Interactions of the diatom algae Pseudo-nitzschia hasleana and Thalassiosira pseudonana in the mixed culture
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Abstract
Representatives of the genus Pseudo-nitzschia (Bacillariophyta) cause blooms in different areas of the World Ocean. Therefore, it is necessary to know their ecological features, including the way those interact with other species of unicellular algae. Moreover, for rapid identification of these algae in the environment, a certain technique is needed. Thus, we assessed the dynamics of cell abundance for Pseudo-nitzschia hasleana and Thalassiosira pseudonana in mono- and mixed cultures by their direct counting in a Nageotte chamber. Temperature curves of chlorophyll a fluorescence obtained by laser-induced fluorescence in a temperature chamber were also analyzed. The experiments lasted for 14 days. As shown, P. hasleana had different effect on T. pseudonana depending on initial abundance of T. pseudonana. At initial concentration of 0.8 × 104 cells·mL−1, a pronounced stimulation of the growth of this diatom occurred. At initial concentrations of 1.6 × 104 and 3.2 × 104 cells·mL−1, T. pseudonana growth was inhibited. In the mixed culture, T. pseudonana remained at the stationary growth phase, while in a monoculture, the population entered the dying phase by the 14th day of the experiment. T. pseudonana had an inhibitory effect on P. hasleana growth. The experiment with P. hasleana and T. pseudonana co-cultivation showed as follows: chlorophyll a fluorescence of the mixture is more affected by the microalga with much higher concentration. The fluorescent signal of two separately cultivated monocultures can potentially be used to search for these cultures in a mixture.
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Balzano S., Percopo I., Siano R., Gourvil P., Chanoine M., Marie D., Vaulot D., Sarno D. Morphological and genetic diversity of Beaufort Sea diatoms with high contributions from the Chaetoceros neogracilis species complex. Journal of Phycology, 2017, vol. 53, iss. 1, pp. 161–187. https://doi.org/10.1111/jpy.12489
Bates S. S., Bird C. J., de Freitas A. S. W., Foxall R., Gilgan M., Hanic L. A., Johnson G. R., McCulloch A. W., Odense P., Pocklington R., Quilliam M. A., Sim P. G., Smith J. C., Subba Rao D. V., Todd E. C. D., Walter J. A., Wrigh J. L. C. Pennate diatom Nitzschia pungens as the primary source of domoic acid, a toxin in shellfish from eastern Prince Edward Island, Canada. Canadian Journal of Fisheries and Aquatic Sciences, 1989, vol. 46, no. 7, pp. 1203–1215. https://doi.org/10.1139/f89-156
Burkholder J. A. M., Glibert P. M., Skelton H. M. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae, 2008, vol. 8, iss. 1, pp. 77–93. https://doi.org/10.1016/j.hal.2008.08.010
Cai Z., Zhu H., Duan S. Allelopathic interactions between the red-tide causative dinoflagellate Prorocentrum donghaiense and the diatom Phaeodactylum tricornutum. Oceanologia, 2014, vol. 56, iss. 3, pp. 639–650. https://doi.org/10.5697/oc.56-3.639
Cohen N. R., Ellis K. A., Lampe R. H., McNair H., Twining B. S., Maldonado M. T., Brzezinski M. A., Kuzminov F. I., Thamatrakoln K., Till C. P., Bruland K. W., Sunda W. G., Bargu S., Marchetti A. Diatom transcriptional and physiological responses to changes in iron bioavailability across ocean provinces. Frontiers in Marine Science, 2017, vol. 4, art. no. 360 (20 p.). https://doi.org/10.3389/fmars.2017.00360
Guillard R. R. L., Ryther J. H. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology, 1962, vol. 8, no. 2, pp. 229–239. https://doi.org/10.1139/m62-029
Harris A. S. D., Medlin L. K., Lewis J., Jones K. J. Thalassiosira species (Bacillariophyceae) from a Scottish sea-loch. European Journal of Phycology, 1995, vol. 30, iss. 2, pp. 117–131. https://doi.org/10.1080/09670269500650881
Hillebrand H., Dürselen C. D., Kirschtel D., Pollingher U., Zohary T. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 1999, vol. 35, iss. 2, pp. 403–424. https://doi.org/10.1046/j.1529-8817.1999.3520403.x
Huang C., Lin X., Lin J., Du H., Dong Q. Population dynamics of Pseudo-nitzschia pungens in Zhelin Bay, China. Journal of the Marine Biological Association of the United Kingdom, 2009, vol. 89, iss. 4, pp. 663–668. https://doi.org/10.1017/S0025315408002919
Hulot F., Huisman J. Allelopathic interactions between phytoplankton species: The roles of heterotrophic bacteria and mixing intensity. Limnology and Oceanography, 2004, vol. 49, iss. 4, pt 2, pp. 1424–1434. https://doi.org/10.4319/lo.2004.49.4_part_2.1424
Hutchinson G. E. The paradox of the plankton. The American Naturalist, 1961, vol. 95, no. 882, pp. 137–145. https://doi.org/10.1086/282171
Felpeto A. B., Śliwińska-Wilczewska S., Klin M., Konarzewska Z., Vasconcelos V. Temperature-dependent impacts of allelopathy on growth, pigment, and lipid content between a subpolar strain of Synechocystis sp. CCBA MA-01 and coexisting microalgae. Hydrobiologia, 2019, vol. 835, iss. 1, pp. 117–128. https://doi.org/10.1007/s10750-019-3933-8
Ianora A., Bentley M. G., Caldwell G. S., Casotti R., Cembella A. D., Engström-Öst J., Halsband C., Sonnenschein E., Legrand C., Llewellyn C. A., Paldavičienë A., Pilkaityte R., Pohnert G., Razinkovas A., Romano G., Tillmann U., Vaiciute D. The relevance of marine chemical ecology to plankton and ecosystem function: An emerging field. Marine Drugs, 2011, vol. 9, iss. 9, pp. 1625–1648. https://doi.org/10.3390/md9091625
Lelong A., Hégaret H., Soudant P., Bates S. S. Pseudo-nitzschia (Bacillariophyceae) species, domoic acid and amnesic shellfish poisoning: Revisiting previous paradigms. Phycologia, 2012, vol. 51, iss. 2, pp. 168–216. https://doi.org/10.2216/11-37.1
Lima-Mendez G., Faust K., Henry N., Decelle J., Colin S., Carcillo F., Chaffron S., Ignacio-Espinosa J. C., Roux S., Vincent F., Bittner L., Darzi Y., Wang J., Audic S., Berline L., Bontempi G., Cabello A. M., Coppola L., Cornejo-Castillo F. M., D’Ovidio F., de Meester L., Ferrera I., Garet-Delmas M.-J., Guidi L., Lara E., Pesant S., Royo-Llonch M., Alazar G., Sánchez P., Sebastian M., Souffreau C., Dimier C., Picheral M., Searson S., Kandels-Lewis S., Tara Oceans Coordinators, Gorsky G., Not F., Ogata H., Speich S., Stemmann L., Weissenbach J., Wincker P., Acinas S. G., Sunagawa S., Bork P., Sullivan M. B., Karsenti E., Bowler C., de Vargas C., Raes J. Determinants of community structure in the global plankton interactome. Science, 2015, vol. 348, no. 6237, art. no. 1262073 (10 p.). https://doi.org/10.1126/science.1262073
Long M., Tallec K., Soudant P., Le Grand F., Donval A., Lambert C., Sarthou G., Jolley D. F., Hégaret H. Allelochemicals from Alexandrium minutum induce rapid inhibition of metabolism and modify the membranes from Chaetoceros muelleri. Algal Research, 2018, vol. 35, pp. 508–518. https://doi.org/10.1016/j.algal.2018.09.023
Louw D. C., Doucette G. J., Voges E. Annual patterns, distribution and long-term trends of Pseudo-nitzschia species in the northern Benguela upwelling system. Journal of Plankton Research, 2017, vol. 39, iss. 1, pp. 35–47. https://doi.org/10.1093/plankt/fbw079
Lundholm N., Hansen P. J., Kotaki Y. Lack of allelopathic effects of the domoic acid-producing marine diatom Pseudo-nitzschia multiseries. Marine Ecology Progress Series, 2005, vol. 288, pp. 21–33. https://doi.org/10.3354/meps288021
Mardones J. I. Screening of Chilean fish-killing microalgae using a gill cell-based assay. Latin American Journal of Aquatic Research, 2020, vol. 48, iss. 2, pp. 329–335. https://dx.doi.org/10.3856/vol48-issue2-fulltext-2400
Mikheev M. A., Ipatova V. I., Spirkina N. E. Biotic interactions between two species of microalgae in mixed culture. Moscow University Biological Sciences Bulletin, 2018, vol. 73, iss. 2, pp. 63–68. https://doi.org/10.3103/S0096392518020062
Orlova T. Yu., Stonik I. V., Shevchenko O. G. Flora of planktonic microalgae of Amursky Bay, Sea of Japan. Russian Journal of Marine Biology, 2009, vol. 35, iss. 1, pp. 60–78. https://doi.org/10.1134/S106307400901009X
Patil V., Abate R., Wu W., Zhang J., Lin H., Chen C., Liang J., Sun L., Li X., Li Y., Gao Y. Allelopathic inhibitory effect of the macroalga Pyropia haitanensis (Rhodophyta) on harmful bloom-forming Pseudo-nitzschia species. Marine Pollution Bulletin, 2020, vol. 161, pt A, art. no. 111752 (12 p.). https://doi.org/10.1016/j.marpolbul.2020.111752
Phatarpekar P. V., Sreepada R. A., Pednekar C., Achuthankutty C. T. A comparative study on growth performance and biochemical composition of mixed culture of Isochrysis galbana and Chaetoceros calcitrans with monocultures. Aquaculture, 2000, vol. 181, iss. 1–2, pp. 141–155. https://doi.org/10.1016/S0044-8486(99)00227-6
Pichierri S., Accoroni S., Pezzolesi L., Guerrini F., Romagnoli T., Pistocchi R., Totti C. Allelopathic effects of diatom filtrates on the toxic benthic dinoflagellate Ostreopsis cf. ovata. Marine Environmental Research, 2017, vol. 131, pp. 116–122. https://doi.org/10.1016/j.marenvres.2017.09.016
Popik A., Gamayunov E., Voznesenskiy S., Markina Zh., Orlova T. The study of fluorescence features of microalgae from the genus Pseudo-nitzschia and the possibility of their detection in water. Algal Research, 2022, vol. 64, art. no. 102662 (10 p.). https://doi.org/10.1016/j.algal.2022.102662
Poulin R. X., Poulson-Ellestad K. L., Roy J. S., Kubanek J. Variable allelopathy among phytoplankton reflected in red tide metabolome. Harmful Algae, 2018, vol. 71, pp. 50–56. https://doi.org/10.1016/j.hal.2017.12.002
Prasetiya F. S., Safitri I., Widowati I., Cognie B., Decottignies P., Gastineau R., Morançais M., Windarto E., Tremblay R., Mouget J. L. Does allelopathy affect co-culturing Haslea ostrearia with other microalgae relevant to aquaculture? Journal of Applied Phycology, 2016, vol. 28, iss. 4, pp. 2241–2254. https://doi.org/10.1007/s10811-015-0779-y
Sobrinho B. F., De Camargo L. M., Sandrini-Neto L., Kleemann C. R., da Costa Machado E., Mafra L. L. Growth, toxin production and allelopathic effects of Pseudo-nitzschia multiseries under iron-enriched conditions. Marine Drugs, 2017, vol. 15, iss. 10, art. no. 331 (16 p.). https://doi.org/10.3390/md15100331
Tan K., Huang Z., Ji R., Qiu Y., Wang Z., Liu J. A review of allelopathy on microalgae. Microbiology, 2019, vol. 165, iss. 6, pp. 587–592. https://doi.org/10.1099/mic.0.000776
Ternon E., Pavaux A. S., Marro S., Thomas O. P., Lemée R. Allelopathic interactions between the benthic toxic dinoflagellate Ostreopsis cf. ovata and a co-occurring diatom. Harmful Algae, 2018, vol. 75, pp. 35–44. https://doi.org/10.1016/j.hal.2018.04.003
Trainer V. L., Bates S. S., Lundholm N., Thessen A. E., Cochlan W. P., Adams N. G., Trick C. G. Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae, 2012, vol. 14, pp. 271–300. https://doi.org/10.1016/j.hal.2011.10.025
Voznesenskiy S. S., Gamayunov E. L., Popik A. Yu., Markina Zh. V., Orlova T. Yu. Temperature dependence of the parameters of laser-induced fluorescence and species composition of phytoplankton: The theory and the experiments. Algal Research, 2019, vol. 44, art. no. 101719 (11 p.). https://doi.org/10.1016/j.algal.2019.101719
Yamasaki Y., Shikata T., Nukata A., Ichiki S., Nagasoe S., Matsubara T., Shimasaki Y., Nakao M., Yamaguchi K., Oshima Y., Oda T., Ito T., Jenkinson I. R., Asakawa M., Honjo T. Extracellular polysaccharide-protein complexes of a harmful alga mediate the allelopathic control it exerts within the phytoplankton community. The ISME Journal, 2009, vol. 3, iss. 7, pp. 808–817. https://doi.org/10.1038/ismej.2009.24
Yamasaki Y., Nagasoe S., Matsubara T., Shikata T., Shimasaki Y., Oshima Y., Honjo T. Allelopathic interactions between the bacillariophyte Skeletonema costatum and the raphidophyte Heterosigma akashiwo. Marine Ecology Progress Series, 2007, vol. 339, pp. 83–92. https://doi.org/10.3354/meps339083
Yasakova O. N. The seasonal dynamics of potentially toxic and harmful phytoplankton species in Novorossiysk Bay (Black Sea). Russian Journal of Marine Biology, 2013, vol. 39, iss. 2, pp. 107–115. https://doi.org/10.1134/S1063074013020090
Xu N., Tang Y. Z., Qin J., Duan S., Gobler C. J. Ability of the marine diatoms Pseudo-nitzschia multiseries and P. pungens to inhibit the growth of co-occurring phytoplankton via allelopathy. Aquatic Microbial Ecology, 2015, vol. 74, no. 1, pp. 29–41. https://doi.org/10.3354/ame01724
Zhao M., Chen X., Ma N., Zhang Q., Qu D., Li M. Overvalued allelopathy and overlooked effects of humic acid-like substances on Microcystis aeruginosa and Scenedesmus obliquus competition. Harmful Algae, 2018, vol. 78, pp. 18–26. https://doi.org/10.1016/j.hal.2018.07.003
Zheng J.-W., Li D.-W., Lu Y., Chen J., Liang J.-J., Zhang L., Yang W.-D., Liu J.-S., Lu S.-H., Li H.-Y. Molecular exploration of algal interaction between the diatom Phaeodactylum tricornutum and the dinoflagellate Alexandrium tamarense. Algal Research, 2016, vol. 17, pp. 132–141. https://doi.org/10.1016/j.algal.2016.04.019