in

Dinophyceae can use exudates as weapons against the parasite Amoebophrya sp. (Syndiniales)

  • 1.

    Carlson CJ, Burgio KR, Dougherty ER, Phillips AJ, Bueno VM, Clements CF, et al. Parasite biodiversity faces extinction and redistribution in a changing climate. Sci Adv. 2017;3:e1602422.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 2.

    Johnson PTJ, Preston DL, Hoverman JT, LaFonte BE. Host and parasite diversity jointly control disease risk in complex communities. Proc Natl Acad Sci USA. 2013;110:16916–21.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 3.

    Dougherty ER, Carlson CJ, Bueno VM, Burgio KR, Cizauskas CA, Clements CF, et al. Paradigms for parasite conservation: parasite conservation. Conserv Biol. 2016;30:724–33.

    PubMed 
    Article 

    Google Scholar 

  • 4.

    Paseka RE, White LA, Van de Waal DB, Strauss AT, González AL, Everett RA, et al. Disease-mediated ecosystem services: pathogens, plants, and people. Trends Ecol Evolut. 2020;35:731–43.

    Article 

    Google Scholar 

  • 5.

    Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, et al. Determinants of community structure in the global plankton interactome. Science. 2015;348:1262073.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 6.

    Bjorbækmo MFM, Evenstad A, Røsæg LL, Krabberød AK, Logares R. The planktonic protist interactome: where do we stand after a century of research? ISME J. 2020;14:544–59.

    PubMed 
    Article 

    Google Scholar 

  • 7.

    Brussaard CPD. Viral control of phytoplankton populations-a review. J Eukaryot Microbiol. 2004;51:125–38.

    PubMed 
    Article 

    Google Scholar 

  • 8.

    Chambouvet A, Morin P, Marie D, Guillou L. Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science. 2008;322:1254–7.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 9.

    Vardi A, Van Mooy BA, Fredricks HF, Popendorf KJ, Ossolinski JE, Haramaty L, et al. Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science. 2009;326:861–5.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 10.

    Guillou L, Viprey M, Chambouvet A, Welsh RM, Kirkham AR, Massana R, et al. Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol. 2008;10:3349–65.

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 11.

    de Vargas C, Audic S, Henry N, Decelle J, Mahé F, Logares R, et al. Eukaryotic plankton diversity in the sunlit ocean. Science. 2015;348:1261605.

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 12.

    Siano R, Alves-de-Souza C, Foulon E, Bendif EM, Simon N, Guillou L, et al. Distribution and host diversity of Amoebophryidae parasites across oligotrophic waters of the Mediterranean Sea. Biogeosciences. 2011;8:267–78.

    Article 

    Google Scholar 

  • 13.

    Park M, Cooney S, Yih W, Coats D. Effects of two strains of the parasitic dinoflagellate Amoebophrya on growth, photosynthesis, light absorption, and quantum yield of bloom-forming dinoflagellates. Mar Ecol Prog Ser. 2002;227:281–92.

    Article 

    Google Scholar 

  • 14.

    Velo-Suárez L, Brosnahan ML, Anderson DM, McGillicuddy DJ. A Quantitative assessment of the role of the parasite Amoebophrya in the termination of Alexandrium fundyense blooms within a small coastal embayment. PLoS ONE. 2013;8:e81150.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 15.

    Li C, Song S, Liu Y, Chen T. Occurrence of Amoebophrya spp. infection in planktonic dinoflagellates in Changjiang (Yangtze River) Estuary, China. Harmful Algae. 2014;37:117–24.

    Article 

    Google Scholar 

  • 16.

    Choi CJ, Brosnahan ML, Sehein TR, Anderson DM, Erdner DL. Insights into the loss factors of phytoplankton blooms: the role of cell mortality in the decline of two inshore Alexandrium blooms. Limnol Oceanogr. 2017;62:1742–53.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 17.

    Coats DW, Park MG. Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta); parasite survival, infectivity, generation time, and host specificity. J Phycol. 2002;38:520–8.

    Article 

    Google Scholar 

  • 18.

    Cai R, Kayal E, Alves-de-Souza C, Bigeard E, Corre E, Jeanthon C, et al. Cryptic species in the parasitic Amoebophrya species complex revealed by a polyphasic approach. Sci Rep. 2020;10:2531.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 19.

    Anderson SR, Harvey EL. Temporal variability and ecological interactions of parasitic marine Syndiniales in coastal protist communities. mSphere. 2020;5:e00209–20.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 20.

    Alves-de-Souza C, Pecqueur D, Le Floc’h E, Mas S, Roques C, Mostajir B, et al. Significance of plankton community structure and nutrient availability for the control of dinoflagellate blooms by parasites: a modeling approach. PLoS ONE. 2015;10:e0127623.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 21.

    Alacid E, Park MG, Turon M, Petrou K, Garcés E. A game of russian roulette for a generalist dinoflagellate parasitoid: host susceptibility is the key to success. Front Microbiol. 2016;7:769.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 22.

    Vincent F, Sheyn U, Porat Z, Schatz D, Vardi A. Visualizing active viral infection reveals diverse cell fates in synchronized algal bloom demise. Proc Natl Acad Sci USA. 2021;118:e2021586118.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 23.

    Chambouvet A, Alves-de-Souza C, Cueff V, Marie D, Karpov S, Guillou L. Interplay between the parasite Amoebophrya sp. (Alveolata) and the cyst formation of the red tide dinoflagellate Scrippsiella trochoidea. Protist. 2011;162:637–49.

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 24.

    Pelusi A, De Luca P, Manfellotto F, Thamatrakoln K, Bidle KD, Montresor M. Virus‐induced spore formation as a defense mechanism in marine diatoms. New Phytol. 2020;229:16951–2259.

    Google Scholar 

  • 25.

    Pouneva ID. Effect of abscisic acid and ontogenic phases of the host alga on the infection process in the pathosystem Scenedesmus acutusPhlyctidium scenenedesmi. Acta Physiol Plant. 2006;28:395–400.

    CAS 
    Article 

    Google Scholar 

  • 26.

    Bai X, Adolf JE, Bachvaroff T, Place AR, Coats DW. The interplay between host toxins and parasitism by Amoebophrya. Harmful Algae. 2007;6:670–8.

    CAS 
    Article 

    Google Scholar 

  • 27.

    Place AR, Bai X, Kim S, Sengco MR, Wayne, Coats D. Dinoflagellate host-parasite sterol profiles dictate karlotoxin sensitivity. J Phycol. 2009;45:375–85.

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 28.

    Rohrlack T, Christiansen G, Kurmayer R. Putative antiparasite defensive system involving ribosomal and nonribosomal oligopeptides in Cyanobacteria of the Genus Planktothrix. Appl Environ Microbiol. 2013;79:2642–7.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 29.

    Scholz B, Küpper F, Vyverman W, Ólafsson H, Karsten U. Chytridiomycosis of marine diatoms—the role of stress physiology and resistance in parasite-host recognition and accumulation of defense molecules. Marine Drugs. 2017;15:26.

    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 30.

    Granéli E, Hansen PJ. Allelopathy in harmful algae: a mechanism to compete for resources? In: Granéli E, Turner JT, editors. Ecology of harmful algae. Springer Berlin Heidelberg; 2006. p. 189–201.

  • 31.

    Farhat S, Le P, Kayal E, Noel B, Bigeard E, Corre E, et al. Rapid protein evolution, organellar reductions, and invasive intronic elements in the marine aerobic parasite dinoflagellate Amoebophrya spp. BMC Biol. 2021;19:1.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 32.

    Chapelle A, Le Bec C, Amzil Z, Dreanno C, Klouch KZ, Labry C, et al. Etude sur la proliferation de la micro algue Alexandrium minutum en rade de Brest (2014).

  • 33.

    Chapelle A, Le Gac M, Labry C, Siano R, Quere J, Caradec F, et al. The Bay of Brest (France), a new risky site for toxic Alexandrium minutum blooms and PSP shellfish contamination. Harmful Algal News. 2015;51:4–5.

  • 34.

    Klouch KZ, Schmidt S, Andrieux-Loyer F, Le Gac M, Hervio-Heath D, Qui-Minet ZN. et al. Historical records from dated sediment cores reveal the multidecadal dynamic of the toxic dinoflagellate Alexandrium minutum in the Bay of Brest (France). FEMS Microbiol Ecol. 2016;92:fiw101

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 35.

    Long M, Tallec K, Soudant P, Le Grand F, Donval A, Lambert C, et al. Allelochemicals from Alexandrium minutum induce rapid inhibition of metabolism and modify the membranes from Chaetoceros muelleri. Algal Res. 2018;35:508–18.

    Article 

    Google Scholar 

  • 36.

    Long M, Peltekis A, González-Fernández C, Bailleul B, Hégaret H. Allelochemicals of Alexandrium minutum: kinetics of membrane disruption and photosynthesis inhibition in a co-occurring diatom. Harmful Algae. 2021;103:101997.

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 37.

    Starr RC, Zeikus JA. Utex—The culture collection of algae at the university of Texas at Austin 1993 List of cultures. J Phycol. 1993;29:1–106.

    Article 

    Google Scholar 

  • 38.

    Keller M, Selvin R, Claus W, Guillard RRL. Media for the culture of oceanic ultraphytoplankton 1, 2. J Phycol. 1987;23:633–8.

  • 39.

    Bigeard. Collect of Amoebophrya parasite (free-living stage) for genomic and transcriptomic analyses. 2019. Protocols.io.

  • 40.

    Kim S, Gil Park M, Yih W, Coats DW. Infection of the bloom-forming thecate dinoflagellates Alexandrium affina and Gonyaulax spinifera by two strains of Amoebophrya (Dinophyta). J Phycol. 2004;40:815–22.

    Article 

    Google Scholar 

  • 41.

    Kim S. Patterns in host range for two strains of Amoebophrya (Dinophyta) infecting thecate dinoflagellates: Amoebophrya spp. ex Alexandrium affine and ex Gonyaulax polygramma. J Phycol. 2006;42:1170–3.

    Article 

    Google Scholar 

  • 42.

    Kayal E, Alves-de-Souza C, Farhat S, Velo-Suarez L, Monjol J, Szymczak J, et al. Dinoflagellate host chloroplasts and mitochondria remain functional during Amoebophrya Infection. Front Microbiol. 2020;11:600823.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 43.

    R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

  • 44.

    John U, Tillmann U, Hülskötter J, Alpermann TJ, Wohlrab S, Van de Waal DB. Intraspecific facilitation by allelochemical mediated grazing protection within a toxigenic dinoflagellate population. Proc R Soc B. 2015;282:20141268.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 45.

    Lelong A, Haberkorn H, Le Goïc N, Hégaret H, Soudant P. A new insight into allelopathic effects of Alexandrium minutum on photosynthesis and respiration of the diatom Chaetoceros neogracile revealed by photosynthetic-performance analysis and flow cytometry. Microb Ecol. 2011;62:919–30.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 46.

    Tillmann U, Alpermann T, John U, Cembella A. Allelochemical interactions and short-term effects of the dinoflagellate Alexandrium on selected photoautotrophic and heterotrophic protists. Harmful Algae. 2008;7:52–64.

    Article 

    Google Scholar 

  • 47.

    Durham WM, Stocker R. Thin phytoplankton layers: characteristics, mechanisms, and consequences. Annu Rev Mar Sci. 2012;4:177–207.

    Article 

    Google Scholar 

  • 48.

    Breier RE, Lalescu CC, Waas D, Wilczek M, Mazza MG. Emergence of phytoplankton patchiness at small scales in mild turbulence. Proc Natl Acad Sci USA. 2018;115:12112–7.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 49.

    Wheeler JD, Secchi E, Rusconi R, Stocker R. Not just going with the flow: the effects of fluid flow on bacteria and plankton. Annu Rev Cell Dev Biol. 2019;35:213–37.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 50.

    Basterretxea G, Font-Muñoz JS, Tuval I. Phytoplankton orientation in a turbulent ocean: a microscale perspective. Front Mar Sci. 2020;7:185.

    Article 

    Google Scholar 

  • 51.

    Blossom HE, Markussen B, Daugbjerg N, Krock B, Norlin A, Hansen PJ. The cost of toxicity in microalgae: direct evidence from the dinoflagellate Alexandrium. Front Microbiol. 2019;10:1065.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 52.

    Martens H, Van de Waal DB, Brandenburg KM, Krock B, Tillmann U. Salinity effects on growth and toxin production in an Alexandrium ostenfeldii (Dinophyceae) isolate from The Netherlands. J Plankton Res. 2016;38:1302–16.

    CAS 
    Article 

    Google Scholar 

  • 53.

    Long M, Holland A, Planquette H, González Santana D, Whitby H, Soudant P, et al. Effects of copper on the dinoflagellate Alexandrium minutum and its allelochemical potency. Aquat Toxicol. 2019;210:251–61.

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 54.

    Brown ER, Kubanek J. Harmful alga trades off growth and toxicity in response to cues from dead phytoplankton. Limnol Oceanogr. 2020;65:1723–33.

    CAS 
    Article 

    Google Scholar 

  • 55.

    Selander E, Thor P, Toth G, Pavia H. Copepods induce paralytic shellfish toxin production in marine dinoflagellates. Proc R Soc B. 2006;273:1673–80.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 56.

    Lu Y, Wohlrab S, Groth M, Glöckner G, Guillou L, John U. Transcriptomic profiling of Alexandrium fundyense during physical interaction with or exposure to chemical signals from the parasite Amoebophrya. Mol Ecol. 2016;25:1294–307.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 57.

    Seymour JR, Amin SA, Raina J-B, Stocker R. Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat Microbiol. 2017;2:17065.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 58.

    Place A, Harvey H, Bai X, Coats D. Sneaking under the toxin surveillance radar: parasitism and sterol content. Afr J Mar Sci. 2006;28:347–51.

    Article 

    Google Scholar 

  • 59.

    Ma H, Krock B, Tillmann U, Bickmeyer U, Graeve M, Cembella A. Mode of action of membrane-disruptive lytic compounds from the marine dinoflagellate Alexandrium tamarense. Toxicon. 2011;58:247–58.

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 60.

    Deeds J, Place A. Sterol-specific membrane interactions with the toxins from Karlodinium micrum (Dinophyceae) — a strategy for self-protection? Afr J Mar Sci. 2006;28:421–5.

    Article 

    Google Scholar 

  • 61.

    Leblond JD, Sengco MR, Sickman JO, Dahmen JL, Anderson DM. Sterols of the Syndinian dinoflagellate Amoebophrya sp., a parasite of the dinoflagellate Alexandrium tamarense (Dinophyceae). J Eukaryotic Microbiol. 2006;53:211–6.

    CAS 
    Article 

    Google Scholar 

  • 62.

    Long M, Tallec K, Soudant P, Lambert C, Le Grand F, Sarthou G, et al. A rapid quantitative fluorescence-based bioassay to study allelochemical interactions from Alexandrium minutum. Environ Pollut. 2018;242:1598–605.

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 63.

    Borcier E, Morvezen R, Boudry P, Miner P, Charrier G, Laroche J, et al. Effects of bioactive extracellular compounds and paralytic shellfish toxins produced by Alexandrium minutum on growth and behaviour of juvenile great scallops Pecten maximus. Aquatic Toxicol. 2017;184:142–54.

    CAS 
    Article 

    Google Scholar 

  • 64.

    Castrec J, Soudant P, Payton L, Tran D, Miner P, Lambert C, et al. Bioactive extracellular compounds produced by the dinoflagellate Alexandrium minutum are highly detrimental for oysters. Aquat Toxicol. 2018;199:188–98.

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 65.

    Wang Y, Tang X. Interactions between Prorocentrum donghaiense Lu and Scrippsiella trochoidea (Stein) Loeblich III under laboratory culture. Harmful Algae. 2008;7:65–75.

    Article 

    Google Scholar 

  • 66.

    Tang YZ, Gobler CJ. Lethal effects of Northwest Atlantic Ocean isolates of the dinoflagellate, Scrippsiella trochoidea, on Eastern oyster (Crassostrea virginica) and Northern quahog (Mercenaria mercenaria) larvae. Mar Biol. 2012;159:199–210.

    Article 

    Google Scholar 

  • 67.

    Felpeto AB, Roy S, Vasconcelos VM. Allelopathy prevents competitive exclusion and promotes phytoplankton biodiversity. Oikos. 2018;127:85–98.

    Article 

    Google Scholar 

  • 68.

    Driscoll WW, Hackett JD, Ferrière R. Eco-evolutionary feedbacks between private and public goods: evidence from toxic algal blooms. Ecol Lett. 2016;19:81–97.

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 69.

    Driscoll WW, Espinosa NJ, Eldakar OT, Hackett JD. Allelopathy as an emergent, exploitable public good in the bloom-forming microalga Prymnesium parvum. Evolution. 2013;67:1582–90.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 70.

    Rodríguez F, Figueroa RI. Confirmation of the wide host range of Parvilucifera corolla (Alveolata, Perkinsozoa). Eur J Protistol. 2020;74:125690.

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 71.

    Chambouvet A, Laabir M, Sengco M, Vaquer A, Guillou L. Genetic diversity of Amoebophryidae (Syndiniales) during Alexandrium catenella/tamarense (Dinophyceae) blooms in the Thau lagoon (Mediterranean Sea, France). Res Microbiol. 2011;162:959–68.

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 72.

    Cosgrove S. Monitoring methods and bloom dynamic studies of the toxic dinoflagellate genus Alexandrium. 2014. Doctoral dissertation, National University of Ireland, Galway.

  • 73.

    Hutchinson GE. The Paradox of the plankton. Am Nat. 1961;95:137–45.

    Article 

    Google Scholar 

  • 74.

    Czaran TL, Hoekstra RF, Pagie L. Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci USA. 2002;99:786–90.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 75.

    Garcés E, Alacid E, Reñé A, Petrou K, Simó R. Host-released dimethylsulphide activates the dinoflagellate parasitoid Parvilucifera sinerae. ISME J. 2013;7:1065–8.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 76.

    Fitzpatrick CR, Salas-González I, Conway JM, Finkel OM, Gilbert S, Russ D. et al. The plant microbiome: from ecology to reductionism and beyond. Annu Rev Microbiol. 2020;74:annurev-micro-022620-014327

    Article 
    CAS 

    Google Scholar 

  • 77.

    Carney LT, Lane TW. Parasites in algae mass culture. Front Microbiol. 2014;5:278.


  • Source: Ecology - nature.com

    Asegun Henry has a big idea for tackling climate change: Store up the sun

    New directions in real estate practice