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Yeyin YANG, Bozhu HUANG, Yingzhong TANG, Ning XU. Allelopathic effects of mixotrophic dinoflagellate Akashiwo sanguinea on co-occurring phytoplankton: the significance of nutritional ecology[J]. Journal of Oceanology and Limnology, 2021, 39(3): 903-917

Allelopathic effects of mixotrophic dinoflagellate Akashiwo sanguinea on co-occurring phytoplankton: the significance of nutritional ecology

Yeyin YANG1, Bozhu HUANG1,2, Yingzhong TANG3, Ning XU1
1 Department of Ecology/Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China;
2 Guangdong Environmental Monitoring Center, Guangzhou 510308, China;
3 Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
Blooms of Akashiwo sanguinea frequently break out around the world, causing huge economic losses to the aquaculture industry and seriously damaging coastal ecosystems. However, the formation mechanisms of A. sanguinea blooms remain unclear. We investigated the allelopathic effects of A. sanguinea on multiple phytoplankton species, explored the mode of allelochemicals action and the way of nutrient factors regulation of the allelopathic activity. Results show that strains of A. sanguinea could inhibit the growth of co-occurring phytoplankton including Scrippsiella trochoidea, Phaeocystis globosa, and Rhodomonas salina, but inhibition of Prorocentrum micans was not obvious. The inhibition rates on phytoplankton were positively correlated with the cell densities of A. sanguinea. The highest inhibition rate of 94% on R. salina was for A. sanguinea CCMA256 culture of 2 000 cells/mL at 72 h. We observed that cells of S. trochoidea, Ph. globosa, and R. salina were lysed when co-cultured with A. sanguinea, with the shortest time for S. trochoidea. Additionally, the growth rates of A. sanguinea were promoted by coculturing with S. trochoidea, Ph. globosa, and R. salina. Four components of A. sanguinea culture were all able to inhibit growth of R. salina: the strongest inhibitory effect was found in the sonicated culture, followed by whole-cell culture, filtrates of sonicated culture, and filtrate culture. The crude extract of A. sanguinea culture also lysed cells of R. salina, and the inhibition rates on R. salina increased with the increasing dose of crude extract. It was shown that both nutrient enrichment and nitrogen:phosphorus ratio imbalance enhanced remarkably the allelopathic activity of A. sanguinea. The highest inhibition rate on R. salina of 70% occurred in A. sanguinea JX13 treatment at 2 000 cells/mL under high nutrient condition in 48 h. In JX14 treatment at 2 000 cells/mL for N:P of 10:1, the inhibition rate increased by 1.7 times of that for N:P of 20:1. In addition, the allelopathy of A. sanguinea could not only be a competitive strategy but also a nutrition strategy, playing an important role in formation and/or maintenance of blooms of the mixotrophic dinoflagellate A. sanguinea.
Key words:    Akashiwo sanguinea|harmful algal blooms|mixotrophy|allelopathy|nutrients   
Received: 2020-03-25   Revised: 2020-05-05
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Accoroni S, Glibert P M, Pichierri S, Romagnoli T, Marini M, Totti C. 2015. A conceptual model of annual Ostreopsis cf. ovata blooms in the northern Adriatic Sea based on the synergic effects of hydrodynamics, temperature, and the N:P ratio of water column nutrients. Harmful Algae, 45:14-25,
Adolf J E, Bachvaroff T R, Krupatkina D N, Nonogaki H, Brown P J P, Lewitus A J, Harvey H R, Place A R. 2006.Species specificity and potential roles of Karlodinium micrum toxin. African Journal of Marine Science, 28(2):415-419,
Adolf J E, Krupatkina D, Bachvaroff T, Place A R. 2007.Karlotoxin mediates grazing by Oxyrrhis marina on strains of Karlodinium veneficum. Harmful Algae, 6(3):400-412,
Anderson D M, Burkholder J M, Cochlan W P, Glibert P M, Gobler C J, Heil C A, Kudela R M, Parsons M L, Rensel J E J, Townsend D W, Trainer V L, Vargo G A. 2008.Harmful algal blooms and eutrophication:examining linkages from selected coastal regions of the United States. Harmful Algae, 8(1):39-53,
Badylak S, Phlips E J, Mathews A L. 2014. Akashiwo sanguinea(Dinophyceae) blooms in a sub-tropical estuary:an alga for all seasons. Plankton and Benthos Research, 9(3):147-155,
Berge T, Poulsen L K, Moldrup M, Daugbjerg N, Juel H P. 2012. Marine microalgae attack and feed on metazoans.The ISME Journal, 6(10):1 926-1 936,
Bockstahler K R, Coats D W. 1993. Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay. Marine Biology, 116(3):477-487,
Botes L, Smit A J, Cook P A. 2003. The potential threat of algal blooms to the abalone (Haliotis midae) mariculture industry situated around the South African coast. Harmful Algae, 2(4):247-259,
Burkholder J M, Glibert P M, Skelton H M. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae, 8(1):77-93,
Castro N O, Domingos P, Moser G A O. 2016. National and international public policies for the management of harmful algal bloom events. A case study on the Brazilian coastal zone. Ocean & Coastal Management, 128:40-51,
Chakraborty S, Feudel U. 2014. Harmful algal blooms:combining excitability and competition. Theoretical Ecology, 7(3):221-237,
Chen T T, Liu Y, Song S Q, Li C W, Tang Y Z, Yu Z M. 2015.The effects of major environmental factors and nutrient limitation on growth and encystment of planktonic dinoflagellate Akashiwo sanguinea. Harmful Algae, 46:62-70,
Driscoll W W, Espinosa N J, Eldakar O T, Hackett J D. 2013.Allelopathy as an emergent, exploitable public good in the bloom-forming microalga Prymnesium parvum.Evolution, 67(6):1 582-1 590,
Du X N, Peterson W, McCulloch A, Liu G X. 2011. An unusual bloom of the dinoflagellate Akashiwo sanguinea off the central Oregon, USA, coast in autumn 2009.Harmful Algae, 10(6):784-793,
Fistarol G O, Legrand C, Selander E, Hummert C, Stolte W, Graneli E. 2004. Allelopathy in Alexandrium spp.:effect on a natural plankton community and on algal monocultures. Aquatic Microbial Ecology, 35(1):45-56,
Fleming L E, Broad K, Clement A, Dewailly E, Elmir S, Knap A, Pomponi S A, Smith S, Solo Gabriele H, Walsh P. 2006. Oceans and human health:emerging public health risks in the marine environment. Marine Pollution Bulletin, 53(10-12):545-560,
Flynn K J, Stoecker D K, Mitra A, Raven J A, Glibert P M, Hansen P J, Granéli E, Burkholder J M. 2013. Misuse of the phytoplankton-zooplankton dichotomy:the need to assign organisms as mixotrophs within plankton functional types. Journal of Plankton Research, 35(1):3-11,
Galloway J N, Cowling E B, Seitzinger S P, Socolow R H. 2002. Reactive nitrogen:too much of a good thing? Ambio A Journal of the Human Environment, 31(2):60-63,
Glibert P M, Allen J I, Bouwman A F, Brown C W, Flynn K J, Lewitus A J, Madden C J. 2010. Modeling of HABs and eutrophication:status, advances, challenges. Journal of Marine Systems, 83(3-4):262-275,
Glibert P M, Beusen A H W, Harrison J A, Dürr H H, Bouwman A F, Laruelle G G. 2018. Changing land-, sea-, and airscapes:sources of nutrient pollution affecting habitat suitability for harmful algae. In:Glibert P M, Berdalet E, Burford M A, Pitcher G C, Zhou M J eds. Global Ecology and Oceanography of Harmful Algal Blooms. Cham:Springer. p.53-76.
Glibert P M, Burkholder J A M, Kana T M, Alexander J, Skelton H, Shilling C. 2009. Grazing by Karenia brevis on Synechococcus enhances its growth rate and may help to sustain blooms. Aquatic Microbial Ecology, 55(1):17-30,
Glibert P M, Maranger R, Sobota D J, Bouwman L. 2014. The Haber Bosch-harmful algal bloom (HB-HAB) link.Environmental Research Letters, 9(10):105001,
Gobler C J, Sunda W G. 2012. Ecosystem disruptive algal blooms of the brown tide species, Aureococcus anophagefferens and Aureoumbra lagunensis. Harmful Algae, 14:36-45,
Gómez F, Boicenco L. 2004. An annotated checklist of dinoflagellates in the Black Sea. Hydrobiologia, 517(1-3):43-59,
Granéli E, Hansen P J. 2006. Allelopathy in harmful algae:a mechanism to compete for resources? In:Granéli E, Turner J T eds. Ecology of Harmful Algae. Berlin, Heidelberg:Springer-Verlag. p.189-201.
Granéli E, Johansson N. 2003. Increase in the production of allelopathic substances by Prymnesium parvum cells grown under N- or P-deficient conditions. Harmful Algae, 2(2):135-145,
Granéli E, Salomon P S. 2010. Factors influencing allelopathy and toxicity in Prymnesium parvum. JAWRA Journal of the American Water Resources Association, 46(1):108-120,
Guillard R R L. 1975. Culture of phytoplankton for feeding marine invertebrates. In:Smith W L, Chanley M H eds.Culture of Marine Invertebrate Animals. Boston:Springer.p.29-60.
Hakanen P, Suikkanen S, Kremp A. 2014. Allelopathic activity of the toxic dinoflagellate Alexandrium ostenfeldii:intrapopulation variability and response of co-occurring dinoflagellates. Harmful Algae, 39:287-294,
Hallegraeff G M. 1992. Harmful algal blooms in the Australian region. Marine Pollution Bulletin, 25(5-8):186-190,
Hallegraeff G M. 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms:a formidable predictive challenge. Journal of Phycology, 46(2):220-235,
Hansen P J, Hjorth M. 2002. Growth and grazing responses of Chrysochromulina ericina (Prymnesiophyceae):the role of irradiance, prey concentration and pH. Marine Biology, 141(5):975-983,
Harper Jr D E, Guillen G. 1989. Occurrence of a dinoflagellate bloom associated with an influx of low salinity water at Galveston, Texas, and coincident mortalities of demersal fish and benthic invertebrates. Contributions in Marine Science, 31:147-161.
Hattenrath-Lehmann T K, Gobler C J. 2011. Allelopathic inhibition of competing phytoplankton by North American strains of the toxic dinoflagellate, Alexandrium fundyense:evidence from field experiments, laboratory experiments, and bloom events. Harmful Algae, 11:106-116.
Heisler J, Glibert P M, Burkholder J M, Anderson D M, Cochlan W, Dennison W C, Dortch Q, Gobler C J, Heil C A, Humphries E, Lewitus A, Magnien R, Marshall H G, Sellner K, Stockwell D A, Stoecker D K, Suddleson M. 2008. Eutrophication and harmful algal blooms:a scientific consensus. Harmful Algae, 8(1):3-13,
Higman W A, Stone D M, Lewis J M. 2001. Sequence comparisons of toxic and non-toxic Alexandrium tamarense (Dinophyceae) isolates from UK waters.Phycologia, 40(3):256-262,
Hodgkiss I J, Lu S H. 2004. The effects of nutrients and their ratios on phytoplankton abundance in Junk Bay, Hong Kong. Hydrobiologia, 512(1-3):215-229,
Horner R A, Garrison D L, Plumley F G. 1997. Harmful algal blooms and red tide problems on the U.S. west coast.Limnology and Oceanography, 42(5part2):1 076-1 088,
Jang S H, Jeong H J, Kwon J E, Lee K H. 2017. Mixotrophy in the newly described dinoflagellate Yihiella yeosuensis:a small, fast dinoflagellate predator that grows mixotrophically, but not autotrophically. Harmful Algae, 62:94-103,
Jeong H J, Du Yoo Y, Kim J S, Kim T H, Kim J H, Kang N S, Yih W. 2004. Mixotrophy in the phototrophic Harmful Alga Cochlodinium polykrikoides (Dinophycean):prey species, the effects of prey concentration, and grazing impact. Journal of Eukaryotic Microbiology, 51(5):563-569,
Jeong H J, Du Yoo Y, Seong K A, Kim J H, Park J Y, Kim S, Lee S H, Ha J H. 2005a. Feeding by the mixotrophic redtide dinoflagellate Gonyaulax polygramma:mechanisms, prey species, effects of prey concentration, and grazing impact. Aquatic Microbial Ecology, 38(3):249-257,
Jeong H J, Ok J H, Lim A S, Kwon J E, Kim S J, Lee S Y. 2016.Mixotrophy in the phototrophic dinoflagellate Takayama helix (family Kareniaceae):predator of diverse toxic and harmful dinoflagellates. Harmful Algae, 60:92-106,
Jeong H J, Park J Y, Nho J H, Park M O, Ha J H, Seong K A, Jeng C, Seong C N, Lee K Y, Yih W H. 2005b. Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquatic Microbial Ecology, 41(2):131-143,
Jessup D A, Miller M A, Ryan J P, Nevins H M, Kerkering H A, Mekebri A, Crane D B, Johnson T A, Kudela R M. 2009. Mass stranding of marine birds caused by a surfactant-producing red tide. PLoS One, 4(2):e4550,
Kahru M, Michell B G, Diaz A, Miura M. 2004. MODIS detects a devastating algal bloom in Paracas Bay, Peru. Eos, 85(45):465-472,
Katano T, Yoshida M, Yamaguchi S, Hamada T, Yoshino K, Hayami Y. 2011. Diel vertical migration and cell division of bloom-forming dinoflagellate Akashiwo sanguinea in the Ariake Sea, Japan. Plankton and Benthos Research, 6(2):92-100,
Kim J H, Jeong H J, Lim A S, Rho J R, Lee S B. 2016. Killing potential protist predators as a survival strategy of the newly described dinoflagellate Alexandrium pohangense.Harmful Algae, 55:41-55,
Kubanek J, Hicks M K, Naar J, Villareal T A. 2005. Does the red tide dinoflagellate Karenia brevis use allelopathy to outcompete other phytoplankton? Limnology and Oceanography, 50(3):883-895,
Legrand C, Rengefors K, Fistarol G O, Granéli E. 2003.Allelopathy in phytoplankton-biochemical, ecological and evolutionary aspects. Phycologia, 42(4):406-419,
Leong S C Y, Murata A, Nagashima Y, Taguchi S. 2004.Variability in toxicity of the dinoflagellate Alexandrium tamarense in response to different nitrogen sources and concentrations. Toxicon, 43(4):407-415,
Lim A S, Jeong H J, Ok J H, Kim S J. 2018. Feeding by the harmful phototrophic dinoflagellate Takayama tasmanica(Family Kareniaceae). Harmful Algae, 74:19-29,
Matsubara T, Nagasoe S, Yamasaki Y, Shikata T, Shimasaki Y, Oshima Y, Honjo T. 2007. Effects of temperature, salinity, and irradiance on the growth of the dinoflagellate Akashiwo sanguinea. Journal of Experimental Marine Biology and Ecology, 342(2):226-230,
Matsuoka K, Cho H J, Jacobson D M. 2000. Observations of the feeding behavior and growth rates of the heterotrophic dinoflagellate Polykrikos kofoidii (Polykrikaceae, Dinophyceae). Phycologia, 39(1):82-86,
Ok J H, Jeong H J, Lim A S, Lee K H. 2017. Interactions between the mixotrophic dinoflagellate Takayama helix and common heterotrophic protists. Harmful Algae, 68:178-191,
Ou G Y, Wang H, Si R R, Guan W C. 2017. The dinoflagellate Akashiwo sanguinea will benefit from future climate change:the interactive effects of ocean acidification, warming and high irradiance on photophysiology and hemolytic activity. Harmful Algae, 68:118-127,
Park J, Jeong H J, Du Yoo Y et al. 2013. Mixotrophic dinoflagellate red tides in Korean waters:distribution and ecophysiology. Harmful Algae, 30(S1):S28-S40,
Phlips E J, Badylak S, Christman M, Wolny J, Brame J, Garland J, Hall L, Hart J, Landsberg J, Lasi M, Lockwood J, Paperno R, Scheidt D, Staples A, Steidinger K. 2011.Scales of temporal and spatial variability in the distribution of harmful algae species in the Indian River Lagoon, Florida, USA. Harmful Algae, 10(3):277-290,
Poulin R X, Hogan S, Poulson-Ellestad K L, Brown E, Fernández F M, Kubanek J. 2018. Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors. Scientific Reports, 8(1):9 572,
Prince E K, Myers T L, Kubanek J. 2008. Effects of harmful algal blooms on competitors:allelopathic mechanisms of the red tide dinoflagellate Karenia brevis. Limnology and Oceanography, 53(2):531-541,
Remmel E J, Hambright K D. 2012. Toxin-assisted micropredation:experimental evidence shows that contact micropredation rather than exotoxicity is the role of Prymnesium toxins. Ecology Letters, 15(2):126-132,
Skovgaard A, Hansen P J. 2003. Food uptake in the harmful alga Prymnesium parvum mediated by excreted toxins.Limnology and Oceanography, 48(3):1 161-1 166,
Tang Y Z, Gobler C J. 2010. Allelopathic effects of Cochlodinium polykrikoides isolates and blooms from the estuaries of Long Island, New York, on co-occurring phytoplankton. Marine Ecology Progress, 406:19-31,
Tang Y Z, Gobler C J. 2015. Sexual resting cyst production by the dinoflagellate Akashiwo sanguinea:a potential mechanism contributing to the ubiquitous distribution of a harmful alga. Journal of Phycology, 51(2):298-309,
Williamson G B, Richardson D. 1988. Bioassays for allelopathy:measuring treatment responses with independent controls. Journal of Chemical Ecology, 14(1):181-187,
Xu N, Tang Y Z, Qin J L, Duan S S, Gobler C J. 2015. Ability of the marine diatoms Pseudo-nitzschia multiseries and P. pungens to inhibit the growth of co-occurring phytoplankton via allelopathy. Aquatic Microbial Ecology, 74(1):29-41,
Xu N, Wang M, Tang Y Z, Zhang Q, Duan S S, Gobler C J. 2017. Acute toxicity of the cosmopolitan bloom-forming dinoflagellate Akashiwo sanguinea to finfish, shellfish, and zooplankton. Aquatic Microbial Ecology, 80(3):209-222,
Yang C Y, Li Y, Zhou Y Y, Zheng W, Tian Y, Zheng T L. 2012.Bacterial community dynamics during a bloom caused by Akashiwo sanguinea in the Xiamen sea area, China.Harmful Algae, 20:132-141,
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