skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Characterization of a sperm motility signalling pathway in a gonochoric coral suggests conservation across cnidarian sexual systems
Most stony corals liberate their gametes into the water column via broadcast spawning, where fertilization hinges upon the activation of directional sperm motility. Sperm from gonochoric and hermaphroditic corals display distinct morphological and molecular phenotypes, yet it is unknown whether the signalling pathways controlling sperm motility are also distinct between these sexual systems. Here, we addressed this knowledge gap using the gonochoric, broadcast spawning coralAstrangia poculata. We found that cytosolic alkalinization of sperm activates the pH-sensing enzyme soluble adenylyl cyclase (sAC), which is required for motility. Additionally, we demonstrate for the first time in any cnidarian that sAC activity leads to protein kinase A (PKA) activation, and that PKA activity contributes to sperm motility activation. Ultrastructures ofA. poculatasperm displayed morphological homology with other gonochoric cnidarians, and sAC exhibited broad structural and functional conservation across this phylum. These results indicate a conserved role for pH-dependent sAC-cAMP-PKA signalling in sperm motility across coral sexual systems, and suggest that the role of this pathway in sperm motility may be ancestral in metazoans. Finally, the dynamics of this pH-sensitive pathway may play a critical role in determining the sensitivity of marine invertebrate reproduction to anthropogenic ocean acidification.  more » « less
Award ID(s):
1923743
PAR ID:
10467266
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
The Royal Society Publishing
Date Published:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Volume:
290
Issue:
2004
ISSN:
0962-8452
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Background. Reproductive biology and the evolutionary constraints acting on dispersal stages are poorly understood in many stony coral species. A key piece of missing information is egg and sperm gene expression. This is critical for broadcast spawning corals, such as our model, the Hawaiian species Montipora capitata, because eggs and sperm are exposed to environmental stressors during dispersal. Furthermore, parental effects such as transcriptome investment may provide a means for cross- or transgenerational plasticity and be apparent in egg and sperm transcriptome data. Methods. Here, we analyzed M. capitata egg and sperm transcriptomic data to address three questions: (1) Which pathways and functions are actively transcribed in these gametes? (2) How does sperm and egg gene expression differ from adult tissues? (3) Does gene expression differ between these gametes? Results. We show that egg and sperm display surprisingly similar levels of gene expression and overlapping functional enrichment patterns. These results may reflect similar environmental constraints faced by these motile gametes. We find significant differences in differential expression of egg vs. adult and sperm vs. adult RNA-seq data, in contrast to very few examples of differential expression when comparing egg vs. sperm transcriptomes. Lastly, using gene ontology and KEGG orthology data we show that both egg and sperm have markedly repressed transcription and translation machinery compared to the adult, suggesting a dependence on parental transcripts. We speculate that cell motility and calcium ion binding genes may be involved in gamete to gamete recognition in the water column and thus, fertilization. 
    more » « less
  2. Fujimura, Atsushi (Ed.)
    Identifying processes that promote coral reef recovery and resilience is crucial as ocean warming becomes more frequent and severe. Sexual reproduction is essential for the replenishment of coral populations and maintenance of genetic diversity; however, the ability for corals to reproduce may be impaired by marine heatwaves that cause coral bleaching. In 2014 and 2015, the Hawaiian Islands experienced coral bleaching with differential bleaching susceptibility in the speciesMontipora capitata, a dominant reef-building coral in the region. We tested the hypothesis that coral bleaching resistance enhances reproductive capacity and offspring performance by examining the reproductive biology of colonies that bleached and recovered (B) and colonies that did not bleach (NB) in 2015 in the subsequent spawning seasons. The proportion of colonies that spawned was higher in 2016 than in 2017. Regardless of parental bleaching history, we found eggs with higher abnormality and bundles with fewer eggs in 2016 than 2017. While reproductive output was similar between B and NB colonies in 2016, survivorship of offspring that year were significantly influenced by the parental bleaching history (egg donor × sperm donor: B × B, B × NB, NB × B, and NB × NB). Offspring produced by NB egg donors had the highest survivorship, while offspring from previously bleached colonies had the lowest survivorship, highlighting the negative effects of bleaching on parental investment and offspring performance. While sexual reproduction continues inM.capitatapost-bleaching, gametes are differentially impacted by recovery time following a bleaching event and by parental bleaching resistance. Our results demonstrate the importance of identifying bleaching resistant individuals during and after heating events. This study further highlights the significance of maternal effects through potential egg provisioning for offspring survivorship and provides a baseline for human-assisted intervention (i.e., selective breeding) to mitigate the effects of climate change on coral reefs. 
    more » « less
  3. Escriva, Hector (Ed.)
    In an era of climate change, impacts on the marine environment include warming and ocean acidification. These effects can be amplified in shallow coastal regions where conditions often fluctuate widely. This type of environmental variation is potentially important for many nearshore species that are broadcast spawners, releasing eggs and sperm into the water column for fertilization. We conducted two experiments to investigate: 1) the impact of water temperature on sperm swimming characteristics and fertilization rate in sand dollars (Dendraster excentricus; temperatures 8-38°C) and sea urchins (Mesocentrotus franciscanus; temperatures 8-28°C) and; 2) the combined effects of multiple stressors (water temperature and pH) on these traits in sand dollars. We quantify thermal performance curves showing that sand dollar fertilization rates, sperm swimming velocities, and sperm motility display remarkably wide thermal breadths relative to red urchins, perhaps reflecting the wider range of water temperatures experienced by sand dollars at our field sites. For sand dollars, both temperature (8, 16, 24°C) and pH (7.1, 7.5, 7.9) affected fertilization but only temperature influenced sperm swimming velocity and motility. Although sperm velocities and fertilization were positively correlated, our fertilization kinetics model dramatically overestimated measured rates and this discrepancy was most pronounced under extreme temperature and pH conditions. Our results suggest that environmental stressors like temperature and pH likely impair aspects of the reproductive process beyond simple sperm swimming behavior. 
    more » « less
  4. null (Ed.)
    Species-specific sperm−egg interactions are essential for sexual reproduction. Broadcast spawning of marine organisms is under particularly stringent conditions, since eggs released into the water column can be exposed to multiple different sperm. Bindin isolated from the sperm acrosome results in insoluble particles that cause homospecific eggs to aggregate, whereas no aggregation occurs with heterospecific eggs. Therefore, Bindin is concluded to play a critical role in fertilization, yet its function has never been tested. Here we report that Cas9-mediated inactivation of the bindin gene in a sea urchin results in perfectly normal-looking embryos, larvae, adults, and gametes in both males and females. What differed between the genotypes was that the bindin −/− sperm never fertilized an egg, functionally validating Bindin as an essential gamete interaction protein at the level of sperm–egg cell surface binding. 
    more » « less
  5. Laruelle, Goulven G (Ed.)
    Coral reefs are facing threats from a variety of global change stressors, including ocean warming, acidification, and deoxygenation. It has been hypothesized that growing corals near primary producers such as macroalgae or seagrass may help to ameliorate acidification and deoxygenation stress, however few studies have explored this effect in situ. Here, we investigated differences in coral growth rates across a natural gradient in seawater temperature, pH, and dissolved oxygen (DO) variability in a nearshore seagrass bed on Dongsha Atoll, Taiwan, South China Sea. We observed strong spatial gradients in temperature (5°C), pH (0.29 pH units), and DO (129 μmol O2kg-1) across the 1-kilometer wide seagrass bed. Similarly, diel variability recorded by an autonomous sensor in the shallow seagrass measured diel ranges in temperature, pH, and DO of up to 2.6°C, 0.55, and 204 μmol O2kg-1, respectively. Skeletal cores collected from 15 massivePoritescorals growing in the seagrass bed at 4 sites revealed no significant differences in coral calcification rates between sites along the gradients. However, significant differences in skeletal extension rate and density suggest that the dynamic temperature, pH, and/or DO variability may have influenced these properties. The lack of differences in coral growth between sites may be because favorable calcification conditions during the day (high temperature, pH, and DO) were proportionally balanced by unfavorable conditions during the night (low temperature, pH, and DO). Alternatively, other factors were simply more important in controlling coral calcification and/or corals were acclimated to the prevailing conditions at each site. 
    more » « less