Global Shifts in Gene Expression Profiles Accompanied with Environmental Changes in Cnidarian-Dinoflagellate Endosymbiosis

Reef-building corals are keystone species that are threatened by anthropogenic stresses including climate change. To investigate corals’ responses to stress and other aspects of their biology, numerous genomic and transcriptomic studies have been performed, generating many hypotheses about the roles of particular genes and molecular pathways. However, it has not generally been possible to test these hypotheses rigorously because of the lack of genetic tools for corals or closely related cnidarians. CRISPR technology seems likely to alleviate this problem. Indeed, we show here that microinjection of single-guide RNA/Cas9 ribonucleoprotein complexes into fertilized eggs of the coralAcropora milleporacan produce a sufficiently high frequency of mutations to detect a clear phenotype in the injected generation. Based in part on experiments in a sea-anemone model system, we targeted the gene encoding Heat Shock Transcription Factor 1 (HSF1) and obtained larvae in which >90% of the gene copies were mutant. The mutant larvae survived well at 27 °C but died rapidly at 34 °C, a temperature that did not produce detectable mortality over the duration of the experiment in wild-type (WT) larvae or larvae injected with Cas9 alone. We conclude that HSF1 function (presumably its induction of genes in response to heat stress) plays an important protective role in corals. More broadly, we conclude that CRISPR mutagenesis in corals should allow wide-ranging and rigorous tests of gene function in both larval and adult corals.

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Reduced thermal tolerance in a coral carrying CRISPR-induced mutations in the gene for a heat-shock transcription factor

Cleves

Tinoco

Bradford

et al. 2020

“…However, that study only examined gene expression during the first few hours of heat stress, so that the full dynamics of the NFκB response remained unclear. Moreover, another study that examined early time points did not note changes in NFκB mRNA levels (19), whereas of two studies that examined a later time point (∼24 h of heat stress), one reported elevated levels of NFκB mRNA (26) while the other did not (27). A sustained elevation of NFκB mRNA during heatinduced bleaching would be consistent with the evidence that NFκB protein is present at lower levels in symbiotic than in aposymbiotic animals, which may be necessary to avoid innateimmune rejection of the foreign cells (28).…”

Section: Significancementioning

confidence: 96%

Insights into coral bleaching under heat stress from analysis of gene expression in a sea anemone model system

Cleves

Krediet

Lehnert

et al. 2020

Loss of endosymbiotic algae (“bleaching”) under heat stress has become a major problem for reef-building corals worldwide. To identify genes that might be involved in triggering or executing bleaching, or in protecting corals from it, we used RNAseq to analyze gene-expression changes during heat stress in a coral relative, the sea anemone Aiptasia. We identified >500 genes that showed rapid and extensive up-regulation upon temperature increase. These genes fell into two clusters. In both clusters, most genes showed similar expression patterns in symbiotic and aposymbiotic anemones, suggesting that this early stress response is largely independent of the symbiosis. Cluster I was highly enriched for genes involved in innate immunity and apoptosis, and most transcript levels returned to baseline many hours before bleaching was first detected, raising doubts about their possible roles in this process. Cluster II was highly enriched for genes involved in protein folding, and most transcript levels returned more slowly to baseline, so that roles in either promoting or preventing bleaching seem plausible. Many of the genes in clusters I and II appear to be targets of the transcription factors NFκB and HSF1, respectively. We also examined the behavior of 337 genes whose much higher levels of expression in symbiotic than aposymbiotic anemones in the absence of stress suggest that they are important for the symbiosis. Unexpectedly, in many cases, these expression levels declined precipitously long before bleaching itself was evident, suggesting that loss of expression of symbiosis-supporting genes may be involved in triggering bleaching.

“…A July 2019 study found that 292 cnidarian genes in transcriptome analysis of the symbiotic sea anemone Exaiptasia diaphana, a close relative and emerging model organism of corals, changed their expression levels at bleaching-threshold temperatures (12). Some of the most affected genes are involved in metabolizing sugars, which the algae normally provide to the coral.…”

Section: Forward Thinkingmentioning

confidence: 99%

A microscopic mystery at the heart of mass-coral bleaching

McDermott¹

2020

In the summer of 2017, a small plane hummed over Australia's Great Barrier Reef. Corals far below gleamed pale white in the sunlight, a stark contrast to the cerulean sea. The scene might have been gorgeous, if it wasn't so bleak. Aerial surveys by the Australian Research Council Centre of Excellence for Coral Reef Studies in Townsville, Australia, revealed that two-thirds of the Great Barrier Reef had severely paled in 2016 and 2017, "bleaching" under the extreme stress of marine heat waves that can kill corals (1, 2). Summer 2017 marked the finale of the worst mass-bleaching event on record worldwide, three consecutive years of feverish ocean temperatures, driven by climate change, which affected more than 75% of reefs (3, 4). Newspaper headlines frequently reference bleaching events. It's no secret that reefs are in trouble. But for all the attention to bleaching, researchers are still puzzling over the cellular mechanisms that cause it. What's clear is that bleaching is the breakup of the tenuous relationship between a coral and the photosynthetic algae that live inside its cells. Heat stress can disrupt this relationship, causing the coral to expel its algae and to pale. New research suggests that algae, too, can be disruptive, turning on their hosts at high temperatures by switching from symbionts to parasites, which may also lead to bleaching. Coral algae have a reputation "as this friendly, only do-good kind of hero," because they provision the coral with nutrients, says reef ecologist David Baker at the University of Hong Kong. "And I think that's a misguided sentiment." New efforts in genomics are helping to further explicate the basic biology of bleaching. In 2018, researchers even used CRISPR/Cas9 to edit coral At least two-thirds of the Great Barrier Reef has been bleached under the extreme stress of marine heat waves. Image credit: The Ocean Agency/XL Catlin Seaview Survey.