Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching

The disruption of the coral–algae symbiosis (coral bleaching) due to rising sea surface temperatures has become an unprecedented global threat to coral reefs. Despite decades of research, our ability to manage mass bleaching events remains hampered by an incomplete mechanistic understanding of the processes involved. In this study, we induced a coral bleaching phenotype in the absence of heat and light stress by adding sugars. The sugar addition resulted in coral symbiotic breakdown accompanied by a fourfold increase of coral‐associated microbial nitrogen fixation. Concomitantly, increased N:P ratios by the coral host and algal symbionts suggest excess availability of nitrogen and a disruption of the nitrogen limitation within the coral holobiont. As nitrogen fixation is similarly stimulated in ocean warming scenarios, here we propose a refined coral bleaching model integrating the cascading effects of stimulated microbial nitrogen fixation. This model highlights the putative role of nitrogen‐fixing microbes in coral holobiont functioning and breakdown.     

Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions

Functional traits define species by their ecological role in the ecosystem. Animals themselves are host–microbe ecosystems (holobionts), and the application of ecophysiological approaches can help to understand their functioning. In hard coral holobionts, communities of dinitrogen (N₂)-fixing prokaryotes (diazotrophs) may contribute a functional trait by providing bioavailable nitrogen (N) that could sustain coral productivity under oligotrophic conditions. This study quantified N₂ fixation by diazotrophs associated with four genera of hermatypic corals on a northern Red Sea fringing reef exposed to high seasonality. We found N₂ fixation activity to be 5- to 10-fold higher in summer, when inorganic nutrient concentrations were lowest and water temperature and light availability highest. Concurrently, coral gross primary productivity remained stable despite lower Symbiodinium densities and tissue chlorophyll a contents. In contrast, chlorophyll a content per Symbiodinium cell increased from spring to summer, suggesting that algal cells overcame limitation of N, an essential element for chlorophyll synthesis. In fact, N₂ fixation was positively correlated with coral productivity in summer, when its contribution was estimated to meet 11% of the Symbiodinium N requirements. These results provide evidence of an important functional role of diazotrophs in sustaining coral productivity when alternative external N sources are scarce.     

Climate change affects key nitrogen-fixing bacterial populations on coral reefs

Coral reefs are at serious risk due to events associated with global climate change. Elevated ocean temperatures have unpredictable consequences for the ocean''s biogeochemical cycles. The nitrogen cycle is driven by complex microbial transformations, including nitrogen fixation. This study investigated the effects of increased seawater temperature on bacteria able to fix nitrogen (diazotrophs) that live in association with the mussid coral Mussismilia harttii. Consistent increases in diazotroph abundances and diversities were found at increased temperatures. Moreover, gradual shifts in the dominance of particular diazotroph populations occurred as temperature increased, indicating a potential future scenario of climate change. The temperature-sensitive diazotrophs may provide useful bioindicators of the effects of thermal stress on coral reef health, allowing the impact of thermal anomalies to be monitored. In addition, our findings support the development of research on different strategies to improve the fitness of corals during events of thermal stress, such as augmentation with specific diazotrophs.     

The trace metal economy of the coral holobiont: supplies,demands and exchanges

The juxtaposition of highly productive coral reef ecosystems in oligotrophic waters has spurred substantial interest and progress in our understanding of macronutrient uptake, exchange, and recycling among coral holobiont partners (host coral, dinoflagellate endosymbiont, endolithic algae, fungi, viruses, bacterial communities). By contrast, the contribution of trace metals to the physiological performance of the coral holobiont and, in turn, the functional ecology of reef-building corals remains unclear. The coral holobiont's trace metal economy is a network of supply, demand, and exchanges upheld by cross-kingdom symbiotic partnerships. Each partner has unique trace metal requirements that are central to their biochemical functions and the metabolic stability of the holobiont. Organismal homeostasis and the exchanges among partners determine the ability of the coral holobiont to adjust to fluctuating trace metal supplies in heterogeneous reef environments. This review details the requirements for trace metals in core biological processes and describes how metal exchanges among holobiont partners are key to sustaining complex nutritional symbioses in oligotrophic environments. Specifically, we discuss how trace metals contribute to partner compatibility, ability to cope with stress, and thereby to organismal fitness and distribution. Beyond holobiont trace metal cycling, we outline how the dynamic nature of the availability of environmental trace metal supplies can be influenced by a variability of abiotic factors (e.g. temperature, light, pH, etc.). Climate change will have profound consequences on the availability of trace metals and further intensify the myriad stressors that influence coral survival. Lastly, we suggest future research directions necessary for understanding the impacts of trace metals on the coral holobiont symbioses spanning subcellular to organismal levels, which will inform nutrient cycling in coral ecosystems more broadly. Collectively, this cross-scale elucidation of the role of trace metals for the coral holobiont will allow us to improve forecasts of future coral reef function.     

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.     

Estimating the Potential for Adaptation of Corals to Climate Warming

The persistence of tropical coral reefs is threatened by rapidly increasing climate warming, causing a functional breakdown of the obligate symbiosis between corals and their algal photosymbionts (Symbiodinium) through a process known as coral bleaching. Yet the potential of the coral-algal symbiosis to genetically adapt in an evolutionary sense to warming oceans is unknown. Using a quantitative genetics approach, we estimated the proportion of the variance in thermal tolerance traits that has a genetic basis (i.e. heritability) as a proxy for their adaptive potential in the widespread Indo-Pacific reef-building coral Acropora millepora. We chose two physiologically different populations that associate respectively with one thermo-tolerant (Symbiodinium clade D) and one less tolerant symbiont type (Symbiodinium C2). In both symbiont types, pulse amplitude modulated (PAM) fluorometry and high performance liquid chromatography (HPLC) analysis revealed significant heritabilities for traits related to both photosynthesis and photoprotective pigment profile. However, quantitative real-time polymerase chain reaction (qRT-PCR) assays showed a lack of heritability in both coral host populations for their own expression of fundamental stress genes. Coral colony growth, contributed to by both symbiotic partners, displayed heritability. High heritabilities for functional key traits of algal symbionts, along with their short clonal generation time and high population sizes allow for their rapid thermal adaptation. However, the low overall heritability of coral host traits, along with the corals'' long generation time, raise concern about the timely adaptation of the coral-algal symbiosis in the face of continued rapid climate warming.     

Patterns of environmental variability influence coral‐associated bacterial and algal communities on the Mesoamerican Barrier Reef

A coral's capacity to alter its microbial symbionts may enhance its fitness in the face of climate change. Recent work predicts exposure to high environmental variability may increase coral resilience and adaptability to future climate conditions. However, how this heightened environmental variability impacts coral‐associated microbial communities remains largely unexplored. Here, we examined the bacterial and algal symbionts associated with two coral species of the genus Siderastrea with distinct life history strategies from three reef sites on the Belize Mesoamerican Barrier Reef System with low or high environmental variability. Our results reveal bacterial community structure, as well as alpha‐ and beta‐diversity patterns, vary by host species. Differences in bacterial communities between host species were partially explained by high abundance of Deltaproteobacteria and Rhodospirillales and high bacterial diversity in Siderastrea radians. Our findings also suggest Siderastrea spp. have dynamic core bacterial communities that likely drive differences observed in the entire bacterial community, which may play a critical role in rapid acclimatization to environmental change. Unlike the bacterial community, Symbiodiniaceae composition was only distinct between host species at high thermal variability sites, suggesting that different factors shape bacterial versus algal communities within the coral holobiont. Our findings shed light on how domain‐specific shifts in dynamic microbiomes may allow for unique methods of enhanced host fitness.     

Assessing the effects of iron enrichment across holobiont compartments reveals reduced microbial nitrogen fixation in the Red Sea coral Pocillopora verrucosa

The productivity of coral reefs in oligotrophic tropical waters is sustained by an efficient uptake and recycling of nutrients. In reef‐building corals, the engineers of these ecosystems, this nutrient recycling is facilitated by a constant exchange of nutrients between the animal host and endosymbiotic photosynthetic dinoflagellates (zooxanthellae), bacteria, and other microbes. Due to the complex interactions in this so‐called coral holobiont, it has proven difficult to understand the environmental limitations of productivity in corals. Among others, the micronutrient iron has been proposed to limit primary productivity due to its essential role in photosynthesis and bacterial processes. Here, we tested the effect of iron enrichment on the physiology of the coral Pocillopora verrucosa from the central Red Sea during a 12‐day experiment. Contrary to previous reports, we did not see an increase in zooxanthellae population density or gross photosynthesis. Conversely, respiration rates were significantly increased, and microbial nitrogen fixation was significantly decreased. Taken together, our data suggest that iron is not a limiting factor of primary productivity in Red Sea corals. Rather, increased metabolic demands in response to iron enrichment, as evidenced by increased respiration rates, may reduce carbon (i.e., energy) availability in the coral holobiont, resulting in reduced microbial nitrogen fixation. This decrease in nitrogen supply in turn may exacerbate the limitation of other nutrients, creating a negative feedback loop. Thereby, our results highlight that the effects of iron enrichment appear to be strongly dependent on local environmental conditions and ultimately may depend on the availability of other nutrients.     

Meta-analysis of diazotrophic signatures across terrestrial ecosystems at the continental scale

Biological nitrogen fixation performed by diazotrophs forms a cornerstone of Earth's terrestrial ecosystem productivity. However, the composition, diversity and distribution of soil diazotrophs are poorly understood across different soil ecosystems. Furthermore, the biological potential of the key diazotroph species in relation to key environmental parameters is unknown. To address this, we used meta-analysis approach to merge together 39 independent diazotroph amplicon sequencing (nifH gene) datasets consisting of 1988 independent soil samples. We then employed multiple statistical analyses and machine-learning approaches to compare diazotroph community differences and indicator species between terrestrial ecosystems on a global scale. The distribution, composition and structure of diazotroph communities varied across seven different terrestrial ecosystems, with community composition exhibiting an especially clear effect. The Cyanobacteria were the most abundant taxa in crust ecosystems (accounting for ~45% of diazotrophs), while other terrestrial ecosystems were dominated by Proteobacteria, including Alpha-, Beta- and Gamma-Proteobacteria (accounting for ~70% of diazotrophs). Farmland ecosystems harboured the highest and crust ecosystems the lowest alpha and phylogenetic diversities. Azospirillum zeae, Skermanella aerolata and four Bradyrhizobium species were identified as key indicator species of potential diazotroph activity. Overall, diazotroph abundances and distribution were affected by multiple environmental parameters, including soil pH, nitrogen, organic carbon, C:N ratio and annual mean precipitation and temperature. Together, our findings suggest that based on the relative abundance and diversity of nifH marker gene, diazotrophs have adapted to a range of environmental niches globally.     

Microbially facilitated nitrogen cycling in tropical corals

Tropical scleractinian corals support a diverse assemblage of microbial symbionts. This ‘microbiome’ possesses the requisite functional diversity to conduct a range of nitrogen (N) transformations including denitrification, nitrification, nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA). Very little direct evidence has been presented to date verifying that these processes are active within tropical corals. Here we use a combination of stable isotope techniques, nutrient uptake calculations and captured metagenomics to quantify rates of nitrogen cycling processes in a selection of tropical scleractinian corals. Denitrification activity was detected in all species, albeit with very low rates, signifying limited importance in holobiont N removal. Relatively greater nitrogen fixation activity confirms that corals are net N importers to reef systems. Low net nitrification activity suggests limited N regeneration capacity; however substantial gross nitrification activity may be concealed through nitrate consumption. Based on nrfA gene abundance and measured inorganic N fluxes, we calculated significant DNRA activity in the studied corals, which has important implications for coral reef N cycling and warrants more targeted investigation. Through the quantification and characterisation of all relevant N-cycling processes, this study provides clarity on the subject of tropical coral-associated biogeochemical N-cycling.Subject terms: Stable isotope analysis, Biogeochemistry, Biogeochemistry, Biogeochemistry, Microbial ecology     

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.     

The Roles and Interactions of Symbiont,Host and Environment in Defining Coral Fitness

Background

Reef-building corals live in symbiosis with a diverse range of dinoflagellate algae (genus Symbiodinium) that differentially influence the fitness of the coral holobiont. The comparative role of symbiont type in holobiont fitness in relation to host genotype or the environment, however, is largely unknown. We addressed this knowledge gap by manipulating host-symbiont combinations and comparing growth, survival and thermal tolerance among the resultant holobionts in different environments.

Methodology/Principal Findings

Offspring of the coral, Acropora millepora, from two thermally contrasting locations, were experimentally infected with one of six Symbiodinium types, which spanned three phylogenetic clades (A, C and D), and then outplanted to the two parental field locations (central and southern inshore Great Barrier Reef, Australia). Growth and survival of juvenile corals were monitored for 31–35 weeks, after which their thermo-tolerance was experimentally assessed. Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness. Furthermore, coral-algal associations were established with symbiont types belonging to clades A, C and D, but three out of four symbiont types belonging to clade C failed to establish a symbiosis. Associations with clade A had the lowest fitness and were unstable in the field. Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.

Conclusions/Significance

These results highlight the complex interactions that occur between the coral host, the algal symbiont, and the environment to shape the fitness of the coral holobiont. An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.     

Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome

The importance of Symbiodinium algal endosymbionts and a diverse suite of bacteria for coral holobiont health and functioning are widely acknowledged. Yet, we know surprisingly little about microbial community dynamics and the stability of host‐microbe associations under adverse environmental conditions. To gain insight into the stability of coral host‐microbe associations and holobiont structure, we assessed changes in the community structure of Symbiodinium and bacteria associated with the coral Pocillopora verrucosa under excess organic nutrient conditions. Pocillopora‐associated microbial communities were monitored over 14 days in two independent experiments. We assessed the effect of excess dissolved organic nitrogen (DON) and excess dissolved organic carbon (DOC). Exposure to excess nutrients rapidly affected coral health, resulting in two distinct stress phenotypes: coral bleaching under excess DOC and severe tissue sloughing (>90% tissue loss resulting in host mortality) under excess DON. These phenotypes were accompanied by structural changes in the Symbiodinium community. In contrast, the associated bacterial community remained remarkably stable and was dominated by two Endozoicomonas phylotypes, comprising on average 90% of 16S rRNA gene sequences. This dominance of Endozoicomonas even under conditions of coral bleaching and mortality suggests the bacterial community of P. verrucosa may be rather inflexible and thereby unable to respond or acclimatize to rapid changes in the environment, contrary to what was previously observed in other corals. In this light, our results suggest that coral holobionts might occupy structural landscapes ranging from a highly flexible to a rather inflexible composition with consequences for their ability to respond to environmental change.     

A symbiotic nutrient exchange within the cyanosphere microbiome of the biocrust cyanobacterium,Microcoleus vaginatus

Microcoleus vaginatus plays a prominent role as both primary producer and pioneer in biocrust communities from dryland soils. And yet, it cannot fix dinitrogen, essential in often nitrogen-limited drylands. But a diazotroph-rich “cyanosphere” has been described in M. vaginatus, hinting that there exists a C for N exchange between the photoautotroph and heterotrophic diazotrophs. We provide evidence for this by establishing such a symbiosis in culture and by showing that it is selective and dependent on nitrogen availability. In natural populations, provision of nitrogen resulted in loss of diazotrophs from the cyanosphere of M. vaginatus compared to controls, but provision of phosphorus did not. Co-culturing of pedigreed cyanosphere diazotroph isolates with axenic M. vaginatus resulted in copious growth in C and N-free medium, but co-culture with non-cyanosphere diazotrophs or other heterotrophs did not. Unexpectedly, bundle formation in M. vaginatus, diacritical to the genus but not seen in axenic culture, was restored in vitro by imposed nitrogen limitation or, even more strongly, by co-culture with diazotrophic partners, implicating this trait in the symbiosis. Our findings provide direct evidence for a symbiotic relationship between M. vaginatus and its cyanosphere and help explain how it can be a global pioneer in spite of its genetic shortcomings.Subject terms: Microbial ecology, Soil microbiology     

Regulation and control of intracellular algae (= zooxanthellae) in hard corals

To examine algal (= zooxanthellae) regulation and control, and the factors determining algal densities in hard corals, the zooxanthellae mitotic index and release rates were regularly determined in branch tips from a colony of a staghorn coral, Acropora formosa, recovering from a coral ''bleaching'' event (the stress-related dissociation of the coral–algal symbiosis). Mathematical models based upon density-dependent decreases in the algal division frequency and increases in algal release rates during the post-bleaching recovery period accurately predict the observed recovery period (ca. 20 weeks). The models suggest that (i) the colony recovered its algal population from the division of the remaining zooxanthellae, and (ii) the continual loss of zooxanthellae significantly slowed the recovery of the coral. Possible reasons for the ''paradoxical'' loss of healthy zooxanthellae from the bleached coral are discussed in terms of endodermal processes occurring in the recovering coral and the redistribution of newly formed zooxanthellae to aposymbiotic host cells. At a steady-state algal density of 2.1 x 10⁶ zooxanthellae cm^-2 at the end of the recovery period, the zooxanthellae would have to form a double layer of cells in the coral tissues, consistent with microscopic observations. Neighbouring colonies of A. formosa with inherently higher algal densities possess proportionately smaller zooxanthellae. Results suggest that space availability and the size of the algal symbionts determines the algal densities in the coral colonies. The large increases in the algal densities reported in corals exposed to elevated nutrient concentrations (i.e between a two- and five-fold increase in the algal standing stock) are not consistent with this theory. We suggest that increases of this magnitude are a product of the experimental conditions: reasons for this statement are discussed. We propose that the stability of the coral–algal symbiosis under non-stress conditions, and the constancy of zooxanthellae densities in corals reported across growth form, depth and geographic range, are related to space availability limiting algal densities. However, at these densities, zooxanthellae have attributes consistent with nutrient limitation.     

Unfamiliar partnerships limit cnidarian holobiont acclimation to warming

Enhancing the resilience of corals to rising temperatures is now a matter of urgency, leading to growing efforts to explore the use of heat tolerant symbiont species to improve their thermal resilience. The notion that adaptive traits can be retained by transferring the symbionts alone, however, challenges the holobiont concept, a fundamental paradigm in coral research. Holobiont traits are products of a specific community (holobiont) and all its co‐evolutionary and local adaptations, which might limit the retention or transference of holobiont traits by exchanging only one partner. Here we evaluate how interchanging partners affect the short‐ and long‐term performance of holobionts under heat stress using clonal lineages of the cnidarian model system Aiptasia (host and Symbiodiniaceae strains) originating from distinct thermal environments. Our results show that holobionts from more thermally variable environments have higher plasticity to heat stress, but this resilience could not be transferred to other host genotypes through the exchange of symbionts. Importantly, our findings highlight the role of the host in determining holobiont productivity in response to thermal stress and indicate that local adaptations of holobionts will likely limit the efficacy of interchanging unfamiliar compartments to enhance thermal tolerance.     

Communality in microbial stress response and differential metabolic interactions revealed by time-series analysis of sponge symbionts

The diversity and function of sponge-associated symbionts is now increasingly understood; however, we lack an understanding of how they dynamically behave to ensure holobiont stability in the face of environmental variation. Here, we performed a metatransciptomic analysis on three microbial symbionts of the sponge Cymbastela concentrica in situ over 14 months and through differential gene expression and correlation analysis to environmental variables uncovered differences that speak to their metabolic activities and level of symbiotic and environmental interactions. The nitrite-oxidizing Ca. Porinitrospira cymbastela maintained a seemingly stable metabolism, with the few differentially expressed genes related only to stress responses. The heterotrophic Ca. Porivivens multivorans displayed differential use of holobiont-derived compounds and respiration modes, while the ammonium-oxidizing archaeon Ca. Nitrosopumilus cymbastelus differentially expressed genes related to phosphate metabolism and symbiosis effectors. One striking similarity between the symbionts was their similar variation in expression of stress-related genes. Our time-series study showed that the microbial community of C. concentrica undertakes dynamic gene expression adjustments in response to the surroundings, tuned to deal with general stress and metabolic interactions between holobiont members. The success of these dynamic adjustments likely underpins the stability of the sponge holobiont and may provide resilience against environmental change.     

Long‐term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome

Scleractinian corals are assumed to be stenohaline osmoconformers, although they are frequently subjected to variations in seawater salinity due to precipitation, freshwater run‐off and other processes. Observed responses to altered salinity levels include differences in photosynthetic performance, respiration and increased bleaching and mortality of the coral host and its algal symbiont, but a study looking at bacterial community changes is lacking. Here, we exposed the coral Fungia granulosa to strongly increased salinity levels in short‐ and long‐term experiments to disentangle temporal and compartment effects of the coral holobiont (i.e. coral host, symbiotic algae and associated bacteria). Our results show a significant reduction in calcification and photosynthesis, but a stable microbiome after short‐term exposure to high‐salinity levels. By comparison, long‐term exposure yielded unchanged photosynthesis levels and visually healthy coral colonies indicating long‐term acclimation to high‐salinity levels that were accompanied by a major coral microbiome restructuring. Importantly, a bacterium in the family Rhodobacteraceae was succeeded by Pseudomonas veronii as the numerically most abundant taxon. Further, taxonomy‐based functional profiling indicates a shift in the bacterial community towards increased osmolyte production, sulphur oxidation and nitrogen fixation. Our study highlights that bacterial community composition in corals can change within days to weeks under altered environmental conditions, where shifts in the microbiome may enable adjustment of the coral to a more advantageous holobiont composition.     

Competition and succession among coral endosymbionts

Host species often support a genetically diverse guild of symbionts, the identity and performance of which can determine holobiont fitness under particular environmental conditions. These symbiont communities are structured by a complex set of potential interactions, both positive and negative, between the host and symbionts and among symbionts. In reef‐building corals, stable associations with specific symbiont species are common, and we hypothesize that this is partly due to ecological mechanisms, such as succession and competition, which drive patterns of symbiont winnowing in the initial colonization of new generations of coral recruits. We tested this hypothesis using the experimental framework of the de Wit replacement series and found that competitive interactions occurred among symbionts which were characterized by unique ecological strategies. Aposymbiotic octocoral recruits within high‐ and low‐light environments were inoculated with one of three Symbiodiniaceae species as monocultures or with cross‐paired mixtures, and we tracked symbiont uptake using quantitative genetic assays. Priority effects, in which early colonizers excluded competitive dominants, were evidenced under low light, but these early opportunistic species were later succeeded by competitive dominants. Under high light, a more consistent competitive hierarchy was established in which competitive dominants outgrew and limited the abundance of others. These findings provide insight into mechanisms of microbial community organization and symbiosis breakdown and recovery. Furthermore, transitions in competitive outcomes across spatial and temporal environmental variation may improve lifetime host fitness.