Lingulodinium polyedra
1. Classification
Higher order taxa
Eukaryota; Sar; Alveolata; Dinophyceae; Gonyaulacales; Lingulodiniaceae; Lingulodinium[14]
Species
‘‘Lingulodinium polyedra’‘
2. Description and significance
Lingulodinium polyedra is a motile, marine dinoflagellate protozoan most commonly found in temperate ocean waters; although it has expanded beyond its predicted range in recent years. It is most well known for being a perpetrator of the phenomenon known as red tides worldwide and can produce large amounts of harmful yessotoxin when observed in high concentrations [10]. Red tides can be driven by human activity such as deep ocean trawling or naturally through spring currents. The yessotoxin is capable of causing diarrhetic shellfish poisoning and can affect oceanic zooplankton diversity. [2]. The accumulation of toxins in lower trophic levels can concentrate the effect of yessotoxin in vertebrates, causing more acute symptoms. L. polyedra can bioluminescence a blue-green light when perturbed, either by the force of ocean currents or directly colliding with other organisms or objects. Its bioluminescence is correlated with its internal circadian rhythm, peaking at night, which is controlled by molecular clocks, providing insight into research on how circadian rhythms may be controlled in higher eukaryotes [6][13]. Lingulodinium polyedra can form a phytoplanktonic, dormant cyst when in unfavorable conditions, which rely on both the nitrate and temperature variation of its environment [5]. The effects of nitrates, specifically due to agricultural runoff, can induce dormant cyst formation and cause swathes of dinoflagellates to accumulate in coastal sediment [11]. When in the cyst stage, they can remain buried in anoxic sediment until external conditions are favorable for growth again, causing algal blooms [11]. Understanding L.polyedra and its role in the environment allows people to predict the interactions human agricultural and economic activity can have on ocean ecology, and thus reduce the risks that come with increasing frequencies of red tides in an ever-changing marine ecosystem.
3. Genome structure
The genome size of Lingulodinium polyedrum has reportedly been sequenced [7]: is 191.7 Mb and has a 57% G-C content, but has not been described further.
- Lingulodinium polyedra’s transcriptome has been sequenced using expressed sequence tags (ESTS) [1]. Within the profiled sequences, 93-94% of the transcriptome was present [1]. The gene catalog transcribes 64% of the same proteins found in mammals. It did not contain the transcription factor IID subunit TATA-binding protein (TBP), but instead, has a similar binding protein with a different specificity [1]. The TBP protein is involved in the binding of DNA and initiating transcription by RNA polymerase [15]. L. polyedra DNA binding domains are mostly cold-shock, as they lack the heat-shock factor domains. There is an underrepresentation of these proteins in L. polyedra, indicating that dinoflagellates regulate gene expression through post-transcriptional mechanisms [1]. It is hypothesized that this regulatory preference plays a role in L. polyedra’s ability to control translation and its circadian protein synthesis.
4. Cell structure
The cell of Lingulodinium polyedra is 42-54 μm in size with a cell surface area of 3180 μm2 and has an angular, sphere-like shape with a deep ridge going diagonally through the middle, with well-defined pores in its cellulose shell plate [9]. The cells are polyhedral, and they lack any textured protrusions, such as spines and horns [8]. It also contains chloroplasts and forms cysts that can be easily identified under a microscope [8]. The dormant cyst is a slightly smaller (31-54 μm) diameter, with a fully spherical shape that has protruding spines [9]. Inside the L. Polyedra cell, there are scintillons (organelles functioning as vesicles that have the luciferin protein, including a luciferin substrate and the luciferase enzyme)[16]. These incredibly small structures, about 0.5-0.9μm usually, are the organelles that are activated in dark environments and reflect light in response to a stressor, primarily to fend off predators [16].
5. Metabolic processes
Lingulodinium polyedra is a mixotrophic eukaryote [3]. It contains different pigments, such as chlorophyll a and c, as well as carotenoids [5]. L. polyedra has mechanisms to help survive changes in nitrogen and phosphorus availability, including producing yessotoxins (harmful toxin), which can protect it from being eaten [10], allowing it to outcompete other phytoplankton [2]. In addition, Lingulodinium polyedra can collect starch and lipids for energy [3]. L. polyedra typically regulates gene expression post-transcriptionally [1]. It can survive different environmental changes, specifically in nitrite concentrations and temperature [4]. Additionally, L. Polyedra undergoes an intricate pathway to produce bioluminescence, which is a pH-dependent reaction [16]. This happens through the activation of scintillas by a stressor in the environment acting on the cell membrane, which then produces an action potential in the membrane of the scintillas that causes an increase in Ca2+ concentrations in the cytosol [16]. This ultimately reduces the pH of the vacuole whose membrane generated the action potential from roughly 8 to 6. G-protein coupled receptors in the membrane of the cell are involved, but there is little research on which during this process they are activated and used [16]. The activation of this pathway is also used as a method of avoiding predators and is unique to L. polyedra among the dinoflagellate species that produce bioluminescence [12].
6. Ecology
Lingulodinium polyedra is a marine dinoflagellate that inhabits warm subtropical coastal areas and estuarine systems. It flourishes in nutrient-rich waters and is linked with harmful algal blooms [2]. The species is widely distributed and dispersed globally in coastal waters, including in regions such as southern Benguela in Africa, and Galician Rias in Northwestern Iberian Peninsula. The optimal growth conditions include moderate or high salinity levels [11]. It can adapt to a range of temperatures but is known to proliferate in warm water during the summer which leads to the formation of red tide events [11]. Its ability to produce biotoxins has ecological impacts during bloom events. Some examples include its biotoxins (yessotoxins) that deter grazing by zooplankton and other predators conferring L. polyedra a competitive advantage against other dinoflagellates [2].
7. Pathology
Lingulodinium polyedra has not been reported as a pathogen of humans, animals, or plants. Nonetheless, it can indirectly bring harm to animals and humans with its ability to produce biotoxins (yessotoxins) that are present during harmful algal blooms (HABs) [10]. The biotoxins can accumulate in marine organisms, which later could be a risk to humans if seafood is consumed. An illness such as yessotoxin poisoning can be developed after ingestion [10]. Furthermore, aerosolization of the toxins during blooms can pose another risk due to airborne exposure [14]. As for animals, the biotoxin can lead to death during large-scale algal blooms [2]. Despite L. polyedra not being an infectious pathogen, there are unknown aspects of the biotoxins and its indirect effects, specifically toxin transfer in the food web, that are not fully understood. As well as the long-term effects of low-level exposure to the toxins [10].
8. Current Research
Current research on Lingulodinium polyedra involves its role in the harmful algal blooms (red tide), especially in the context of climate change.
- Recent findings have pointed to rising water temperatures and varied concentrations of nitrogen oxides, ammonium, and silicon as the cause of red tide [2]. The optimal temperature for these blooms is between 18 and 19 °C. The optimal salinity window is between 34 and 35 [2]. In these conditions, L. polyedra can out-compete the other microorganisms through the production of yessotoxin. This can lead to changes in the food chains, not only affecting other microorganisms but also larger organisms such as fish [2]. There has been a correlation between L. polyedra and yessotoxin content in seawater, indicating that it is the dinoflagellate producing the toxin [10,14]. Some studies have detailed the effects of salinity on yessotoxin, focusing on the chemical components of the toxin rather than the conditions affecting the microbe itself [10]. At higher salinity levels there is a high production of the yessotoxin. The yessotoxin, however, is not directly affected by salinity: rather, salinity influences the post-transcriptional modifications of the protein by L. polyedra [10]. Other research on yessotoxin has focused on the types of cells that produce the toxin, as well as the conditions that led to its production [14]. One study concluded that L. polyedra is a low yessotoxin producer, but it is the most concentrated cell type at the peak of an algal bloom. It is predicted that L. polyedra focuses its energy on growth, rather than toxin production [14]. Another study focused on the triggering events of the algal blooms determined that sediment disturbance might play a bigger role than temperature and salinity in the environment. The same study urges continued research on the effect of L. polyedra to develop warning systems for the harmful blooms. An understanding of what triggers these blooms could help mitigate the harmful impact on ecosystems, human health, and socio-economics. [11]
References
[1] Beauchemin, M., Roy, S., Daoust, P., Dagenais-Bellefeuille, S., Bertomeu, T., Letourneau, L.,. . . Morse, D. (2012). Dinoflagellate tandem array gene transcripts are highly conserved and not polycistronic. Proceedings of the National Academy of Sciences - PNAS, 109(39), 15793–15798. doi:10.1073/pnas.1206683109
[2] Bizani, M., Bornman, T. G., Campbell, E. E., Perissinotto, R., & Deyzel, S. H. P. (2023). Mesozooplankton community responses to a large-scale harmful algal bloom induced by the non-indigenous dinoflagellate: lingulodinium polyedra. The Science of the Total Environment, 860, 161030. doi:10.1016/j.scitotenv.2022.161030
[3] Dagenais Bellefeuille, S., Dorion, S., Rivoal, J., & Morse, D. (2014). The dinoflagellate lingulodinium polyedrum responds to N depletion by a polarized deposition of starch and lipid bodies. PloS One, 9(11), e111067. doi:10.1371/journal.pone.0111067
[4] Dzhembekova N, Zlateva I, Rubino F, Belmonte M, Doncheva V, Popov I, Moncheva S (2024) Spatial distribution models and biodiversity of phytoplankton cysts in the Black Sea. Nature Conservation 55: 269-296. https://doi.org/10.3897/natureconservation.55.121181
[5] Figueroa, R. I., & Bravo, I. (2005). Sexual reproduction and two different encystment strategies of lingulodinium polyedrum (dinophyceae) in culture. Journal of Phycology, 41(2), 370–379. doi:10.1111/j.1529-8817.2005.04150.x
[6] Hastings JW. (2007). The Gonyaulax clock at 50: translational control of circadian expression. Cold Spring Harb Symp Quant Biol. 2007;72:141-4. doi: 10.1101/sqb.2007.72.026. PMID: 18419271.
[7] Iridian Genomes. (2024, March 26). Genome assembly ASM3757599v1. National Center of Biotechnology Information. https://api.ncbi.nlm.nih.gov/datasets/v2/genome/accession/GCA_037575995.1/download?include_annotation_type=GENOME_FASTA&include_annotation_type=GENOME_GFF&include_annotation_type=RNA_FASTA&include_annotation_type=CDS_FASTA&include_annotation_type=PROT_FAST
[8] Kudela Lab at University of California Santa Cruz. Phytoplankton Identification. Ocean Data Center. http://oceandatacenter.ucsc.edu/PhytoGallery/Dinoflagellates/lingulodinium .html#:~:text=Descrption:%20Armored%2C%20polyhedral%20cells%20without,Forms%20distinctive%20cysts.
[9] LEWIS, J., & HALLETT, R. (1997). Lingulodinium polyedrum (gonyaulax polyedra) a blooming dinoflagellate. Oceanography and Marine Biology, 35, 97–161
[10] Peter, C., Krock, B., & Cembella, A. (2018). Effects of salinity variation on growth and yessotoxin composition in the marine dinoflagellate lingulodinium polyedra from a skagerrak fjord system (western sweden). Harmful Algae, 78, 9–17. doi:10.1016/j.hal.2018.07.001
[11] Prego, R., Bao, R., Varela, M., & Carballeira, R. (2024). Naturally and anthropogenically induced lingulodinium polyedra dinoflagellate red tides in the galician rias (NW iberian peninsula). Toxins, 16(6), 280. doi:10.3390/toxins16060280
[12] Prevett, A., Lindström, J., Xu, J., Karlson, B., & Selander, E. (2019). Grazer-induced bioluminescence gives dinoflagellates a competitive edge. 29(12), PR564-R565. https://www.cell.com/current-biology/fulltext/S0960-9822(19)30554-8
[13] Roy, S., Beauchemin, M., Dagenais-Bellefeuille, S., Letourneau, L., Cappadocia, M., & Morse, D. (2014). The lingulodinium circadian system lacks rhythmic changes in transcript abundance. BMC Biology, 12(1), 107–107. doi:10.1186/s12915-014-0107-z
[14] Ternon, E., Carter, M. L., Cancelada, L., Lampe, R. H., Allen, A. E., Anderson, C. R., . . . Gerwick, W. H. (2023). Yessotoxin production and aerosolization during the unprecedented red tide of 2020 in southern California. Elementa, 11(1) doi:10.1525/elementa.2023.00021
[15] Schoch CL, et al. NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database (Oxford). 2020: baaa062. PubMed: 32761142 PMC: PMC7408187.
[16] Shen, C.-H. (2023). Gene Expression. Diagnostic Molecular Biology.
[17] Valiadi, M. & Iglesias-Rodriguez, D. (2013). Understanding Bioluminescence in Dinoflagellates–How Far Have We Come? https://pmc.ncbi.nlm.nih.gov/articles/PMC5029497/#B6-microorganisms-01-00003
Edited by [Lucy Arrillaga, Anna Babashak, Vidhi Chiplunkar, Melanie Flores, Amirah Mirza], students of [mailto:jmbhat@bu.edu Jennifer
Bhatnagar] for [http://www.bu.edu/academics/cas/courses/cas-bi-311/ BI 311
General Microbiology], Fall 2024, Boston University.
[[Category:Pages edited by students of Jennifer Bhatnagar at Boston University]]
