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12 - Trait Trade-Offs in Mixoplankton: An Analysis

from Part II - Physiology of Photosynthetic Autotrophs in Present-Day Environments

Published online by Cambridge University Press:  24 October 2024

By
Aditee Mitra ,
Kevin J. Flynn ,
Diane Stoecker  and
John A. Raven
Edited by
Mario Giordano ,
John Beardall ,
John A. Raven  and
Stephen C. Maberly
Mario Giordano
Affiliation:
Università degli Studi di Ancona, Italy
John Beardall
Affiliation:
Monash University, Victoria
John A. Raven
Affiliation:
University of Dundee
Stephen C. Maberly
Affiliation:
UK Centre for Ecology & Hydrology, Lancaster
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Summary

Mixoplankton are planktonic protists engaging in photo-autotrophy plus osmo-heterotrophy plus phago-heterotrophy, contrasting with non-phagotrophic phytoplankton (e.g., diatoms) and non-phototrophic zooplankton (e.g., tintinnids). All mixoplankton are mixotrophs, but not all mixotrophs are mixoplanktonic. Mixoplankton are often considered as inferior in their capabilities compared to diatoms that surrendered phagotrophy, and those zooplankton that lost phototrophy. However, such views undersell the synergistic activities of mixoplankton. Thus, the phototrophic capacity of mixoplankton provides a predatory phagotroph with a ready source of carbon and energy supplementing phagotrophy and retention of the 30% of resources that would otherwise have to be released in specific dynamic action. Phagotrophy brings in nutrients to support phototrophy. Beyond these generalisations, we know little about the whole integrated physiology and ecology of mixoplankton. To fully appreciate the comparative fitness of two species, we need to consider all aspects of their life cycles. The emphasis for plankton is usually placed on resource acquisition and the maximum specific growth rate without considering the metabolic and mortality costs of being unable to support the growth rate, and predatory pressures. This suggests that trait trade-offs are less useful for conceptual and simulation modelling than approaches more securely founded in physiology and evolution.

Keywords

grazinggrowth ratemixotrophyosmotrophyphagotrophyphoto-osmo-phago-trophyphototrophyphytoplanktonsurvivaltrait trade-offszooplankton
Type
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Information
Evolutionary Physiology of Algae and Aquatic Plants , pp. 227 - 251
Publisher: Cambridge University Press
Print publication year: 2024

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References

Adl, S. M., Simpson, A. G., Lane, C. E. et al. (2012). The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59: 429–514.CrossRefGoogle ScholarPubMed
Adolf, J. E., Stoecker, D. K. & Harding, Jr. L. W. (2003). Autotrophic growth and photoacclimation in Karlodinium micrum (Dinophyceae) and Storeatula major (Cryptophyceae). Journal of Phycology 39: 1101–1108.CrossRefGoogle Scholar
Adolf, J. E., Stoecker, D. K. & Harding, Jr. L. W. (2006). The balance of autotrophy and heterotrophy during mixotrophic growth of Karlodinium micrum (Dinophyceae). Journal of Plankton Research 28: 737–751.CrossRefGoogle Scholar
Altenburger, A., Cai, H., Li, Q. et al. (2021). Limits to the cellular control of sequestered cryptophyte prey in the marine ciliate Mesodinium rubrum. The ISME Journal 15: 1056–1072.CrossRefGoogle Scholar
Andersen, K. H., Berge, T., Gonçalves, R. J. et al. (2016). Characteristic sizes of life in the oceans, from bacteria to whales. Annual Review of Marine Science 8: 217–241.CrossRefGoogle ScholarPubMed
Anschütz, A. A. & Flynn, K. J. (2020). Niche separation between different functional types of mixoplankton: Results from NPZ-style N-based model simulations. Marine Biology 167: 1–21.CrossRefGoogle Scholar
Avrahami, Y. & Frada, M. J. (2020). Detection of phagotrophy in the marine phytoplankton group of the coccolithophores (Calcihaptophycidae, Haptophyta) during nutrient-replete and phosphate-limited growth. Journal of Phycology 56: 1103–1108.CrossRefGoogle ScholarPubMed
Behrenfeld, M. J., Halsey, K. H., Boss, E. et al. (2021). Thoughts on the evolution and ecological niche of diatoms. Ecological Monographs 91: e01457.CrossRefGoogle Scholar
Biard, T., Stemmann, L., Picheral, M. et al. (2016). In situ imaging reveals the biomass of giant protists in the global ocean. Nature 532: 504–507.CrossRefGoogle ScholarPubMed
Biddanda, B. & Benner, R. (1997). Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton. Limnology and Oceanography 42: 506–518.CrossRefGoogle Scholar
Blossom, H. E. & Hansen, P. J. (2021). The loss of mixotrophy in Alexandrium pseudogonyaulax: Implications for trade-offs between toxicity, mucus trap production, and phagotrophy. Limnology and Oceanography 66: 528–542.CrossRefGoogle Scholar
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: 77–93.CrossRefGoogle Scholar
Caron, D. A., Porter, K. G. & Sanders, R. W. (1990). Carbon, nitrogen, and phosphorus budgets for the mixotrophic phytoflagellate Poterioochromonas malhamensis (Chrysophyceae) during bacterial ingestion. Limnology and Oceanography 35: 433–443.CrossRefGoogle Scholar
Charalampous, E., Matthiessen, B. & Sommer, U. (2018). Light effects on phytoplankton morphometric traits influence nutrient utilization ability. Journal of Plankton Research 40: 568–579.CrossRefGoogle Scholar
Clark, D. R., Flynn, K. J. & Owens, N. J. P. (2002). The large capacity for dark nitrate-assimilation in diatoms may overcome nitrate limitation of growth. New Phytologist 155: 101–108.CrossRefGoogle ScholarPubMed
Crawford, D. W. (1989). Mesodinium rubrum: The phytoplankter that wasn’t. Marine Ecology Progress Series 79: 259–265.CrossRefGoogle Scholar
Crawford, D. W. & Purdie, D. A. (1992). Evidence for avoidance of flushing from an estuary by a planktonic, phototrophic ciliate. Marine Ecology Progress Series 79: 259–265.CrossRefGoogle Scholar
Davison, I. R. (1991). Environmental effects on algal photosynthesis: Temperature. Journal of Phycology 27: 2–8.CrossRefGoogle Scholar
de Castro, F., Gaedke, U. & Boenigk, J. (2009). Reverse evolution: Driving forces behind the loss of acquired photosynthetic traits. PLOS ONE 4: e8465.CrossRefGoogle ScholarPubMed
de Figueiredo, G. M., Nash, R. D. & Montagnes, D. J. (2007). Do protozoa contribute significantly to the diet of larval fish in the Irish Sea? Journal of the Marine Biological Association of the United Kingdom 87: 843–850.CrossRefGoogle Scholar
de Vries, J. & Gould, S. B. (2018). The monoplastidic bottleneck in algae and plant evolution. Journal of Cell Science 131: jcs203414.CrossRefGoogle ScholarPubMed
Dolan, J. R. & Pérez, M. T. (2000). Costs, benefits and characteristics of mixotrophy in marine oligotrichs. Freshwater Biology 45: 227–238.CrossRefGoogle Scholar
Edwards, K. F., Thomas, M. K., Klausmeier, C. A. et al. (2012). Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton. Limnology and Oceanography 57: 554–566.CrossRefGoogle Scholar
Ehrlich, E., Kath, N. J. & Gaedke, U. (2020). The shape of a defense-growth trade-off governs seasonal trait dynamics in natural phytoplankton. The ISME Journal 14: 1451–1462.CrossRefGoogle ScholarPubMed
Esteban, G. F., Fenchel, T. & Finlay, B. J. (2010). Mixotrophy in ciliates. Protist 161: 621–641.CrossRefGoogle ScholarPubMed
Fenchel, T. & Hansen, P. J. (2006). Motile behaviour of the bloom-forming ciliate Mesodinium rubrum. Marine Biology Research 2: 33–40.CrossRefGoogle Scholar
Flynn, K. J. (2009). Going for the slow burn: Why should possession of a low maximum growth rate be advantageous for microalgae? Plant Ecology and Diversity 2: 179–189.CrossRefGoogle Scholar
Flynn, K. J. & Berry, L. S. (1999). The loss of organic nitrogen during marine primary production may be overestimated significantly when estimated using 15N substrates. Proceedings of the Royal Society of London. Series B: Biological Sciences 266: 641–647.Google Scholar
Flynn, K. J. & Hansen, P. J. (2013). Cutting the canopy to defeat the ‘selfish gene’; conflicting selection pressures for the integration of phototrophy in mixotrophic protists. Protist 164: 811–823.CrossRefGoogle ScholarPubMed
Flynn, K. J. & Skibinski, D. O. (2020). Exploring evolution of maximum growth rates in plankton. Journal of Plankton Research 42: 497–513.CrossRefGoogle ScholarPubMed
Flynn, K. J. & Hipkin, C. R. (1999). Interactions between iron, light, ammonium, and nitrate: Insights from the construction of a dynamic model of algal physiology. Journal of Phycology 35: 1171–1190.CrossRefGoogle Scholar
Flynn, K. J. & Mitra, A. (2016). Why plankton modelers should reconsider using rectangular hyperbolic (Michaelis-Menten, Monod) descriptions of predator-prey interactions. Frontiers in Marine Science 3: 165.CrossRefGoogle Scholar
Flynn, K. J. & Skibinski, D. O. F., (2020). Exploring evolution of maximum growth rates in plankton. Journal of Plankton Research 42: 497–513.CrossRefGoogle ScholarPubMed
Flynn, K. J., Blackford, J. C., Baird, M. E. et al. (2012). Changes in pH at the exterior surface of plankton with ocean acidification. Nature Climate Change 2: 510–513.CrossRefGoogle Scholar
Flynn, K. J., Stoecker, D. K., Mitra, A. et al. (2013). Misuse of the phytoplankton–zooplankton dichotomy: The need to assign organisms as mixotrophs within plankton functional types. Journal of Plankton Research 35: 3–11.CrossRefGoogle Scholar
Flynn, K. J., St. John, M., Raven, J. A. et al. (2015a). Acclimation, adaptation, traits and trade-offs in plankton functional type models: Reconciling terminology for biology and modelling. Journal Plankton Research 37: 683–691.CrossRefGoogle Scholar
Flynn, K. J., Clark, D. R., Mitra, A. et al. (2015b). Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession. Proceedings of the Royal Society of London. Series B: Biological Sciences 282: 20142604.CrossRefGoogle Scholar
Flynn, K. J., Skibinski, D. O. F. & Lindemann, C. (2018). Effects of growth rate, cell size, motion, and elemental stoichiometry on nutrient transport kinetics. PLOS Computational Biology 14: e1006118.CrossRefGoogle ScholarPubMed
Flynn, K. J., Mitra, A., Anestis, K. et al. (2019). Mixotrophic protists and a new paradigm for marine ecology: Where does plankton research go now? Journal of Plankton Research 41: 375–391.CrossRefGoogle Scholar
Flynn, K. J., Kimmance, S. A., Clark, D. R. et al. (2021) Modelling the effects of traits and abiotic factors on viral lysis in phytoplankton. Frontiers in Marine Science 8: 667184.CrossRefGoogle Scholar
Fogg, G. E. (1991). The phytoplanktonic ways of life. New Phytologist 118: 191–232.CrossRefGoogle ScholarPubMed
Gavelis, G. S., Wakeman, K. C., Tillmann, U. et al. (2017). Microbial arms race: Ballistic ‘nematocysts’ in dinoflagellates represent a new extreme in organelle complexity. Science Advances 3: e1602552.CrossRefGoogle ScholarPubMed
Glibert, P. M. (2016). Margalef revisited: A new phytoplankton mandala incorporating twelve dimensions, including nutritional physiology. Harmful Algae 55: 25–30.CrossRefGoogle ScholarPubMed
Glibert, P. M. & Mitra, A. (2022). From webs, loops, shunts, and pumps to microbial multitasking: Evolving concepts of marine microbial ecology, the mixoplankton paradigm, and implications for a future ocean. Limnology and Oceanography 67: 585–597.CrossRefGoogle Scholar
Gómez-Consarnau, L., Raven, J. A., Levine, N. M. et al. (2019). Microbial rhodopsins are major contributors to the solar energy captured in the sea. Science Advances 5: eaaw8855.CrossRefGoogle Scholar
Granéli, E. & Flynn, K. J. (2006). Chemical and physical factors influencing toxin production. In Granéli, E. & Turner, J. T. (eds.) Ecology of Harmful Algae, Springer-Verlag, Berlin, 189, pp. 229–241.CrossRefGoogle Scholar
Hansen, P. J. (2002). Effect of high pH on the growth and survival of marine phytoplankton: Implications for species succession. Aquatic Microbial Ecology 28: 279–288.CrossRefGoogle Scholar
Hansen, P. J., Skovgaard, A., Glud, R. N. et al. (2000). Physiology of the mixotrophic dinoflagellate Fragilidium subglobosum. II. Effects of time scale and prey concentration on photosynthetic performance. Marine Ecology Progress Series 201: 137–146.CrossRefGoogle Scholar
Hartmann, M., Grob, C., Tarran, G. A. et al. (2012). Mixotrophic basis of Atlantic oligotrophic ecosystems. Proceedings of the National Academy of Sciences USA 109: 5756–5760.Google Scholar
Hausmann, K. (2002). Food acquisition, food ingestion and food digestion by protists. Japanese Journal of Protozoology 35: 85–95.Google Scholar
Hughes, E. A., Maselli, M., Sørensen, H. et al. (2021). Metabolic reliance on photosynthesis depends on both irradiance and prey availability in the mixotrophic ciliate, Strombidium cf. basimorphum. Frontiers in Microbiology 12: 642600.CrossRefGoogle ScholarPubMed
Jeong, H. J., Du Yoo, Y., Kim, J. S. et al. (2010). Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Science Journal 45: 65–91.CrossRefGoogle Scholar
Jiang, H. & Johnson, M. D. (2017). Jumping and overcoming diffusion limitation of nutrient uptake in the photosynthetic ciliate Mesodinium rubrum. Limnology and Oceanography 62: 421–436.CrossRefGoogle Scholar
John, E. H. & Flynn, K. J. (2002). Modelling changes in paralytic shellfish toxin content of dinoflagellates in response to nitrogen and phosphorus supply. Marine Ecology Progress Series 225: 147–160.CrossRefGoogle Scholar
Johnson, M. D. (2011). The acquisition of phototropy: Adaptive strategies of hosting endosymbionts and organelles. Photosynthesis Research 107: 117–132.CrossRefGoogle Scholar
Johnson, M. D. & Stoecker, D. K. (2005). The role of feeding in growth and the photophysiology of Myrionecta rubra. Aquatic Microbial Ecology 39: 303–312.CrossRefGoogle Scholar
Johnson, P. W., Donaghay, P. L., Small, E. B. et al. (1995). Ultrastructure and ecology of Perispira ovum (Ciliophora, Litostomatea) an aerobic, planktonic ciliate that sequesters the chloroplasts, mitochrondria, and paramylon of Euglenia proxima in a micro-oxic habitat. Journal of Eukaryotic Microbiology 42: 323–335.CrossRefGoogle Scholar
Johnson, M. D., Stoecker, D. K., Tengs, T. et al. (2006). Sequestration and performance of cryptophyte plastids in Myrionecta rubra. Journal of Phycology 42: 1236–1246.CrossRefGoogle Scholar
Johnson, M. D., Beaudoin, D. J., Frada, M. J. et al. (2018). High grazing rates on cryptophyte algae in Chesapeake Bay. Frontiers in Marine Science 5: 241.CrossRefGoogle Scholar
Keeling, P. J., Burki, F., Wilcox, H. M. et al. (2014). The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLOS Biology 12: e1001889.CrossRefGoogle ScholarPubMed
Kemp, A. E. & Villareal, T. A. (2018). The case of the diatoms and the muddled mandalas: Time to recognize diatom adaptations to stratified waters. Progress in Oceanography 167: 138–149.CrossRefGoogle Scholar
Kim, G. H., Han, J. H., Kim, B. et al. (2016). Cryptophyte gene regulation in the kleptoplastidic, karyokleptic ciliate Mesodinium rubrum. Harmful Algae 52: 23–33.CrossRefGoogle ScholarPubMed
Lee, K. H., Jeong, H. J., Jang, T. Y. et al. (2014). Feeding by the newly described mixotrophic dinoflagellate Gymnodinium smaydae: Feeding mechanism, prey species, and effect of prey concentration. Journal of Experimental Marine Biology and Ecology 459: 114–125.CrossRefGoogle Scholar
Leles, S. G., Mitra, A., Flynn, K. J. et al. (2017). Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance. Proceedings of the Royal Society of London. Series B: Biological Sciences 284: 20170664.Google Scholar
Leles, S. C., Mitra, A., Flynn, K. J. et al. (2019). Sampling bias misrepresents the biogeographic significance of constitutive mixotrophs across global oceans. Global Ecology and Biogeography 28: 418–428.CrossRefGoogle Scholar
Leles, S. G., Bruggeman, J., Polimene, L. et al. (2021). Differences in physiology explain succession of mixoplankton functional types and affect carbon fluxes in temperate seas. Progress in Oceanography 190: 102481.CrossRefGoogle Scholar
Li, A., Stoecker, D. K. & Adolf, J. E. (1999). Feeding, pigmentation, photosynthesis and growth of the mixotrophic dinoflagellate Gyrodinium galatheanum. Aquatic Microbial Ecology 19: 163–176.CrossRefGoogle Scholar
Litchman, E. & Klausmeier, C. A. (2008). Trait-based community ecology of phytoplankton. Annual Review of Ecology, Evolution and Systematics 39: 615–639.CrossRefGoogle Scholar
Litchman, E., Ohman, M. D. & Kiørboe, T. (2013). Trait-based approaches to zooplankton communities. Journal of Plankton Research 35: 473–484.CrossRefGoogle Scholar
Maberly, S. C., Ball, L. A., Raven, J. A. et al. (2009). Inorganic carbon acquisition by chrysophytes. Journal of Phycology 45: 1052–1061.CrossRefGoogle ScholarPubMed
Malviya, S., Scalco, E., Audic, S. et al. (2016). Insights into global diatom distribution and diversity in the world’s ocean. Proceedings of the National Academy of Sciences USA 113: E1516–E1525.Google Scholar
Margalef, R. (1978). Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanologia Acta 1: 493–509.Google Scholar
McCue, M. D. (2006). Specific dynamic action: A century of investigation. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 144: 381–394.CrossRefGoogle Scholar
McKie-Krisberg, Z. M., Gast, R. J. & Sanders, R. W. (2015). Physiological responses of three species of Antarctic mixotrophic phytoflagellates to changes in light and dissolved nutrients. Microbial Ecology 70: 21–29.CrossRefGoogle ScholarPubMed
McManus, G. B., Schoener, D. M. & Haberlandt, K. (2017). Chloroplast symbiosis in a marine ciliate: Ecophysiology and the risks and rewards of hosting foreign organelles. Frontiers in Microbiology 3: 321.Google Scholar
Millette, N. C., Pierson, J. J., Aceves, A. et al. (2017). Mixotrophy in Heterocapsa rotundata: A mechanism for dominating the winter phytoplankton. Limnology and Oceanography 62: 836–845.CrossRefGoogle Scholar
Mitra, A. & Flynn, K. J. (2006). Promotion of harmful algal blooms by zooplankton predatory activity. Biology Letters 2: 194–197.CrossRefGoogle ScholarPubMed
Mitra, A. & Flynn, K. J. (2010). Modelling mixotrophy in harmful algal blooms: More or less the sum of the parts? Journal of Marine Systems 83: 158–169.CrossRefGoogle Scholar
Mitra, A. & Flynn, K. J. (2021). HABs and the mixoplankton paradigm. Harmful Algae News 67: 4–6.Google Scholar
Mitra, A. & Flynn, K. J. (2023). Low rates of bacterivory enhances phototrophy and competitive advantage for mixoplankton growing in oligotrophic waters. Scientific Reports 13: 6900.Google Scholar
Mitra, A., Flynn, K. J., Burkholder, J. M. et al. (2014). The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11: 995–1005.CrossRefGoogle Scholar
Mitra, A., Flynn, K. J., Tillmann, U. et al. (2016). Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition; incorporation of diverse mixotrophic strategies. Protist 167: 106–120.CrossRefGoogle ScholarPubMed
Mitra, A., Caron, D. A., Faure, E. et al. (2023a). The Mixoplankton Database – diversity of photo-phago-trophic plankton in form, function and distribution across the global ocean. Journal of Eukaryotic Microbiology 70: e12972. https://doi.org/10.1111/jeu.12972.CrossRefGoogle ScholarPubMed
Mitra, A., Caron, D. A., Faure, E. et al. (2023b). The Mixoplankton Database (MDB). Zenodo. https://doi.org/10.5281/zenodo.7560583.CrossRefGoogle Scholar
Moestrup, Ø., Akselmann-Cardella, R., Churro, C. et al. (eds.) (2021). IOC-UNESCO Taxonomic Reference List of Harmful Micro Algae. Accessed at www.marinespecies.org/hab on 2021–02–08. https://doi.org/10.14284/362.CrossRefGoogle Scholar
Nishitani, G. O. H., Nagai, S., Sakiyama, S. et al. (2008). Successful cultivation of the toxic dinoflagellate Dinophysis caudata (Dinophyceae). Plankton and Benthos Research 3: 78–85.CrossRefGoogle Scholar
Öpik, H. & Flynn, K. J. (1989). The digestive process of the dinoflagellate, Oxyrrhis marina Dujardin, feeding on the chlorophyte, Dunaliella primolecta Butcher: A combined study of ultrastructure and free amino acids. New Phytologist 113: 143–151.CrossRefGoogle Scholar
Pančić, M. & Kiørboe, T. (2018). Phytoplankton defence mechanisms: Traits and trade-offs. Biological Reviews 93: 1269–1303. https://doi.org/10.1111/brv.12395.CrossRefGoogle ScholarPubMed
Park, M. G., Kim, S., Kim, H. S. et al. (2006). First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquatic Microbial Ecology 45: 101–106.CrossRefGoogle Scholar
Park, J. S., Myung, G., Kim, H. S. et al. (2007). Growth responses of the marine photosynthetic ciliate Myrionecta rubra to different cryptomonad strains. Aquatic Microbial Ecology 48: 83–90.CrossRefGoogle Scholar
Pérez, M. T., Dolan, J. R. & Fukai, E. (1997). Planktonic oligotrich ciliates in the NW Mediterranean: Growth rates and consumption by copepods. Marine Ecology Progress Series 155: 89–101.CrossRefGoogle Scholar
Ponce-Toledo, R. I., Deschamps, P., López-García, P. et al. (2017). An early-branching freshwater cyanobacterium at the origin of plastids. Current Biology 27: 368–391.CrossRefGoogle ScholarPubMed
Princiotta, S. D., Smith, B. T. & Sanders, R. W. (2016). Temperature-dependent phagotrophy and phototrophy in a mixotrophic chrysophyte. Journal of Phycology 52: 432–440.CrossRefGoogle Scholar
Raven, J. A., Beardall, J., Flynn, K. J. et al. (2009). Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: Relation to Darwin’s insectivorous plants. Journal of Experimental Botany 60: 3975–3987.CrossRefGoogle ScholarPubMed
Raven, J. A., Suggett, D. J. & Giordano, M. (2020). Inorganic carbon concentrating mechanisms in free-living and symbiotic dinoflagellates and chromerids. Journal of Applied Phycology 56: 1377–1397.CrossRefGoogle ScholarPubMed
Rottberger, J., Gruber, A., Boenigk, J. et al. (2013). Influence of nutrients and light on autotrophic, mixotrophic and heterotrophic freshwater chrysophytes. Aquatic Microbial Ecology 71: 179–191.CrossRefGoogle Scholar
Sánchez-Baracaldo, P., Raven, J. A., Pisari, D. et al. (2017). Early photosynthetic eukaryotes inhabited low-salinity habitats. Proceedings of the National Academy of Sciences USA 114: E7737–E7745.Google Scholar
Sato, N. (2020). Complex origins of chloroplast membranes with photosynthetic machineries: Multiple transfers of genes from divergent organisms at different times or a single endosymbiotic event? Journal of Plant Research 133: 15–33.CrossRefGoogle ScholarPubMed
Schoener, D. M. & McManus, G. B. (2012). Plastid retention, use and replacement in a kleptoplastidic ciliate. Aquatic Microbial Ecology 67: 177–187.CrossRefGoogle Scholar
Silkin, V., Fedorov, A., Flynn, K. J. et al. (2021). Protoplasmic streaming of chloroplasts enables rapid photoacclimation in large diatoms. Journal of Plankton Research 43: 831–845.CrossRefGoogle Scholar
Sonntag, B., Summerer, M. & Sommaruga, R. (2011). Are freshwater mixotrophic ciliates less sensitive to solar ultraviolet radiation than heterotrophic ones? Journal of Eukaryotic Microbiology 58: 196–202.CrossRefGoogle ScholarPubMed
Stoecker, D. K. (1999). Mixotrophy among dinoflagellates. Journal of Eukaryotic Microbiology 46: 397–401.CrossRefGoogle Scholar
Stoecker, D. K., Silver, M. W. (1990). Replacement and aging of chloroplasts in Strombidium capitatum (Ciliata, Oligotrichida). Marine Biology 107: 491–502.CrossRefGoogle Scholar
Stoecker, D. K., Silver, M. W., Michaels, A. E. et al. (1988). Obligate mixotrophy in Laboea strobila, a ciliate which retains chloroplasts. Marine Biology 99: 415–423.CrossRefGoogle Scholar
Stoecker, D. K., Johnson, M. D., de Vargas, C. et al. (2009). Acquired phototrophy in aquatic protists. Aquatic Microbial Ecology 57: 279–310.CrossRefGoogle Scholar
Stoecker, D. K., Hansen, P. J., Caron, D. A. et al. (2017). Mixotrophy in the marine plankton. Annual Review of Marine Science 9: 311–335.CrossRefGoogle ScholarPubMed
Tillmann, U. (2003). Kill and eat your predator: A winning strategy of the planktonic flagellate Prymnesium parvum. Aquatic Microbial Ecology 32: 73–84.CrossRefGoogle Scholar
van der Meeren, T. & Naess, T. (1993). How does cod (Gadus morhua) cope with variability in feeding conditions during early larval stages? Marine Biology 116: 637–647.CrossRefGoogle Scholar
Ward, B. A. & Follows, M. J. (2016). Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. Proceedings of the National Academy of Sciences USA 113: 2958–2963.Google Scholar
Wetz, M. S. & Wheeler, P. A. (2007). Release of dissolved organic matter by coastal diatoms. Limnology and Oceanography 52:798–807.CrossRefGoogle Scholar
Yamasaki, Y., Nagasoe, S., Matsubara, T. et al. (2007). Allelopathic interactions between the bacillariophyte Skeletonema costatum and the raphidophyte Heterosigma akashiwo. Marine Ecology Progress Series 339: 83–92.CrossRefGoogle Scholar
Zubkov, M. V. & Tarran, G. A. (2008). High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455: 224–226.CrossRefGoogle ScholarPubMed

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