 and 3.44 for piscivorous fish such as barracuda Sphyraena barracuda and garfish Tylosurus crocodilus, respectively, whereas a herbivorous fish such as the rabbit fish Siganus virgatus feeds at a trophic level of only 1.91, characterizing it as a primary consumer. Neither seagrass nor phytoplankton was found to be utilized widely as a food source in the present seagrass bed. Seagrass epiphytes appear to play a major role in trophic relationship of the described food web. Analysis of gut content revealed four major feeding guilds (zoobenthivores, omnivores, piscivores, herbivores). The most common food items over all guts sampled were crustaceans, gastropods and seagrass. The trophic composition of the fish assemblages differs distinctly between intertidal and subtidal study sites. In contrast to gut content analysis, the trophic contribution of fish assemblages based on visual census data revealed six feeding guilds in the seagrass beds (herbivorous, zooplanktivorous, corallivores, omnivorous, zoobenthivorous, piscivorous). This difference to gut-content analysis might be due to the fact that not all fish species could be included into the analysis (no zooplanktivores and corallivores). With respect to taxon numbers, zoobenthivores dominate over all study sites, and corallivores, piscivores and zooplanktivores accounted for the smallest proportions. With respect to individual counts, zooplanktivores dominated intertidal sites and omnivores and zoobenthivores dominated subtidal sites; again, corallivores, piscivores and herbivores accounted for smallest trophic guilds

Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling

Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions

Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling

Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions.Peer reviewe

Coral microbiome diversity reflects mass coral bleaching susceptibility during the 2016 El Niño heat wave

Repeat marine heat wave‐induced mass coral bleaching has decimated reefs in Seychelles for 35 years, but how coral‐associated microbial diversity (microalgal endosymbionts of the family Symbiodiniaceae and bacterial communities) potentially underpins broad‐scale bleaching dynamics remains unknown. We assessed microbiome composition during the 2016 heat wave peak at two contrasting reef sites (clear vs. turbid) in Seychelles, for key coral species considered bleaching sensitive (Acropora muricata, Acropora gemmifera) or tolerant (Porites lutea, Coelastrea aspera). For all species and sites, we sampled bleached versus unbleached colonies to examine how microbiomes align with heat stress susceptibility. Over 30% of all corals bleached in 2016, half of which were from Acropora sp. and Pocillopora sp. mass bleaching that largely transitioned to mortality by 2017. Symbiodiniaceae ITS2‐sequencing revealed that the two Acropora sp. and P. lutea generally associated with C3z/C3 and C15 types, respectively, whereas C. aspera exhibited a plastic association with multiple D types and two C3z types. 16S rRNA gene sequencing revealed that bacterial communities were coral host‐specific, largely through differences in the most abundant families, Hahellaceae (comprising Endozoicomonas), Rhodospirillaceae, and Rhodobacteraceae. Both Acropora sp. exhibited lower bacterial diversity, species richness, and community evenness compared to more bleaching‐resistant P. lutea and C. aspera. Different bleaching susceptibility among coral species was thus consistent with distinct microbiome community profiles. These profiles were conserved across bleached and unbleached colonies of all coral species. As this pattern could also reflect a parallel response of the microbiome to environmental changes, the detailed functional associations will need to be determined in future studies. Further understanding such microbiome‐environmental interactions is likely critical to target more effective management within oceanically isolated reefs of Seychelles

Der Korallen-Holobiont im globalen Wandel

The tropical scleractinian coral holobiont is comprised by the coral animal, dinoflagellate algae of the genus Symbiodinium, and a multitude of other microbes, specifically bacteria, archaea, viruses, and protists. These holobionts are the unit of ecological selection, and remarkably adapted to thrive under oligotrophic (nutrient-poor) conditions. The foundation for this adaptation is provided by the coral-algae symbiosis, a mutualistic nutrient exchange relationship between the coral and Symbiodinium, allowing for the high primary productivity and growth rates of tropical coral holobionts. The coral-algae symbiosis is maintained via nitrogen limitation by the host, and new nitrogen from heterotrophic feeding, dissolved nutrient uptake, or coral-associated nitrogen fixation activity is retained and taken up within the holobiont. This thesis highlights the importance of functional dependencies on nitrogen cycling, particularly the nitrogen fixation pathway, in coral holobiont functioning, and the importance of employing a large set of response parameters covering critical functions of the main holobiont members

Nitrogen cycling in corals: the key to understanding holobiont functioning?

Corals are animals that form close mutualistic associations with endosymbiotic photosynthetic algae of the genus Symbiodinium. Together they provide the calcium carbonate framework of coral reef ecosystems. The importance of the microbiome (i.e., bacteria, archaea, fungi, and viruses) to holobiont functioning has only recently been recognized. Given that growth and density of Symbiodinium within the coral host is highly dependent on nitrogen availability, nitrogen-cycling microbes may be of fundamental importance to the stability of the coral–algae symbiosis and holobiont functioning, in particular under nutrient-enriched and -depleted scenarios. We summarize what is known about nitrogen cycling in corals and conclude that disturbance of microbial nitrogen cycling may be tightly linked to coral bleaching and disease

Stimulated Respiration and Net Photosynthesis in Cassiopeia sp. during Glucose Enrichment Suggests in hospite CO2 Limitation of Algal Endosymbionts

The endosymbiosis between cnidarians and dinoflagellates of the genus Symbiodinium is key to the high productivity of tropical coral reefs. In this endosymbiosis, Symbiodinium translocate most of their photosynthates to their animal host in exchange for inorganic nutrients. Among these, carbon dioxide (CO2) derived from host respiration helps to meet the carbon requirements to sustain photosynthesis of the dinoflagellates. Nonetheless, recent studies suggest that productivity in symbiotic cnidarians such as corals is CO2-limited. Here we show that glucose enrichment stimulates respiration and gross photosynthesis rates by 80 and 140%, respectively, in the symbiotic upside-down jellyfish Cassiopeia sp. from the Central Red Sea. Our findings show that glucose was rapidly consumed and respired within the Cassiopeia sp. holobiont. The resulting increase of CO2 availability in hospite in turn likely stimulated photosynthesis in Symbiodinium. Hence, the increase of photosynthesis under these conditions suggests that CO2 limitation of Symbiodinium is a common feature of stable cnidarian holobionts and that the stimulation of holobiont metabolism may attenuate this CO2 limitation

Relative abundance of nitrogen cycling microbes in coral holobionts reflects environmental nitrate availability

Recent research suggests that nitrogen (N) cycling microbes are important for coral holobiont functioning. In particular, coral holobionts may acquire bioavailable N via prokaryotic dinitrogen (N-2) fixation or remove excess N via denitrification activity. However, our understanding of environmental drivers on these processes in hospite remains limited. Employing the strong seasonality of the central Red Sea, this study assessed the effects of environmental parameters on the proportional abundances of N cycling microbes associated with the hard corals Acropora hemprichii and Stylophora pistillata. Specifically, we quantified changes in the relative ratio between nirS and nifH gene copy numbers, as a proxy for seasonal shifts in denitrification and N-2 fixation potential in corals, respectively. In addition, we assessed coral tissue-associated Symbiodiniaceae cell densities and monitored environmental parameters to provide a holobiont and environmental context, respectively. While ratios of nirS to nifH gene copy numbers varied between seasons, they revealed similar seasonal patterns in both coral species, with ratios closely following patterns in environmental nitrate availability. Symbiodiniaceae cell densities aligned with environmental nitrate availability, suggesting that the seasonal shifts in nirS to nifH gene abundance ratios were probably driven by nitrate availability in the coral holobiont. Thereby, our results suggest that N cycling in coral holobionts probably adjusts to environmental conditions by increasing and/or decreasing denitrification and N-2 fixation potential according to environmental nitrate availability. Microbial N cycling may, thus, extenuate the effects of changes in environmental nitrate availability on coral holobionts to support the maintenance of the coral-Symbiodiniaceae symbiosis.Peer reviewe