Mixotrophic lifestyle of the ichthyotoxic haptophyte, Prymnesium parvum, offered different sources of phosphorus

Many harmful algae are mixoplanktonic, i.e. they combine phototrophy and phagotrophy, and this ability may explain their ecological success, especially when environmental conditions are not optimal for autotrophic growth. In this study, laboratory experiments were conducted with the mixotrophic and...

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Published inHarmful algae Vol. 127; p. 102483
Main Authors Boucher, Clémence, Lacour, Thomas, Julie, André, Damien, Réveillon, Juel, Hansen Per, Francis, Mairet
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier 01.08.2023
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Abstract Many harmful algae are mixoplanktonic, i.e. they combine phototrophy and phagotrophy, and this ability may explain their ecological success, especially when environmental conditions are not optimal for autotrophic growth. In this study, laboratory experiments were conducted with the mixotrophic and ichthyotoxic haptophyte Prymnesium parvum (strain CCAP 946/6) to test the effects of phosphorus (P) sufficiency and deficiency on its growth rate, phagotrophic and lytic activities. P-deficient P. parvum cultures were grown without or with addition of P in the form of inorganic phosphorus (nutrients) and/or living algal prey (i.e. the cryptophyte Teleaulax amphioxeia). The ingestion rate of P. parvum and prey mortality rate were calculated using flow cytometry measurements based on pigment-derived-fluorescence to distinguish between prey, predators and digesting predators. The first aim of the study was to develop a method taking into account the rate of digestion, allowing the calculation of ingestion rates over a two-week period. Growth rates of P. parvum were higher in the treatments with live prey, irrespective of the concentration of inorganic P, and maximum growth rates were found when both inorganic and organic P in form of prey were added (0.79 ± 0.07 d ). In addition, the mortality rate of T. amphioxeia induced by lytic compounds was 0.2 ± 0.02 d in the P-deficient treatment, while no mortality was observed under P-sufficiency in the present experiments. This study also revealed the mortality due to cell lysis exceeded that of prey ingestion. Therefore, additional experiments were conducted with lysed prey cells. When grown with debris from prey cells, the mean growth rate of P. parvum was similar to monocultures without additions of prey debris (0.30 ± 0.1 vs. 0.38 ± 0.03 d ), suggesting that P. parvum is able to grow on prey debris, but not as fast as with live prey. These results provide the first quantitative evidence over two weeks of experiment that ingestion of organic P in the form of living prey and/or debris of prey plays an important role in P. parvum growth and may explain its ecological success in a nutrient-limited environments.
AbstractList Many harmful algae are mixoplanktonic, i.e. they combine phototrophy and phagotrophy, and this ability may explain their ecological success, especially when environmental conditions are not optimal for autotrophic growth. In this study, laboratory experiments were conducted with the mixotrophic and ichthyotoxic haptophyte Prymnesium parvum (strain CCAP 946/6) to test the effects of phosphorus (P) sufficiency and deficiency on its growth rate, phagotrophic and lytic activities. P-deficient P. parvum cultures were grown without or with addition of P in the form of inorganic phosphorus (nutrients) and/or living algal prey (i.e. the cryptophyte Teleaulax amphioxeia). The ingestion rate of P. parvum and prey mortality rate were calculated using flow cytometry measurements based on pigment-derived-fluorescence to distinguish between prey, predators and digesting predators. The first aim of the study was to develop a method taking into account the rate of digestion, allowing the calculation of ingestion rates over a two-week period. Growth rates of P. parvum were higher in the treatments with live prey, irrespective of the concentration of inorganic P, and maximum growth rates were found when both inorganic and organic P in form of prey were added (0.79 ± 0.07 d-1). In addition, the mortality rate of T. amphioxeia induced by lytic compounds was 0.2 ± 0.02 d-1 in the P-deficient treatment, while no mortality was observed under P-sufficiency in the present experiments. This study also revealed the mortality due to cell lysis exceeded that of prey ingestion. Therefore, additional experiments were conducted with lysed prey cells. When grown with debris from prey cells, the mean growth rate of P. parvum was similar to monocultures without additions of prey debris (0.30 ± 0.1 vs. 0.38 ± 0.03 d-1), suggesting that P. parvum is able to grow on prey debris, but not as fast as with live prey. These results provide the first quantitative evidence over two weeks of experiment that ingestion of organic P in the form of living prey and/or debris of prey plays an important role in P. parvum growth and may explain its ecological success in a nutrient-limited environments.
Many harmful algae are mixoplanktonic, i.e. they combine phototrophy and phagotrophy, and this ability may explain their ecological success, especially when environmental conditions are not optimal for autotrophic growth. In this study, laboratory experiments were conducted with the mixotrophic and ichthyotoxic haptophyte Prymnesium parvum (strain CCAP 946/6) to test the effects of phosphorus (P) sufficiency and deficiency on its growth rate, phagotrophic and lytic activities. P-deficient P. parvum cultures were grown without or with addition of P in the form of inorganic phosphorus (nutrients) and/or living algal prey (i.e. the cryptophyte Teleaulax amphioxeia). The ingestion rate of P. parvum and prey mortality rate were calculated using flow cytometry measurements based on pigment-derived-fluorescence to distinguish between prey, predators and digesting predators. The first aim of the study was to develop a method taking into account the rate of digestion, allowing the calculation of ingestion rates over a two-week period. Growth rates of P. parvum were higher in the treatments with live prey, irrespective of the concentration of inorganic P, and maximum growth rates were found when both inorganic and organic P in form of prey were added (0.79 ± 0.07 d ). In addition, the mortality rate of T. amphioxeia induced by lytic compounds was 0.2 ± 0.02 d in the P-deficient treatment, while no mortality was observed under P-sufficiency in the present experiments. This study also revealed the mortality due to cell lysis exceeded that of prey ingestion. Therefore, additional experiments were conducted with lysed prey cells. When grown with debris from prey cells, the mean growth rate of P. parvum was similar to monocultures without additions of prey debris (0.30 ± 0.1 vs. 0.38 ± 0.03 d ), suggesting that P. parvum is able to grow on prey debris, but not as fast as with live prey. These results provide the first quantitative evidence over two weeks of experiment that ingestion of organic P in the form of living prey and/or debris of prey plays an important role in P. parvum growth and may explain its ecological success in a nutrient-limited environments.
ArticleNumber 102483
Author Damien, Réveillon
Francis, Mairet
Juel, Hansen Per
Boucher, Clémence
Lacour, Thomas
Julie, André
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Cites_doi 10.1016/S0012-8252(00)00018-0
10.1016/j.hal.2008.08.010
10.3354/ame033191
10.1093/plankt/fbs062
10.1007/s10811-016-0835-2
10.22541/au.166427474.41023349/v1
10.1016/j.chemosphere.2020.127927
10.3354/meps327223
10.1111/ele.14172
10.1016/j.hal.2008.08.003
10.1111/j.1529-8817.2007.00323.x
10.4319/lo.2001.46.5.1208
10.3354/ame017167
10.1007/PL00001344
10.1016/j.hal.2013.11.006
10.1146/annurev-marine-010816-060617
10.1093/plankt/fbz008
10.1038/ismej.2013.132
10.1016/j.hal.2008.08.006
10.4319/lo.2003.48.3.1161
10.3389/fmars.2018.00157
10.1016/j.hal.2017.07.012
10.1073/pnas.1118179109
10.2216/i0031-8884-42-4-406.1
10.3354/meps105203
10.1590/s1679-87592017140706503
10.1016/j.hal.2009.08.007
10.1111/j.1752-1688.2009.00395.x
10.4319/lo.1993.38.2.0273
10.1016/j.protis.2016.01.003
10.1016/j.hal.2022.102203
10.3354/meps254049
10.1134/S0022093013040014
10.1080/00364827.1996.10413631
10.1016/S1568-9883(03)00006-4
10.3354/meps299137
10.1016/j.hal.2016.01.002
10.1016/j.hal.2011.01.005
10.1002/ecs2.3372
10.1016/j.marenvres.2022.105558
10.1016/j.toxicon.2010.02.017
10.1002/lol2.10294
10.3354/ame014155
10.1093/plankt/fbn114
10.1111/j.1752-1688.2009.00397.x
10.1017/S0030605322001387
10.1016/j.hal.2022.102173
10.1093/plankt/fbq082
10.1073/pnas.1814860116
10.1111/j.1752-1688.2009.00386.x
10.1111/jeu.12972
10.1007/BF02179768
10.5194/bg-11-995-2014
10.3354/meps255115
10.1007/s00248-006-9188-8
10.3354/ame038259
10.1093/plankt/fbq079
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Keywords Allelopathy
Flow cytometry
Phagotrophy
Prymnesium parvum
Mixotrophy
Ingestion rate
Language English
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References 10.1016/j.hal.2023.102483_bib0003
Baker (10.1016/j.hal.2023.102483_bib0004) 2007; 43
Henrikson (10.1016/j.hal.2023.102483_bib0032) 2010; 55
Edwards (10.1016/j.hal.2023.102483_bib0019) 2019; 116
Taylor (10.1016/j.hal.2023.102483_bib0058) 2021; 263
Nygaard (10.1016/j.hal.2023.102483_bib0050) 1993; 38
Cagle (10.1016/j.hal.2023.102483_bib0014) 2021; 12
Johnsen (10.1016/j.hal.2023.102483_bib0034) 2010; 46
Beardall (10.1016/j.hal.2023.102483_bib0006) 2001; 63
Flynn (10.1016/j.hal.2023.102483_bib0023) 2013; 35
Litchman (10.1016/j.hal.2023.102483_bib0039) 2023; 8
Granéli (10.1016/j.hal.2023.102483_bib0026) 2010; 46
Blossom (10.1016/j.hal.2023.102483_bib0009) 2014; 8
Fistarol (10.1016/j.hal.2023.102483_bib0021) 2003; 255
Bowers (10.1016/j.hal.2023.102483_bib0011) 2010; 46
Granéli (10.1016/j.hal.2023.102483_bib0025) 2003; 2
Granéli (10.1016/j.hal.2023.102483_bib0024) 2003; 254
Hambright (10.1016/j.hal.2023.102483_bib0028) 2015
Flynn (10.1016/j.hal.2023.102483_bib0022) 2018
Guevara (10.1016/j.hal.2023.102483_bib0027) 2016; 28
Adolf (10.1016/j.hal.2023.102483_bib0001) 2008; 8
Driscoll (10.1016/j.hal.2023.102483_bib0017) 2023; 26
Roelke (10.1016/j.hal.2023.102483_bib0053) 2011; 33
Matantseva (10.1016/j.hal.2023.102483_bib0043) 2013; 49
Ferreira (10.1016/j.hal.2023.102483_bib0020) 2022; 174
Martin-Cereceda (10.1016/j.hal.2023.102483_bib0042) 2003; 33
Lundgren (10.1016/j.hal.2023.102483_bib0040) 2016; 55
Uronen (10.1016/j.hal.2023.102483_bib0061) 2007; 54
Burkholder (10.1016/j.hal.2023.102483_bib0013) 2008; 8
Almada (10.1016/j.hal.2023.102483_bib0002) 2017; 65
Legrand (10.1016/j.hal.2023.102483_bib0036) 2001; 46
Brutemark (10.1016/j.hal.2023.102483_bib0012) 2011; 10
Carpenter (10.1016/j.hal.2023.102483_bib0015) 2018; 5
Smalley (10.1016/j.hal.2023.102483_bib0055) 1999; 17
James (10.1016/j.hal.2023.102483_bib0033) 2011; 33
Mitra (10.1016/j.hal.2023.102483_bib0046) 2023
Barreiro (10.1016/j.hal.2023.102483_bib0005) 2005; 38
Roelke (10.1016/j.hal.2023.102483_bib0052) 2016; 764
Yoo (10.1016/j.hal.2023.102483_bib0063) 2017; 68
Beisner (10.1016/j.hal.2023.102483_bib0007) 2019; 41
Harrison (10.1016/j.hal.2023.102483_bib0029) 1990; 2
Unrein (10.1016/j.hal.2023.102483_bib0060) 2014; 8
Pujo-Pay (10.1016/j.hal.2023.102483_bib0051) 1994; 105
Uronen (10.1016/j.hal.2023.102483_bib0062) 2005; 299
Marchowski (10.1016/j.hal.2023.102483_bib0041) 2023; 57
Stoecker (10.1016/j.hal.2023.102483_bib0057) 2017; 9
Hartmann (10.1016/j.hal.2023.102483_bib0030) 2012; 109
Medić (10.1016/j.hal.2023.102483_bib0044) 2022; 112
Benitez-Nelson (10.1016/j.hal.2023.102483_bib0008) 2000; 51
10.1016/j.hal.2023.102483_bib0010
Michaloudi (10.1016/j.hal.2023.102483_bib0045) 2008; 31
Skovgaard (10.1016/j.hal.2023.102483_bib0054) 2003; 48
Mitra (10.1016/j.hal.2023.102483_bib0048) 2016; 167
Li (10.1016/j.hal.2023.102483_bib0038) 2022; 113
Sopanen (10.1016/j.hal.2023.102483_bib0056) 2006; 327
Tillmann (10.1016/j.hal.2023.102483_bib0059) 1998; 14
Legrand (10.1016/j.hal.2023.102483_bib0037) 2003; 42
Carvalho (10.1016/j.hal.2023.102483_bib0016) 2010; 9
Heisler (10.1016/j.hal.2023.102483_bib0031) 2008; 8
Mitra (10.1016/j.hal.2023.102483_bib0047) 2014; 11
Nejstgaard (10.1016/j.hal.2023.102483_bib0049) 1996; 81
10.1016/j.hal.2023.102483_bib0018
Karl (10.1016/j.hal.2023.102483_bib0035) 2015
References_xml – volume: 51
  start-page: 109
  issue: 1–4
  year: 2000
  ident: 10.1016/j.hal.2023.102483_bib0008
  article-title: The biogeochemical cycling of phosphorus in marine systems
  publication-title: Earth-Sci. Rev.
  doi: 10.1016/S0012-8252(00)00018-0
  contributor:
    fullname: Benitez-Nelson
– volume: 8
  start-page: 77
  issue: 1
  year: 2008
  ident: 10.1016/j.hal.2023.102483_bib0013
  article-title: Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters
  publication-title: Harmful Algae
  doi: 10.1016/j.hal.2008.08.010
  contributor:
    fullname: Burkholder
– volume: 33
  start-page: 191
  year: 2003
  ident: 10.1016/j.hal.2023.102483_bib0042
  article-title: Grazing by Prymnesium parvum on small planktonic diatoms
  publication-title: Aquat. Microb. Ecol.
  doi: 10.3354/ame033191
  contributor:
    fullname: Martin-Cereceda
– volume: 35
  start-page: 3
  issue: 1
  year: 2013
  ident: 10.1016/j.hal.2023.102483_bib0023
  article-title: Misuse of the phytoplankton–zooplankton dichotomy : the need to assign organisms as mixotrophs within plankton functional types
  publication-title: J. Plankton Res.
  doi: 10.1093/plankt/fbs062
  contributor:
    fullname: Flynn
– volume: 28
  start-page: 2651
  issue: 5
  year: 2016
  ident: 10.1016/j.hal.2023.102483_bib0027
  article-title: Comparison of growth and biochemical parameters of two strains of Rhodomonas salina (Cryptophyceae) cultivated under different combinations of irradiance, temperature, and nutrients
  publication-title: J. Appl. Phycol.
  doi: 10.1007/s10811-016-0835-2
  contributor:
    fullname: Guevara
– ident: 10.1016/j.hal.2023.102483_bib0003
  doi: 10.22541/au.166427474.41023349/v1
– volume: 263
  year: 2021
  ident: 10.1016/j.hal.2023.102483_bib0058
  article-title: Sunlight concurrently reduces Prymnesium parvum elicited acute toxicity to fish and prymnesins
  publication-title: Chemosphere
  doi: 10.1016/j.chemosphere.2020.127927
  contributor:
    fullname: Taylor
– volume: 327
  start-page: 223
  year: 2006
  ident: 10.1016/j.hal.2023.102483_bib0056
  article-title: Toxic haptophyte Prymnesium parvum affects grazing, survival, egestion and egg production of the calanoid copepods Eurytemora affinis and Acartia bifilosa
  publication-title: Mar. Ecol. Prog. Ser.
  doi: 10.3354/meps327223
  contributor:
    fullname: Sopanen
– volume: 26
  start-page: 677
  issue: 5
  year: 2023
  ident: 10.1016/j.hal.2023.102483_bib0017
  article-title: Behavioural differences underlie toxicity and predation variation in blooms of Prymnesium parvum
  publication-title: Ecol. Lett.
  doi: 10.1111/ele.14172
  contributor:
    fullname: Driscoll
– volume: 8
  start-page: 119
  issue: 1
  year: 2008
  ident: 10.1016/j.hal.2023.102483_bib0001
  article-title: Can cryptophyte abundance trigger toxic Karlodinium veneficum blooms in eutrophic estuaries?
  publication-title: Harmful Algae
  doi: 10.1016/j.hal.2008.08.003
  contributor:
    fullname: Adolf
– volume: 43
  start-page: 219
  issue: 2
  year: 2007
  ident: 10.1016/j.hal.2023.102483_bib0004
  article-title: Growth and toxicity of Prymnesium Parvum (haptophyta) as a function of salinity, light, and temperature1
  publication-title: J. Phycol.
  doi: 10.1111/j.1529-8817.2007.00323.x
  contributor:
    fullname: Baker
– volume: 46
  start-page: 1208
  issue: 5
  year: 2001
  ident: 10.1016/j.hal.2023.102483_bib0036
  article-title: Phagotrophy and toxicity variation in the mixotrophic Prymnesium patelliferum (Haptophyceae)
  publication-title: Limnol. Oceanogr.
  doi: 10.4319/lo.2001.46.5.1208
  contributor:
    fullname: Legrand
– volume: 17
  start-page: 167
  year: 1999
  ident: 10.1016/j.hal.2023.102483_bib0055
  article-title: A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate Ceratium furca
  publication-title: Aquat. Microb. Ecol.
  doi: 10.3354/ame017167
  contributor:
    fullname: Smalley
– volume: 63
  start-page: 44
  issue: 1
  year: 2001
  ident: 10.1016/j.hal.2023.102483_bib0006
  article-title: Approaches for determining phytoplankton nutrient limitation
  publication-title: Aquat. Sci.
  doi: 10.1007/PL00001344
  contributor:
    fullname: Beardall
– ident: 10.1016/j.hal.2023.102483_bib0010
  doi: 10.1016/j.hal.2013.11.006
– volume: 9
  start-page: 311
  issue: 1
  year: 2017
  ident: 10.1016/j.hal.2023.102483_bib0057
  article-title: Mixotrophy in the marine plankton
  publication-title: Ann. Rev. Mar. Sci.
  doi: 10.1146/annurev-marine-010816-060617
  contributor:
    fullname: Stoecker
– volume: 41
  start-page: 77
  issue: 2
  year: 2019
  ident: 10.1016/j.hal.2023.102483_bib0007
  article-title: A guide to methods for estimating phago-mixotrophy in nanophytoplankton
  publication-title: J. Plankton Res.
  doi: 10.1093/plankt/fbz008
  contributor:
    fullname: Beisner
– volume: 8
  issue: 1
  year: 2014
  ident: 10.1016/j.hal.2023.102483_bib0060
  article-title: Mixotrophic haptophytes are key bacterial grazers in oligotrophic coastal waters
  publication-title: ISME J.
  doi: 10.1038/ismej.2013.132
  contributor:
    fullname: Unrein
– volume: 8
  start-page: 3
  issue: 1
  year: 2008
  ident: 10.1016/j.hal.2023.102483_bib0031
  article-title: Eutrophication and harmful algal blooms : a scientific consensus
  publication-title: Harmful Algae
  doi: 10.1016/j.hal.2008.08.006
  contributor:
    fullname: Heisler
– volume: 48
  start-page: 1161
  issue: 3
  year: 2003
  ident: 10.1016/j.hal.2023.102483_bib0054
  article-title: Food uptake in the harmful alga Prymnesium parvum mediated by excreted toxins
  publication-title: Limnol. Oceanogr.
  doi: 10.4319/lo.2003.48.3.1161
  contributor:
    fullname: Skovgaard
– volume: 5
  start-page: 157
  year: 2018
  ident: 10.1016/j.hal.2023.102483_bib0015
  article-title: Single-cell view of carbon and nitrogen acquisition in the mixotrophic alga Prymnesium parvum (Haptophyta) inferred from stable isotope tracers and NanoSIMS
  publication-title: Front. Mar. Sci.
  doi: 10.3389/fmars.2018.00157
  contributor:
    fullname: Carpenter
– volume: 764
  start-page: 2950
  issue: 1
  year: 2016
  ident: 10.1016/j.hal.2023.102483_bib0052
  article-title: A chronicle of a killer alga in the west : ecology, assessment, and management of Prymnesium parvum blooms
  publication-title: Hydrobiologia
  contributor:
    fullname: Roelke
– volume: 68
  start-page: 105
  year: 2017
  ident: 10.1016/j.hal.2023.102483_bib0063
  article-title: Mixotrophy in the marine red-tide cryptophyte Teleaulax amphioxeia and ingestion and grazing impact of cryptophytes on natural populations of bacteria in Korean coastal waters
  publication-title: Harmful Algae
  doi: 10.1016/j.hal.2017.07.012
  contributor:
    fullname: Yoo
– volume: 109
  start-page: 5756
  issue: 15
  year: 2012
  ident: 10.1016/j.hal.2023.102483_bib0030
  article-title: Mixotrophic basis of Atlantic oligotrophic ecosystems
  publication-title: Proc. Natl Acad. Sci.
  doi: 10.1073/pnas.1118179109
  contributor:
    fullname: Hartmann
– volume: 42
  start-page: 406
  issue: 4
  year: 2003
  ident: 10.1016/j.hal.2023.102483_bib0037
  article-title: Allelopathy in phytoplankton—biochemical, ecological and evolutionary aspects
  publication-title: Phycologia
  doi: 10.2216/i0031-8884-42-4-406.1
  contributor:
    fullname: Legrand
– volume: 105
  start-page: 203
  year: 1994
  ident: 10.1016/j.hal.2023.102483_bib0051
  article-title: Improvement of the wet-oxidation procedure for simultaneous determination of particulate organic nitrogen and phosphorus collected on filters
  publication-title: Mar. Ecol. Prog. Ser.
  doi: 10.3354/meps105203
  contributor:
    fullname: Pujo-Pay
– volume: 65
  start-page: 392
  issue: 3
  year: 2017
  ident: 10.1016/j.hal.2023.102483_bib0002
  article-title: Investigation of phagotrophy in natural assemblages of the benthic dinoflagellates Ostreopsis, Prorocentrum and Coolia
  publication-title: Braz. J.f Oceanogr.
  doi: 10.1590/s1679-87592017140706503
  contributor:
    fullname: Almada
– volume: 9
  start-page: 105
  issue: 1
  year: 2010
  ident: 10.1016/j.hal.2023.102483_bib0016
  article-title: Contribution of phagotrophy versus autotrophy to Prymnesium parvum growth under nitrogen and phosphorus sufficiency and deficiency
  publication-title: Harmful Algae
  doi: 10.1016/j.hal.2009.08.007
  contributor:
    fullname: Carvalho
– volume: 46
  start-page: 108
  issue: 1
  year: 2010
  ident: 10.1016/j.hal.2023.102483_bib0026
  article-title: Factors influencing allelopathy and toxicity in Prymnesium parvum1
  publication-title: JAWRA J. Am. Water Resour. Assoc.
  doi: 10.1111/j.1752-1688.2009.00395.x
  contributor:
    fullname: Granéli
– volume: 38
  start-page: 273
  issue: 2
  year: 1993
  ident: 10.1016/j.hal.2023.102483_bib0050
  article-title: Bacterivory in algae : a survival strategy during nutrient limitation
  publication-title: Limnol. Oceanogr.
  doi: 10.4319/lo.1993.38.2.0273
  contributor:
    fullname: Nygaard
– volume: 167
  start-page: 106
  issue: 2
  year: 2016
  ident: 10.1016/j.hal.2023.102483_bib0048
  article-title: Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition : incorporation of diverse mixotrophic strategies
  publication-title: Protist
  doi: 10.1016/j.protis.2016.01.003
  contributor:
    fullname: Mitra
– year: 2015
  ident: 10.1016/j.hal.2023.102483_bib0028
  article-title: Regulation of growth and toxicity of a mixotrophic microbe : implications for understanding range expansion in Prymnesium parvum
  publication-title: Freshwater Sci.
  contributor:
    fullname: Hambright
– volume: 113
  year: 2022
  ident: 10.1016/j.hal.2023.102483_bib0038
  article-title: A three-dimensional mixotrophic model of Karlodinium veneficum blooms for a eutrophic estuary
  publication-title: Harmful Algae
  doi: 10.1016/j.hal.2022.102203
  contributor:
    fullname: Li
– volume: 254
  start-page: 49
  year: 2003
  ident: 10.1016/j.hal.2023.102483_bib0024
  article-title: Effects of the toxic haptophyte Prymnesium parvum on the survival and feeding of a ciliate : the influence of different nutrient conditions
  publication-title: Mar. Ecol. Prog. Ser.
  doi: 10.3354/meps254049
  contributor:
    fullname: Granéli
– volume: 49
  start-page: 377
  issue: 4
  year: 2013
  ident: 10.1016/j.hal.2023.102483_bib0043
  article-title: Mixotrophy in microorganisms : ecological and cytophysiological aspects
  publication-title: J. Evol. Biochem. Physiol.
  doi: 10.1134/S0022093013040014
  contributor:
    fullname: Matantseva
– volume: 81
  start-page: 339
  issue: 4
  year: 1996
  ident: 10.1016/j.hal.2023.102483_bib0049
  article-title: Repression of copepod feeding and fecundity by the toxic haptophyte Prymnesium patelliferum
  publication-title: Sarsia
  doi: 10.1080/00364827.1996.10413631
  contributor:
    fullname: Nejstgaard
– volume: 2
  start-page: 135
  issue: 2
  year: 2003
  ident: 10.1016/j.hal.2023.102483_bib0025
  article-title: Increase in the production of allelopathic substances by Prymnesium parvum cells grown under N- or P-deficient conditions
  publication-title: Harmful Algae
  doi: 10.1016/S1568-9883(03)00006-4
  contributor:
    fullname: Granéli
– volume: 299
  start-page: 137
  year: 2005
  ident: 10.1016/j.hal.2023.102483_bib0062
  article-title: Haemolytic activity and allelopathy of the haptophyte Prymnesium parvum in nutrient-limited and balanced growth conditions
  publication-title: Mar. Ecol. Prog. Ser.
  doi: 10.3354/meps299137
  contributor:
    fullname: Uronen
– volume: 55
  start-page: 1
  year: 2016
  ident: 10.1016/j.hal.2023.102483_bib0040
  article-title: Metabolic and physiological changes in Prymnesium parvum when grown under, and grazing on prey of, variable nitrogen:phosphorus stoichiometry
  publication-title: Harmful Algae
  doi: 10.1016/j.hal.2016.01.002
  contributor:
    fullname: Lundgren
– volume: 10
  start-page: 388
  issue: 4
  year: 2011
  ident: 10.1016/j.hal.2023.102483_bib0012
  article-title: Role of mixotrophy and light for growth and survival of the toxic haptophyte Prymnesium parvum
  publication-title: Harmful Algae
  doi: 10.1016/j.hal.2011.01.005
  contributor:
    fullname: Brutemark
– volume: 12
  start-page: e03372
  issue: 2
  year: 2021
  ident: 10.1016/j.hal.2023.102483_bib0014
  article-title: Allelopathy and micropredation paradigms reconcile with system stoichiometry
  publication-title: Ecosphere
  doi: 10.1002/ecs2.3372
  contributor:
    fullname: Cagle
– volume: 174
  year: 2022
  ident: 10.1016/j.hal.2023.102483_bib0020
  article-title: The strengths and weaknesses of Live Fluorescently Labelled Algae (LFLA) to estimate herbivory in protozooplankton and mixoplankton
  publication-title: Mar. Environ. Res.
  doi: 10.1016/j.marenvres.2022.105558
  contributor:
    fullname: Ferreira
– volume: 55
  start-page: 1396
  issue: 7
  year: 2010
  ident: 10.1016/j.hal.2023.102483_bib0032
  article-title: Reassessing the ichthyotoxin profile of cultured Prymnesium parvum (golden algae) and comparing it to samples collected from recent freshwater bloom and fish kill events in North America
  publication-title: Toxicon
  doi: 10.1016/j.toxicon.2010.02.017
  contributor:
    fullname: Henrikson
– year: 2015
  ident: 10.1016/j.hal.2023.102483_bib0035
  article-title: Dynamics of dissolved organic phosphorus
  contributor:
    fullname: Karl
– volume: 8
  start-page: 229
  issue: 2
  year: 2023
  ident: 10.1016/j.hal.2023.102483_bib0039
  article-title: Understanding and predicting harmful algal blooms in a changing climate : a trait-based framework
  publication-title: Limnol. Oceanogr. Lett.
  doi: 10.1002/lol2.10294
  contributor:
    fullname: Litchman
– volume: 14
  start-page: 155
  issue: 2
  year: 1998
  ident: 10.1016/j.hal.2023.102483_bib0059
  article-title: Phagotrophy by a plastidic haptophyte, Prymnesium patelliferum
  publication-title: Aquat. Microb. Ecol.
  doi: 10.3354/ame014155
  contributor:
    fullname: Tillmann
– volume: 31
  start-page: 301
  issue: 3
  year: 2008
  ident: 10.1016/j.hal.2023.102483_bib0045
  article-title: Plankton community structure during an ecosystem disruptive algal bloom of Prymnesium parvum
  publication-title: J. Plankton Res.
  doi: 10.1093/plankt/fbn114
  contributor:
    fullname: Michaloudi
– volume: 46
  start-page: 133
  issue: 1
  year: 2010
  ident: 10.1016/j.hal.2023.102483_bib0011
  article-title: Combining flow cytometry and real-time PCR methodology to demonstrate consumption by Prymnesium parvum 1
  publication-title: JAWRA J. Am. Water Resour. Assoc.
  doi: 10.1111/j.1752-1688.2009.00397.x
  contributor:
    fullname: Bowers
– volume: 57
  issue: 1
  year: 2023
  ident: 10.1016/j.hal.2023.102483_bib0041
  article-title: Unprecedented mass mortality of aquatic organisms in the River Oder
  publication-title: Oryx
  doi: 10.1017/S0030605322001387
  contributor:
    fullname: Marchowski
– volume: 112
  year: 2022
  ident: 10.1016/j.hal.2023.102483_bib0044
  article-title: The coupling between irradiance, growth, photosynthesis and prymnesin cell quota and production in two strains of the bloom-forming haptophyte, Prymnesium parvum
  publication-title: Harmful Algae
  doi: 10.1016/j.hal.2022.102173
  contributor:
    fullname: Medić
– volume: 33
  start-page: 265
  issue: 2
  year: 2011
  ident: 10.1016/j.hal.2023.102483_bib0033
  article-title: Sunlight amelioration of Prymnesium parvum acute toxicity to fish
  publication-title: J. Plankton Res.
  doi: 10.1093/plankt/fbq082
  contributor:
    fullname: James
– volume: 116
  start-page: 6211
  issue: 13
  year: 2019
  ident: 10.1016/j.hal.2023.102483_bib0019
  article-title: Mixotrophy in nanoflagellates across environmental gradients in the ocean
  publication-title: Proc. Natl Acad. Sci.
  doi: 10.1073/pnas.1814860116
  contributor:
    fullname: Edwards
– ident: 10.1016/j.hal.2023.102483_bib0018
– volume: 46
  start-page: 6
  issue: 1
  year: 2010
  ident: 10.1016/j.hal.2023.102483_bib0034
  article-title: Prymnesium parvum : the Norwegian Experience1
  publication-title: JAWRA J. Am. Water Resour. Assoc.
  doi: 10.1111/j.1752-1688.2009.00386.x
  contributor:
    fullname: Johnsen
– start-page: e12972
  year: 2023
  ident: 10.1016/j.hal.2023.102483_bib0046
  article-title: The Mixoplankton Database (MDB) : diversity of photo-phago-trophic plankton in form, function, and distribution across the global ocean
  publication-title: J. Eukar. Microbiol.
  doi: 10.1111/jeu.12972
  contributor:
    fullname: Mitra
– volume: 2
  start-page: 45
  issue: 1
  year: 1990
  ident: 10.1016/j.hal.2023.102483_bib0029
  article-title: Effects of nutrient and light limitation on the biochemical composition of phytoplankton
  publication-title: J. Appl. Phycol.
  doi: 10.1007/BF02179768
  contributor:
    fullname: Harrison
– volume: 11
  issue: 4
  year: 2014
  ident: 10.1016/j.hal.2023.102483_bib0047
  article-title: The role of mixotrophic protists in the biological carbon pump
  publication-title: Biogeosciences
  doi: 10.5194/bg-11-995-2014
  contributor:
    fullname: Mitra
– volume: 255
  start-page: 115
  year: 2003
  ident: 10.1016/j.hal.2023.102483_bib0021
  article-title: Allelopathic effect of Prymnesium parvum on a natural plankton community
  publication-title: Mar. Ecol. Prog. Ser.
  doi: 10.3354/meps255115
  contributor:
    fullname: Fistarol
– volume: 54
  start-page: 183
  issue: 1
  year: 2007
  ident: 10.1016/j.hal.2023.102483_bib0061
  article-title: Allelopathic effects of toxic haptophyte prymnesium parvum lead to release of dissolved organic carbon and increase in bacterial biomass
  publication-title: Microb. Ecol.
  doi: 10.1007/s00248-006-9188-8
  contributor:
    fullname: Uronen
– volume: 38
  start-page: 259
  year: 2005
  ident: 10.1016/j.hal.2023.102483_bib0005
  article-title: Relative importance of the different negative effects of the toxic haptophyte Prymnesium parvum on Rhodomonas salina and Brachionus plicatilis
  publication-title: Aquat. Microb. Ecol.
  doi: 10.3354/ame038259
  contributor:
    fullname: Barreiro
– start-page: 113
  year: 2018
  ident: 10.1016/j.hal.2023.102483_bib0022
  article-title: Mixotrophy in harmful algal blooms : by whom, on whom, when, why, and what next
  contributor:
    fullname: Flynn
– volume: 8
  year: 2014
  ident: 10.1016/j.hal.2023.102483_bib0009
  article-title: Prymnesium parvum revisited : relationship between allelopathy, ichthyotoxicity, and chemical profiles in 5 strains
  publication-title: Aquat. Toxicol.
  contributor:
    fullname: Blossom
– volume: 33
  start-page: 243
  issue: 2
  year: 2011
  ident: 10.1016/j.hal.2023.102483_bib0053
  article-title: A decade of fish-killing Prymnesium parvum blooms in Texas : roles of inflow and salinity
  publication-title: J. Plankton Res.
  doi: 10.1093/plankt/fbq079
  contributor:
    fullname: Roelke
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SubjectTerms Autotrophic Processes
Cryptophyta
Haptophyta
Life Sciences
Phosphorus - pharmacology
Phototrophic Processes
Title Mixotrophic lifestyle of the ichthyotoxic haptophyte, Prymnesium parvum, offered different sources of phosphorus
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