Responses of coral-associated bacterial communities to heat stress differ withSymbiodiniumtype on the same coral host

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.

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Heat stress destabilizes symbiotic nutrient cycling in corals

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2022653118 ◽

2021 ◽

Vol 118 (5) ◽

pp. e2022653118 ◽

Cited By ~ 3

Author(s):

Nils Rädecker ◽

Claudia Pogoreutz ◽

Hagen M. Gegner ◽

Anny Cárdenas ◽

Florian Roth ◽

...

Keyword(s):

Heat Stress ◽

Nutrient Cycling ◽

Energy Demand ◽

Metabolic Energy ◽

Environmental Drivers ◽

Coral Host ◽

Stylophora Pistillata ◽

Coral Holobiont ◽

Algal Symbiosis ◽

Energy Limitation

Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral–algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral–algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral–algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.

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Thirty years of coral heat-stress experiments: a review of methods

Coral Reefs ◽

10.1007/s00338-020-01931-9 ◽

2020 ◽

Vol 39 (4) ◽

pp. 885-902 ◽

Cited By ~ 8

Author(s):

Rowan H. McLachlan ◽

James T. Price ◽

Sarah L. Solomon ◽

Andréa G. Grottoli

Keyword(s):

Heat Stress ◽

Experimental Design ◽

Coral Bleaching ◽

Best Practice ◽

Global Climate ◽

Coral Host ◽

Flow Conditions ◽

Experimental Conditions ◽

Large Variability ◽

Acclimation Period

AbstractFor over three decades, scientists have conducted heat-stress experiments to predict how coral will respond to ocean warming due to global climate change. However, there are often conflicting results in the literature that are difficult to resolve, which we hypothesize are a result of unintended biases, variation in experimental design, and underreporting of critical methodological information. Here, we reviewed 255 coral heat-stress experiments to (1) document where and when they were conducted and on which species, (2) assess variability in experimental design, and (3) quantify the diversity of response variables measured. First, we found that two-thirds of studies were conducted in only three countries, three coral species were more heavily studied than others, and only 4% of studies focused on earlier life stages. Second, slightly more than half of all heat-stress exposures were less than 8 d in duration, only 17% of experiments fed corals, and experimental conditions varied widely, including the level and rate of temperature increase, light intensity, number of genets used, and the length of acclimation period. In addition, 95%, 55%, and > 35% of studies did not report tank flow conditions, light–dark cycle used, or the date of the experiment, respectively. Finally, we found that 21% of experiments did not measure any bleaching phenotype traits, 77% did not identify the Symbiodiniaceae endosymbiont, and the contribution of the coral host in the physiological response to heat-stress was often not investigated. This review highlights geographic, taxonomic, and heat-stress duration biases in our understanding of coral bleaching, and large variability in the reporting and design of heat-stress experiments that could account for some of the discrepancies in the literature. Development of some best practice recommendations for coral bleaching experiments could improve cross-studies comparisons and increase the efficiency of coral bleaching research at a time when it is needed most.

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Effect of chronic cyclic heat stress on the intestinal morphology, oxidative status and cecal bacterial communities in broilers

Journal of Thermal Biology ◽

10.1016/j.jtherbio.2020.102619 ◽

2020 ◽

Vol 91 ◽

pp. 102619

Author(s):

Guanhui Liu ◽

Haibo Zhu ◽

Tenghe Ma ◽

Zhaoyang Yan ◽

Yongying Zhang ◽

...

Keyword(s):

Heat Stress ◽

Bacterial Communities ◽

Oxidative Status ◽

Intestinal Morphology ◽

Cyclic Heat

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Characterization of Geographically Distinct Bacterial Communities Associated with Coral Mucus Produced by Acropora spp. and Porites spp.

Applied and Environmental Microbiology ◽

10.1128/aem.07764-11 ◽

2012 ◽

Vol 78 (15) ◽

pp. 5229-5237 ◽

Cited By ~ 41

Author(s):

B. A. McKew ◽

A. J. Dumbrell ◽

S. D. Daud ◽

L. Hepburn ◽

E. Thorpe ◽

...

Keyword(s):

Relative Abundance ◽

Bacterial Communities ◽

Coral Host ◽

Coral Mucus ◽

Content Type ◽

First Report ◽

Mexican Caribbean ◽

The Caribbean

ABSTRACTAcroporaandPoritescorals are important reef builders in the Indo-Pacific and Caribbean. Bacteria associated with mucus produced byPoritesspp. andAcroporaspp. from Caribbean (Punta Maroma, Mexico) and Indo-Pacific (Hoga and Sampela, Indonesia) reefs were determined. Analysis of pyrosequencing libraries showed that bacterial communities from Caribbean corals were significantly more diverse (H′, 3.18 to 4.25) than their Indonesian counterparts (H′, 2.54 to 3.25). Dominant taxa wereGammaproteobacteria,Alphaproteobacteria,Firmicutes, andCyanobacteria, which varied in relative abundance between coral genera and region. Distinct coral host-specific communities were also found; for example,Clostridialeswere dominant onAcroporaspp. (at Hoga and the Mexican Caribbean) compared toPoritesspp. and seawater. Within theGammproteobacteria,Halomonasspp. dominated sequence libraries fromPoritesspp. (49%) andAcroporaspp. (5.6%) from the Mexican Caribbean, compared to the corresponding Indonesian coral libraries (<2%). Interestingly, with the exception ofPoritesspp. from the Mexican Caribbean, there was also a ubiquity ofPsychrobacterspp., which dominatedAcroporaandPoriteslibraries from Indonesia andAcroporalibraries from the Caribbean. In conclusion, there was a dominance ofHalomonasspp. (associated withAcroporaandPorites[Mexican Caribbean]),Firmicutes(associated withAcropora[Mexican Caribbean] and withAcroporaandPorites[Hoga]), andCyanobacteria(associated withAcroporaandPorites[Hoga] andPorites[Sampela]). This is also the first report describing geographically distinctPsychrobacterspp. associated with coral mucus. In addition, the predominance ofClostridialesassociated withAcroporaspp. provided additional evidence for coral host-specific microorganisms.

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The Effect of a Sublethal Temperature Elevation on the Structure of Bacterial Communities Associated with the CoralPorites compressa

Journal of Marine Biology ◽

10.1155/2011/969173 ◽

2011 ◽

Vol 2011 ◽

pp. 1-9 ◽

Cited By ~ 6

Author(s):

Jennifer L. Salerno ◽

Dan R. Reineman ◽

Ruth D. Gates ◽

Michael S. Rappé

Keyword(s):

Community Structure ◽

Bacterial Community ◽

Bacterial Communities ◽

Bacterial Community Structure ◽

16S Rrna Genes ◽

Rrna Genes ◽

Polymorphism Analysis ◽

Significant Shift ◽

Coral Host ◽

Experimental Conditions

Evidence points to a link between environmental stressors, coral-associated bacteria, and coral disease; however, few studies have examined the details of this relationship under tightly controlled experimental conditions. To address this gap, an array of closed-system, precision-controlled experimental aquaria were used to investigate the effects of an abrupt 1°C above summer ambient temperature increase on the bacterial community structure and photophysiology ofPorites compressacorals. While the temperature treatment rapidly impacted the photophysiology of the coral host, it did not elicit a statistically significant shift in bacterial community structure from control, untreated corals as determined by terminal restriction fragment length polymorphism analysis of 16S rRNA genes. Two of three coral colonies harbored more closely related bacterial communities at the time of collection and, despite statistically significant shifts in bacterial community structure for both control and treatment corals during the 10-day acclimation period, maintained this relationship over the course of the experiment. The experimental design used in this study proved to be a robust, reproducible system for investigating coral microbiology in an aquarium setting.

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Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality

Science Advances ◽

10.1126/sciadv.abg3088 ◽

2021 ◽

Vol 7 (33) ◽

pp. eabg3088

Author(s):

Erika P. Santoro ◽

Ricardo M. Borges ◽

Josh L. Espinoza ◽

Marcelo Freire ◽

Camila S. M. A. Messias ◽

...

Keyword(s):

Heat Stress ◽

Photosynthetic Performance ◽

Coral Host ◽

Immune Genes ◽

Transcriptional Reprogramming ◽

Coral Microbiome ◽

Stress Protection ◽

Restructuring Process ◽

Endosymbiotic Algae

Beneficial microorganisms for corals (BMCs) ameliorate environmental stress, but whether they can prevent mortality and the underlying host response mechanisms remains elusive. Here, we conducted omics analyses on the coral Mussismilia hispida exposed to bleaching conditions in a long-term mesocosm experiment and inoculated with a selected BMC consortium or a saline solution placebo. All corals were affected by heat stress, but the observed “post-heat stress disorder” was mitigated by BMCs, signified by patterns of dimethylsulfoniopropionate degradation, lipid maintenance, and coral host transcriptional reprogramming of cellular restructuration, repair, stress protection, and immune genes, concomitant with a 40% survival rate increase and stable photosynthetic performance by the endosymbiotic algae. This study provides insights into the responses that underlie probiotic host manipulation. We demonstrate that BMCs trigger a dynamic microbiome restructuring process that instigates genetic and metabolic alterations in the coral host that eventually mitigate coral bleaching and mortality.

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Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial Microbiome

Frontiers in Marine Science ◽

10.3389/fmars.2020.573635 ◽

2020 ◽

Vol 7 ◽

Author(s):

Janna L. Randle ◽

Anny Cárdenas ◽

Hagen M. Gegner ◽

Maren Ziegler ◽

Christian R. Voolstra

Keyword(s):

Heat Stress ◽

Bacterial Community ◽

Community Composition ◽

Bacterial Communities ◽

Thermal Tolerance ◽

High Salinity ◽

Bacterial Community Composition ◽

Algal Symbiont ◽

Bacterial Microbiome ◽

Reef Decline

Coral bleaching, i.e., the loss of photosynthetic algal endosymbionts, caused by ocean warming is now among the main factors driving global reef decline, making the elucidation of factors that contribute to thermotolerance important. Recent studies implicate high salinity as a contributing factor in cnidarians, potentially explaining the high thermotolerance of corals from the Arabian Seas. Here we characterized bacterial community composition under heat stress at different salinities using the coral model Aiptasia. Exposure of two Aiptasia host-algal symbiont pairings (H2-SSB01 and CC7-SSA01) to ambient (25°C) and heat stress (34°C) temperatures at low (36 PSU), intermediate (39 PSU), and high (42 PSU) salinities showed that bacterial community composition at high salinity was significantly different, concomitant with reduced bleaching susceptibility in H2-SSB01, not observed in CC7-SSA01. Elucidation of bacteria that showed increased relative abundance at high salinity, irrespective of heat stress, revealed candidate taxa that could potentially contribute to the observed increased thermotolerance. We identified 4 (H2-SSB01) and 3 (CC7-SSA01) bacterial taxa belonging to the orders Alteromonadales (1 OTU), Oligoflexales (1 OTU), Rhizobiales (2 OTUs), and Rhodobacterales (2 OTUs), suggesting that only few bacterial taxa are potential contributors to an increase in thermal tolerance at high salinities. These taxa have previously been implicated in nitrogen and DMSP cycling, processes that are considered to affect thermotolerance. Our study demonstrates microbiome restructuring in symbiotic cnidarians under heat stress at different salinities. As such, it underlines how host-associated bacterial communities adapt to prevailing environmental conditions with putative consequences for the environmental stress tolerance of the emergent metaorganism.

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Response of Endozoicomonas montiporae to heat stress and coral host lysates

10.1101/2021.09.27.461970 ◽

2021 ◽

Author(s):

YaFan Chan ◽

Chia-Yu Chen ◽

Chih-Ying Lu ◽

Yung-Chi Tu ◽

Kshitij Tandon ◽

...

Keyword(s):

Heat Stress ◽

Antioxidant Defense ◽

Molecular Mechanisms ◽

Proteome Analysis ◽

Differentially Expressed ◽

Coral Host ◽

Defense Proteins ◽

Depth Analysis ◽

Pyruvate Synthase ◽

Shock Proteins

Endozoicomonas, a core bacterial group in corals, may also be a coral symbiont. Endozoicomonas communities often decrease rapidly in corals under heat stress. However, how the bacteria respond to changes in temperature and coral host during heat stress is unknown. Here, we employed the cultivable, dominant species E. montiporae as a working organism to explore how Endozoicomonas responds to heat stress. We designed two experiments to clarify the extent to which E. montiporae is influenced by temperature and coral host. We detected differentially expressed protein (DEP) profiles in this bacterium at 31°C and 33°C compared to 25°C by tandem mass tags-based quantitative proteome analysis. Fifty DEPs, including many heat shock proteins, were detected when the temperature changed. The expression of antioxidant defense proteins and key pyruvate synthase proteins decreased, suggesting that E. montiporae were in a physiology of stress at 33°C. Furthermore, some proteins were differentially expressed because of the heat-stress-treated coral lysate specifically, suggesting that not only heat but also heat-induced host factors can affect the protein expression of the bacterium. This study provides an in-depth analysis of how the molecular mechanisms of Endozoicomonas are affected by heat stress and coral host.

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