scholarly journals Host genotype and stable differences in algal symbiont communities explain patterns of thermal stress response of Montipora capitata following thermal pre-exposure and across multiple bleaching events

2020 ◽  
Author(s):  
Jenna Dilworth ◽  
Carlo Caruso ◽  
Valerie A. Kahkejian ◽  
Andrew C. Baker ◽  
Crawford Drury

AbstractAs sea surface temperatures increase worldwide due to climate change, coral bleaching events are becoming more frequent and severe, resulting in reef degradation. Leveraging the inherent ability of reef-building corals to acclimatize to thermal stress via pre-exposure to protective temperature treatments may become an important tool in improving the resilience of coral reefs to rapid environmental change. We investigated whether historical bleaching phenotype, coral host genotype, and exposure to protective temperature treatments would affect the response of the Hawaiian coral Montipora capitata to natural thermal stress. Fragments were collected from colonies that demonstrated different bleaching responses during the 2014-2015 event in Kāne’ohe Bay (O’ahu, Hawai’i) and exposed to four different artificial temperature pre-treatments (and a control at ambient temperature). After recovery, fragments experienced a natural thermal stress event either in laboratory conditions or their native reef environment. Response to thermal stress was quantified by measuring changes in the algal symbionts’ photochemical efficiency, community composition, and relative density. Historical bleaching phenotype was reflected in stable differences in symbiont community composition, with historically bleached corals containing only Cladocopium symbionts and historically non-bleached corals having mixed symbiont communities dominated by Durusdinium. Mixed-community corals lost more Cladocopium than Cladocopium-only corals during the natural thermal stress event, and preferentially recovered with Durusdinium. Laboratory pre-treatments exposed corals to more thermal stress than anticipated, causing photochemical damage that varied significantly by genotype. While none of the treatments had a protective effect, temperature variation during treatments had a significant detrimental effect on photochemical efficiency during the thermal stress event. These results show that acclimatization potential is affected by fine-scale differences in temperature regime, host genotype, and relatively stable differences in symbiont community composition that underpin historical bleaching phenotypes in M. capitata.

2021 ◽  
Author(s):  
Andrea N. Chan ◽  
Luis A. González-Guerrero ◽  
Roberto Iglesias-Prieto ◽  
Elizabeth M. Burmester ◽  
Randi D. Rotjan ◽  
...  

AbstractScleractinian corals form the foundation of coral reefs by secreting skeletons of calcium carbonate. Their intracellular algal symbionts (Symbiodiniaceae) translocate a large proportion of photosynthate to the coral host, which is required to maintain high rates of calcification. Global warming is causing dissociation of coral host and algal symbiont, visibly presented as coral bleaching. Despite decades of study, the precise mechanisms of coral bleaching remain unknown. Separating the thermal stress response of the coral from the algal symbiont is key to understanding bleaching in tropical corals. The facultatively symbiotic northern star coral, Astrangia poculata, naturally occurs as both symbiotic and aposymbiotic (lacking algal symbionts) polyps – sometimes on the same coral colony. Thus, it is possible to separate the heat stress response of the coral host alone from the coral in symbiosis with its symbiont Breviolum psygmophilum. Using replicate symbiotic and aposymbiotic ramets of A. poculata, we conducted a chronic heat stress experiment to increase our understanding of the cellular mechanisms resulting in coral bleaching. Sustained high temperature stress resulted in photosynthetic dysfunction in B. psygmophilum, including a decline in maximum photosynthesis rate, maximum photochemical efficiency, and the absorbance peak of chlorophyll a. Interestingly, the metabolic rates of symbiotic and aposymbiotic corals were differentially impacted. RNAseq analysis revealed more differentially expressed genes between heat-stressed and control aposymbiotic colonies than heat-stressed and control symbiotic colonies. Notably, aposymbiotic colonies increased the expression of inflammation-associated genes such as nitric oxide synthases. Unexpectedly, the largest transcriptional response was observed between heat-stressed and control B. psygmophilum, including genes involved in photosynthesis, response to oxidative stress, and meiosis. Thus, it appears that the algal symbiont suppresses the immune response of the host, potentially increasing the vulnerability of the host to pathogens. The A. poculata-B. psygmophilum symbiosis provides a tractable model system for investigating thermal stress and immune challenge in scleractinian corals.


PLoS ONE ◽  
2011 ◽  
Vol 6 (10) ◽  
pp. e26687 ◽  
Author(s):  
William Leggat ◽  
Francois Seneca ◽  
Kenneth Wasmund ◽  
Lubna Ukani ◽  
David Yellowlees ◽  
...  

2021 ◽  
Author(s):  
Ana M. Palacio-Castro ◽  
Caroline E. Dennison ◽  
Stephanie M. Rosales ◽  
Andrew C. Baker

Coral cover is declining worldwide due to multiple interacting threats. We compared the effects of elevated nutrients and temperature on three Caribbean corals: Acropora cervicornis, Orbicella faveolata, and Siderastrea siderea. Colonies hosting different algal types were exposed to either ambient nutrients (A), elevated NH4 (N), or elevated NH4 + PO4 (N+P) at control temperatures (26 °C) for > 2 months, followed by a 3-week thermal challenge (31.5 °C). A. cervicornis hosted Symbiodinium (S. fitti) and was highly susceptible to the combination of elevated nutrients and temperature. During heat stress, A. cervicornis pre-exposed to elevated nutrients experienced 84%-100% mortality and photochemical efficiency (Fv/Fm) declines of 41-50%. In comparison, no mortality and lower Fv/Fm declines (11-20%) occurred in A. cervicornis that were heat-stressed but not pre-exposed to nutrients. O. faveolata and S. siderea response to heat stress was determined by their algal symbiont community and was not affected by nutrients. O. faveolata predominantly hosted Durusdinium trenchii or Breviolum, but only corals hosting Breviolum were susceptible to heat, experiencing 100% mortality, regardless of nutrient treatment. S. siderea colonies predominantly hosted Cladocopium C1 (C. goreaui), Cladocopium C3, D. trenchii, or variable proportions of Cladocopium C1 and D. trenchii. This species was resilient to elevated nutrients and temperature, with no significant mortality in any of the treatments. However, during heat stress, S. siderea hosting Cladocopium C3 suffered higher reductions in Fv/Fm (41-56%) compared to S. siderea hosting Cladocopium C1 and D. trenchii (17-26% and 10-16%, respectively). These differences in holobiont susceptibility to elevated nutrients and heat may help explain historical declines in A. cervicornis starting decades earlier than other Caribbean corals. Our results suggest that tackling only warming temperatures may be insufficient to ensure the continued persistence of Caribbean corals, especially A. cervicornis. Reducing nutrient inputs to reefs may also be necessary for these iconic coral species to survive.


2019 ◽  
Author(s):  
SW Davies ◽  
K Moreland ◽  
DC Wham ◽  
MR Kanke ◽  
MV Matz

AbstractMany broadly-dispersing corals acquire their algal symbionts (Symbiodiniaceae) ‘horizontally’ from their environment upon recruitment. Horizontal transmission could promote coral fitness across diverse environments provided that corals can associate with divergent algae across their range and that these symbionts exhibit reduced dispersal potential. Here we quantified community divergence of Cladocopium algal symbionts in two coral host species (Acropora hyacinthus, Acropora digitifera) across two spatial scales (reefs on the same island, and between islands) across the Micronesian archipelago using microsatellites. We find that both hosts associated with two genetically distinct Cladocopium lineages (C40, C21), confirming that Acropora coral hosts associate with a range of Cladocopium symbionts across this region. Both C40 and C21 exhibited extensive clonality. Clones not only existed across host conspecifics living on the same reef, but also spanned host species, reef sites within islands, and even different islands. Both Cladocopium lineages exhibited moderate host specialization and divergence across islands. In addition, within every island, algal symbiont communities were significantly clustered by both host species and reef site, highlighting that coral-associated Cladocopium communities are structured across small spatial scales and within hosts on the same reef. This is in stark contrast to their coral hosts, which never exhibited significant genetic divergence between reefs on the same island. These results support the view that horizontal transmission could improve local fitness for broadly dispersing Acropora coral species.


2020 ◽  
Author(s):  
Amanda Williams ◽  
Eric N. Chiles ◽  
Dennis Conetta ◽  
Jananan S. Pathmanathan ◽  
Phillip A. Cleves ◽  
...  

SummaryCoral reef systems are under global threat due to warming and acidifying oceans1. Understanding the response of the coral holobiont to environmental change is crucial to aid conservation efforts. The most pressing problem is “coral bleaching”, usually precipitated by prolonged thermal stress that disrupts the algal symbiosis sustaining the holobiont2,3. We used metabolomics to understand how the coral holobiont metabolome responds to heat stress with the goal of identifying diagnostic markers prior to bleaching onset. We studied the heat tolerant Montipora capitata and heat sensitive Pocillopora acuta coral species from the Hawaiian reef system in Kāne’ohe Bay, O’ahu. Untargeted LC-MS analysis uncovered both known and novel metabolites that accumulate during heat stress. Among those showing the highest differential accumulation were a variety of co-regulated dipeptides present in both species. The structures of four of these compounds were determined (Arginine-Glutamine, Lysine-Glutamine, Arginine-Valine, and Arginine-Alanine). These dipeptides also showed differential accumulation in symbiotic and aposymbiotic (alga free) individuals of the sea anemone model Aiptasia4, suggesting their animal provenance and algal symbiont related function. Our results identify a suite of metabolites associated with thermal stress that can be used to diagnose coral health in wild samples.


2019 ◽  
Vol 99 (06) ◽  
pp. 1273-1279 ◽  
Author(s):  
Jeric P. Da-Anoy ◽  
Patrick C. Cabaitan ◽  
Cecilia Conaco

AbstractThermal stress events threaten coral populations by disrupting symbiosis between the coral animal and microalgal symbionts in its tissues. These symbionts are key players in the response of the coral holobiont to elevated temperature. However, little is known about the microalgal symbiont type in select corals in the north-western Philippines and how they contribute to the differential responses of coral species. Based on sequencing of major ITS2 bands from DGGE, the dominant algal symbiont inAcropora digitifera,A. millepora,A. tenuisandFavites colemaniwas identified to be closely related to ITS2 type C3u,Montipora digitatacontained ITS2 type C15, andSeriatopora caliendrumhosted ITS2 types similar to C3-Gulf and D1. Thin branching corals, such asA. tenuisandS. caliendrum, exhibited the greatest reduction in photochemical efficiency (Fv/Fm) and symbiont density at elevated temperature, followed byM. digitataandA. millepora, to a lesser extent.A. digitiferaandF. colemaniwere least affected by the temperature treatment. Reduction in Fv/Fm and symbiont density was more apparent inA. tenuisandA. milleporathan inM. digitataandF. colemani, although these species all host ITS2 type C3u symbionts. These results suggest that the impact of elevated temperature is influenced by factors apart from symbiont type. This highlights the importance of further studies on the diversity of corals and their microalgal symbionts in the region to gain insights into their potential resilience to recurring thermal stress events.


2021 ◽  
Author(s):  
Mariana Rocha de Souza ◽  
Carlo Caruso ◽  
Lupita Ruiz-Jones ◽  
Crawford Drury ◽  
Ruth D. Gates ◽  
...  

The survival of reef-building corals is dependent upon a symbiosis between the coral and the community of Symbiodiniaceae. Montipora capitata, one of the main reef building coral species in Hawaiʻi, is known to host a diversity of symbionts, but it remains unclear how they change spatially and whether environmental factors drive those changes. Here, we surveyed the Symbiodiniaceae community in 600 M. capitata colonies from 30 sites across Kāneʻohe Bay and tested for host specificity and environmental gradients driving spatial patterns of algal symbiont distribution. We found that the Symbiodiniaceae community differed markedly across sites, with M. capitata in the most open-ocean (northern) site hosting few or none of the genus Durusdinium, whereas individuals at other sites had a mix of Durusdinium and Cladocopium. Our study shows that the algal symbiont community composition responds to fine-scale differences in environmental gradients; depth and temperature variability were the most significant predictor of Symbiodiniaceae community, although environmental factors measured in the study explained only about 20% of observed variation. Identifying and mapping Symbiodiniaceae community distribution at multiple scales is an important step in advancing our understanding of algal symbiont diversity, distribution and evolution, and the potential responses of corals to future environmental change.


PeerJ ◽  
2021 ◽  
Vol 9 ◽  
pp. e12335
Author(s):  
Amanda Williams ◽  
Jananan S. Pathmanathan ◽  
Timothy G. Stephens ◽  
Xiaoyang Su ◽  
Eric N. Chiles ◽  
...  

Background Corals, which form the foundation of biodiverse reef ecosystems, are under threat from warming oceans. Reefs provide essential ecological services, including food, income from tourism, nutrient cycling, waste removal, and the absorption of wave energy to mitigate erosion. Here, we studied the coral thermal stress response using network methods to analyze transcriptomic and polar metabolomic data generated from the Hawaiian rice coral Montipora capitata. Coral nubbins were exposed to ambient or thermal stress conditions over a 5-week period, coinciding with a mass spawning event of this species. The major goal of our study was to expand the inventory of thermal stress-related genes and metabolites present in M. capitata and to study gene-metabolite interactions. These interactions provide the foundation for functional or genetic analysis of key coral genes as well as provide potentially diagnostic markers of pre-bleaching stress. A secondary goal of our study was to analyze the accumulation of sex hormones prior to and during mass spawning to understand how thermal stress may impact reproductive success in M. capitata. Methods M. capitata was exposed to thermal stress during its spawning cycle over the course of 5 weeks, during which time transcriptomic and polar metabolomic data were collected. We analyzed these data streams individually, and then integrated both data sets using MAGI (Metabolite Annotation and Gene Integration) to investigate molecular transitions and biochemical reactions. Results Our results reveal the complexity of the thermal stress phenome in M. capitata, which includes many genes involved in redox regulation, biomineralization, and reproduction. The size and number of modules in the gene co-expression networks expanded from the initial stress response to the onset of bleaching. The later stages involved the suppression of metabolite transport by the coral host, including a variety of sodium-coupled transporters and a putative ammonium transporter, possibly as a response to reduction in algal productivity. The gene-metabolite integration data suggest that thermal treatment results in the activation of animal redox stress pathways involved in quenching molecular oxygen to prevent an overabundance of reactive oxygen species. Lastly, evidence that thermal stress affects reproductive activity was provided by the downregulation of CYP-like genes and the irregular production of sex hormones during the mass spawning cycle. Overall, redox regulation and metabolite transport are key components of the coral animal thermal stress phenome. Mass spawning was highly attenuated under thermal stress, suggesting that global climate change may negatively impact reproductive behavior in this species.


Forests ◽  
2020 ◽  
Vol 11 (3) ◽  
pp. 262 ◽  
Author(s):  
Leszek Karliński ◽  
Sabine Ravnskov ◽  
Maria Rudawska

Poplars, known for their diversity, are trees that can develop symbiotic relationships with several groups of microorganisms. The genetic diversity of poplars and different abiotic factors influence the properties of the soil and may shape microbial communities. Our study aimed to analyse the impact of poplar genotype on the biomass and community composition of the microbiome of four poplar genotypes grown under different soil conditions and soil depths. Of the three study sites, established in the mid-1990s, one was near a copper smelter, whereas the two others were situated in unpolluted regions, but were differentiated according to the physicochemical traits of the soil. The whole-cell fatty acid analysis was used to determine the biomass and proportions of gram-positive, gram-negative and actinobacteria, arbuscular fungi (AMF), other soil fungi, and protozoa in the whole microbial community in the soil. The results showed that the biomass of microorganisms and their contributions to the community of organisms in the soil close to poplar roots were determined by both factors: the tree-host genotype and the soil environment. However, each group of microorganisms was influenced by these factors to a different degree. In general, the site effect played the main role in shaping the microbial biomass (excluding actinobacteria), whereas tree genotype determined the proportions of the fungal and bacterial groups in the microbial communities and the proportion of AMF in the fungal community. Bacterial biomass was influenced more by site factors, whereas fungal biomass more by tree genotype. With increasing soil depth, a decrease in the biomass of all microorganisms was observed; however, the proportions of the different microorganisms within the soil profile were the result of interactions between the host genotype and soil conditions. Despite the predominant impact of soil conditions, our results showed the important role of poplar genotype in shaping microorganism communities in the soil.


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