Environment-dependent metabolic investments in the mixotrophic chrysophyte Ochromonas.
metabolism
mixoplankton
phagotrophy
photoacclimation
photosynthesis
plasticity
tradeoffs
Journal
Journal of phycology
ISSN: 1529-8817
Titre abrégé: J Phycol
Pays: United States
ID NLM: 9882935
Informations de publication
Date de publication:
23 Dec 2023
23 Dec 2023
Historique:
revised:
06
10
2023
received:
24
07
2023
accepted:
15
11
2023
medline:
23
12
2023
pubmed:
23
12
2023
entrez:
23
12
2023
Statut:
aheadofprint
Résumé
Mixotrophic protists combine photosynthesis and phagotrophy to obtain energy and nutrients. Because mixotrophs can act as either primary producers or consumers, they have a complex role in marine food webs and biogeochemical cycles. Many mixotrophs are also phenotypically plastic and can adjust their metabolic investments in response to resource availability. Thus, a single species's ecological role may vary with environmental conditions. Here, we quantified how light and food availability impacted the growth rates, energy acquisition rates, and metabolic investment strategies of eight strains of the mixotrophic chrysophyte, Ochromonas. All eight Ochromonas strains photoacclimated by decreasing chlorophyll content as light intensity increased. Some strains were obligate phototrophs that required light for growth, while other strains showed stronger metabolic responses to prey availability. When prey availability was high, all eight strains exhibited accelerated growth rates and decreased their investments in both photosynthesis and phagotrophy. Photosynthesis and phagotrophy generally produced additive benefits: In low-prey environments, Ochromonas growth rates increased to maximum, light-saturated rates with increasing light but increased further with the addition of abundant bacterial prey. The additive benefits observed between photosynthesis and phagotrophy in Ochromonas suggest that the two metabolic modes provide nonsubstitutable resources, which may explain why a tradeoff between phagotrophic and phototrophic investments emerged in some but not all strains.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Division of Ocean Sciences
ID : OCE-1851194
Organisme : Simons Foundation
ID : Award 689265
Informations de copyright
© 2023 The Authors. Journal of Phycology published by Wiley Periodicals LLC on behalf of Phycological Society of America.
Références
Aaronson, S., & Behrens, U. (1973). A note on the fine structure of the Ochromonas danica “tail.” Archiv für Mikrobiologie, 93(4), 359-362. https://doi.org/10.1007/BF00427931
Andersen, R. A., Graf, L., Malakhov, Y., & Yoon, H. S. (2017). Rediscovery of the Ochromonas type species Ochromonas triangulata (Chrysophyceae) from its type locality (Lake Veysove, Donetsk region, Ukraine). Phycologia, 56(6), 591-604. https://doi.org/10.2216/17-15.1
Andersson, A., Falk, S., Samuelsson, G., & Hagström, Å. (1989). Nutritional characteristics of a mixotrophic nanoflagellate, Ochromonas sp. Microbial Ecology, 17(3), 251-262. https://doi.org/10.1007/BF02012838
Berge, T., Chakraborty, S., Hansen, P. J., & Andersen, K. H. (2017). Modeling succession of key resource-harvesting traits of mixotrophic plankton. The ISME Journal, 11(1), 212-223. https://doi.org/10.1038/ismej.2016.92
Caron, D. A. (2016). Mixotrophy stirs up our understanding of marine food webs. Proceedings of the National Academy of Sciences of the United States of America, 113(11), 2806-2808. https://doi.org/10.1073/pnas.1600718113
Caron, D. A., Sanders, R. W., Lim, E. L., Marrasé, C., Amaral, L. A., Whitney, S., Aoki, R. B., & Porters, K. G. (1993). Light-dependent phagotrophy in the freshwater mixotrophic chrysophyte Dinobryon cylindricum. Microbial Ecology, 25(1), 93-111. https://doi.org/10.1007/BF00182132
Castelfranco, P. A., & Beale, S. I. (1981). 9-Chlorophyll biosynthesis. In M. D. Hatch & N. K. Boardman (Eds.), Photosynthesis (pp. 375-421). Academic Press. https://doi.org/10.1016/B978-0-12-675408-7.50015-X
Clark, J. R., Lenton, T. M., Williams, H. T. P., & Daines, S. J. (2013). Environmental selection and resource allocation determine spatial patterns in picophytoplankton cell size. Limnology and Oceanography, 58(3), 1008-1022. https://doi.org/10.4319/lo.2013.58.3.1008
Coats, D. W., & Harding, L. W., Jr. (1988). Effect of light history on the ultrastructure and physiology of Prorocentrum mariae-lebouriae (Dinophyceae). Journal of Phycology, 24(1), 67-77. https://doi.org/10.1111/j.1529-8817.1988.tb04457.x
Diniz-Filho, J. A. F., Soares, T. N., Lima, J. S., Dobrovolski, R., Landeiro, V. L., Telles, M. P. d. C., Rangel, T. F., & Bini, L. M. (2013). Mantel test in population genetics. Genetics and Molecular Biology, 36, 475-485. https://doi.org/10.1590/S1415-47572013000400002
Dubinsky, Z., & Stambler, N. (2009). Photoacclimation processes in phytoplankton: Mechanisms, consequences, and applications. Aquatic Microbial Ecology, 56(2-3), 163-176. https://doi.org/10.3354/ame01345
Escoubas, J. M., Lomas, M., LaRoche, J., & Falkowski, P. G. (1995). Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proceedings of the National Academy of Sciences of the United States of America, 92(22), 10237-10241.
Estep, K. W., Davis, P. G., Keller, M. D., & Sieburth, J. M. N. (1986). How important are oceanic algal nanoflagellates in bacterivory? Limnology and Oceanography, 31(3), 646-650. https://doi.org/10.4319/lo.1986.31.3.0646
Falkowski, P. G. (1980). Light-shade adaptation in marine phytoplankton. In P. G. Falkowski (Ed.), Primary productivity in the sea (pp. 99-119). Springer. https://doi.org/10.1007/978-1-4684-3890-1_6
Falkowski, P. G., Owens, T. G., Ley, A. C., & Mauzerall, D. C. (1981). Effects of growth irradiance levels on the ratio of reaction centers in two species of marine phytoplankton. Plant Physiology, 68(4), 969-973. https://doi.org/10.1104/pp.68.4.969
Fischer, R., Kitzwögerer, J., & Ptacnik, R. (2022). Light-dependent niche differentiation in two mixotrophic bacterivores. Environmental Microbiology Reports, 14(4), 530-537. https://doi.org/10.1111/1758-2229.13071
Flynn, K. J., & Mitra, A. (2009). Building the “perfect beast”: Modelling mixotrophic plankton. Journal of Plankton Research, 31(9), 965-992. https://doi.org/10.1093/plankt/fbp044
Foster, B. L. L., & Chrzanowski, T. H. (2012). The mixotrophic protist Ochromonas danica is an indiscriminant predator whose fitness is influenced by prey type. Aquatic Microbial Ecology, 68(1), 1-11. https://doi.org/10.3354/ame01594
Gast, R. J., Dennett, M. R., & Caron, D. A. (2004). Characterization of protistan assemblages in the Ross Sea, Antarctica, by denaturing gradient gel electrophoresis. Applied and Environmental Microbiology, 70(4), 2028-2037. https://doi.org/10.1128/AEM.70.4.2028-2037.2004
Gorbunov, M. Y., & Falkowski, P. G. (2005). Fluorescence induction and relaxation (FIRe) technique and instrumentation for monitoring photosynthetic processes and primary production in aquatic ecosystems. In A. van der ESt, & B. Bruce (Eds.), Photosynthesis: Fundamental aspects to global perspectives - Proceedings of the 13th International Congress of Photosynthesis (Vol. 2, pp. 1029-1031). Allen Press.
Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology, 59(3), 307-321. https://doi.org/10.1093/sysbio/syq010
Harding, L. W., Jr. (1988). The time-course of photoadaptation to low-light in Prorocentrum mariae-lebouriae (Dinophyceae). Journal of Phycology, 24(2), 274-281. https://doi.org/10.1111/j.1529-8817.1988.tb04243.x
Hartmann, M., Grob, C., Tarran, G. A., Martin, A. P., Burkill, P. H., Scanlan, D. J., & Zubkov, M. V. (2012). Mixotrophic basis of Atlantic oligotrophic ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 109(15), 5756-5760. https://doi.org/10.1073/pnas.1118179109
Holen, D. (2010). Mixotrophy in two species of Ochromonas. Nova Hedwigia, Beiheft, 136, 153-165.
Jansson, M., Blomqvist, P., Jonsson, A., & Bergström, A.-K. (1996). Nutrient limitation of bacterioplankton, autotrophic and mixotrophic phytoplankton, and heterotrophic nanoflagellates in Lake Örträsket. Limnology and Oceanography, 41(7), 1552-1559. https://doi.org/10.4319/lo.1996.41.7.1552
Jassby, A. D. & Platt, T. (1976). Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnology and Oceanography, 21(4), 540-547. https://doi.org/10.4319/lo.1976.21.4.0540
Jassey, V. E. J., Signarbieux, C., Hättenschwiler, S., Bragazza, L., Buttler, A., Delarue, F., Fournier, B., Gilbert, D., Laggoun-Défarge, F., Lara, E., Mills, R. T. E., Mitchell, E. A. D., Payne, R. J., & Robroek, B. J. M. (2015). An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming. Scientific Reports, 5, 16931. https://doi.org/10.1038/srep16931
Jeong, H. J., & Latz, M. I. (1994). Growth and grazing rates of the heterotrophic dinoflagellates Protoperidinium spp. on red tide dinoflagellates. Marine Ecology Progress Series, 106(1/2), 173-185.
Keller, M. D., Selvin, R. C., Claus, W., & Guillard, R. R. L. (1987). Media for the culture of oceanic ultraphytoplankton. Journal of Phycology, 23(4), 633-638. https://doi.org/10.1111/j.1529-8817.1987.tb04217.x
Kimura, B., & Ishida, Y. (1989). Phospholipid as a growth factor of Uroglena americana, a red tide Chrysophyceae in Lake Biwa. Nippon Suisan Gakkaishi, 55(5), 799-804. https://doi.org/10.2331/suisan.55.799
Lawrenz, E., Silsbe, G., Capuzzo, E., Ylöstalo, P., Forster, R. M., Simis, S. G. H., Prášil, O., Kromkamp, J. C., Hickman, A. E., Moore, C. M., Forget, M.-H., Geider, R. J., & Suggett, D. J. (2013). Predicting the electron requirement for carbon fixation in seas and oceans. PLoS ONE, 8(3), e58137. https://doi.org/10.1371/journal.pone.0058137
Laws, E. A. (1991). Photosynthetic quotients, new production and net community production in the open ocean. Deep Sea Research Part A. Oceanographic Research Papers, 38(1), 143-167. https://doi.org/10.1016/0198-0149(91)90059-O
Lefort, V., Longueville, J.-E., & Gascuel, O. (2017). SMS: Smart model selection in PhyML. Molecular Biology and Evolution, 34(9), 2422-2424. https://doi.org/10.1093/molbev/msx149
Lepori-Bui, M., Paight, C., Eberhard, E., Mertz, C. M., & Moeller, H. V. (2022). Evidence for evolutionary adaptation of mixotrophic nanoflagellates to warmer temperatures. bioRxiv https://doi.org/10.1101/2022.02.03.479051
Lewitus, A. J., Caron, D. A., & Miller, K. R. (1991). Effects of light and glycerol on the organization of the photosynthetic apparatus in the facultative heterotroph Pyrenomonas salina (Cryptophyceae). Journal of Phycology, 27(5), 578-587. https://doi.org/10.1111/j.0022-3646.1991.00578.x
Li, Q., Edwards, K., Schvarcz, C., Selph, K., & Steward, G. (2021). Plasticity in the grazing ecophysiology of Florenciella (Dichtyochophyceae), a mixotrophic nanoflagellate that consumes Prochlorococcus and other bacteria. Limnology and Oceanography, 66, 47-60. https://doi.org/10.1002/lno.11585
Lie, A. A. Y., Liu, Z., Terrado, R., Tatters, A. O., Heidelberg, K. B., & Caron, D. A. (2018). A tale of two mixotrophic chrysophytes: Insights into the metabolisms of two Ochromonas species (Chrysophyceae) through a comparison of gene expression. PLoS ONE, 13(2), e0192439. https://doi.org/10.1371/journal.pone.0192439
MacIntyre, H. L., Kana, T. M., Anning, T., & Geider, R. J. (2002). Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. Journal of Phycology, 38(1), 17-38. https://doi.org/10.1046/j.1529-8817.2002.00094.x
Maddison, W. P., & Maddison, D. R. (2023). Mesquite: A modular system for evolutionary analysis (3.81) [computer software]. http://www.mesquiteproject.org
Maranger, R., Bird, D. F., & Price, N. M. (1998). Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria. Nature, 396(6708), 248-251. https://doi.org/10.1038/24352
Mattson, C. A., & Messac, A. (2005). Pareto frontier based concept selection under uncertainty, with visualization. Optimization and Engineering, 6(1), 85-115. https://doi.org/10.1023/B:OPTE.0000048538.35456.45
Mitra, A., Flynn, K. J., Tillmann, U., Raven, J. A., Caron, D., Stoecker, D. K., Not, F., Hansen, P. J., Hallegraeff, G., Sanders, R., Wilken, S., McManus, G., Johnson, M., Pitta, P., Våge, S., Berge, T., Calbet, A., Thingstad, F., Jeong, H. J., … Lundgren, V. (2016). Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition: Incorporation of diverse mixotrophic strategies. Protist, 167(2), 106-120. https://doi.org/10.1016/j.protis.2016.01.003
Moeller, H. V., Neubert, M. G., & Johnson, M. D. (2019). Intraguild predation enables coexistence of competing phytoplankton in a well-mixed water column. Ecology, 100(12), e02874. https://doi.org/10.1002/ecy.2874
Münkemüller, T., Lavergne, S., Bzeznik, B., Dray, S., Jombart, T., Schiffers, K., & Thuiller, W. (2012). How to measure and test phylogenetic signal. Methods in Ecology and Evolution, 3(4), 743-756. https://doi.org/10.1111/j.2041-210X.2012.00196.x
Paradis, E., Blomberg, S., Bolker, B., Brown, J., Claramunt, S., Claude, J., Cuong, H. S., Desper, R., Didier, G., Durand, B., Dutheil, J., Ewing, R. J., Gascuel, O., Guillerme, T., Heibl, C., Ives, A., Jones, B., Krah, F., … de Vienne, D. (2023). ape: Analyses of Phylogenetics and Evolution (5.7-1) [Computer software]. https://cran.r-project.org/web/packages/ape/
R Core Team. (2023). R: A language and environment for statistical computing [computer software]. R Foundation for Statistical Computing https://www.R-project.org/
Raven, J. A. (1997). Phagotrophy in phototrophs. Limnology and Oceanography, 42(1), 198-205. https://doi.org/10.4319/lo.1997.42.1.0198
Revell, L. J. (2023). Phytools: Phylogenetic tools for comparative biology (and other things) (1.9-16) [computer software]. https://cran.r-project.org/web/packages/phytools/index.html
Sanders, R. W., Caron, D. A., Davidson, J. M., Dennett, M. R., & Moran, D. M. (2001). Nutrient acquisition and population growth of a mixotrophic alga in axenic and bacterized cultures. Microbial Ecology, 42(4), 513-523. https://doi.org/10.1007/s00248-001-1024-6
Sanders, R. W., Porter, K. G., Bennett, S. J., & DeBiase, A. E. (1989). Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnology and Oceanography, 34(4), 673-687. https://doi.org/10.4319/lo.1989.34.4.0673
Sanders, R. W., Porter, K. G., & Caron, D. A. (1990). Relationship between phototrophy and phagotrophy in the mixotrophic chrysophyte Poterioochromonas malhamensis. Microbial Ecology, 19(1), 97-109. https://doi.org/10.1007/BF02015056
Schmidtke, A., Bell, E. M., & Weithoff, G. (2006). Potential grazing impact of the mixotrophic flagellate Ochromonas sp. (Chrysophyceae) on bacteria in an extremely acidic lake. Journal of Plankton Research, 28(11), 991-1001. https://doi.org/10.1093/plankt/fbl034
Stoecker, D. K. (1998). Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. European Journal of Protistology, 34(3), 281-290. https://doi.org/10.1016/S0932-4739(98)80055-2
Sukenik, A., Bennett, J., & Falkowski, P. (1988). Changes in the abundance of individual apoproteins of light-harvesting chlorophyll ab-protein complexes of photosystem I and II with growth irradiance in the marine chlorophyte Dunaliella tertiolecta. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 932, 206-215. https://doi.org/10.1016/0005-2728(88)90157-0
Terrado, R., Pasulka, A. L., Lie, A. A.-Y., Orphan, V. J., Heidelberg, K. B., & Caron, D. A. (2017). Autotrophic and heterotrophic acquisition of carbon and nitrogen by a mixotrophic chrysophyte established through stable isotope analysis. The ISME Journal, 11(9), Article 9-Article 2034. https://doi.org/10.1038/ismej.2017.68
Tilman, D. (1980). Resources: A graphical-mechanistic approach to competition and predation. The American Naturalist, 116(3), 362-393.
Våge, S., Castellani, M., Giske, J., & Thingstad, T. F. (2013). Successful strategies in size structured mixotrophic food webs. Aquatic Ecology, 47(3), 329-347. https://doi.org/10.1007/s10452-013-9447-y
Ward, B. A., Dutkiewicz, S., Barton, A. D., & Follows, M. J. (2011). Biophysical aspects of resource acquisition and competition in algal mixotrophs. The American Naturalist, 178(1), 98-112. https://doi.org/10.1086/660284
Wilken, S., Choi, C. J., & Worden, A. Z. (2020). Contrasting mixotrophic lifestyles reveal different ecological niches in two closely related marine protists. Journal of Phycology, 56(1), 52-67. https://doi.org/10.1111/jpy.12920
Wilken, S., Schuurmans, J. M., & Matthijs, H. C. P. (2014). Do mixotrophs grow as photoheterotrophs? Photophysiological acclimation of the chrysophyte Ochromonas danica after feeding. New Phytologist, 204(4), 882-889. https://doi.org/10.1111/nph.12975
Wilken, S., Yung, C. C. M., Hamilton, M., Hoadley, K., Nzongo, J., Eckmann, C., Corrochano-Luque, M., Poirier, C., & Worden, A. Z. (2019). The need to account for cell biology in characterizing predatory mixotrophs in aquatic environments. Philosophical Transactions of the Royal Society B: Biological Sciences, 374(1786), 20190090. https://doi.org/10.1098/rstb.2019.0090
Yang, E. C., Boo, G. H., Kim, H. J., Cho, S. M., Boo, S. M., Andersen, R. A., & Yoon, H. S. (2012). Supermatrix data highlight the phylogenetic relationships of photosynthetic stramenopiles. Protist, 163(2), 217-231. https://doi.org/10.1016/j.protis.2011.08.001
Zubkov, M. V., & Tarran, G. A. (2008). High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature, 455(7210), 224-226. https://doi.org/10.1038/nature07236