Abstract
Large-scale blooms of Phaeocystis globosa have caused serious damage to marine ecosystems in coastal waters of China. Phaeocystis blooms depend on the competitive advantage of their heteromorphic life history: colony formation has the benefit of resisting herbivory by zooplankton, and solitary cells can absorb nutrients rapidly. In order to better understand the mechanisms underlying the metabolic differences between the two types of cells, morphological observations, rapid light curve analysis, fatty acid profiling, and transcriptome assessment were conducted in the laboratory. The rapid light curve of colonial cells was higher than that of solitary cells, which indicated that colonial cells had higher CO2 fixation capacity. The fatty acid level of colonial cells was evidently lower than that of solitary cells, which is consistent with down-regulated synthesis of fatty acids and up-regulated degradation of fatty acids in the transcriptome. ATP-binding cassette transporters, the TCA cycle, and biosynthesis of exopolysaccharides (EPS) also displayed obvious differences. In summary, colonial cells have stronger carbon fixation capacity. They do not synthesize fatty acids as energy storage materials but secrete EPS, which might be one of the mechanisms of colony formation. Here we present a physiological and molecular overview of the differences between solitary cells and colonial cells and thereby provide further insight to help unravel the mechanisms that help Phaeocystis globosa adapt to different environments.
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References
Aslam, S. N., Strauss, J., Thomas, D. N., and Underwood, G., 2018. Identifying metabolic pathways for production of extracellsular polymeric substances by the diatom Fragilariopsis cylindrus inhabiting sea ice. ISME Journal, 12(5): 66–79, DOI: https://doi.org/10.1038/s41396-017-0039-z.
Bender, S. J., Moran, D. M., McIlvin, M. R., Zheng, H., Mccrow, J. P., Badger, J., et al., 2018. Colony formation in Phaeocystis antárctica: Connecting molecular mechanisms with iron biogeochemistry. Biogeosciences, 15(16): 4923–4942, DOI: https://doi.org/10.5194/bg-15-4923-2018.
Boggetto, N., Gontero, B., and Maberly, S. C., 2007. Regulation of phosphoribulokinase and glyceraldehyde 3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa. Journal of Phycology, 43(6): 1227–1235, DOI: https://doi.org/10.1111/j.1529-8817.2007.00409.x.
Breton, E., Rousseau, V., Parent, J. Y., Ozer, J., and Lancelot, C., 2006. Hydroclimatic modulation of diatom/Phaeocystis blooms in the nutrient-enriched Belgian coastal waters (North Sea). Limnology and Oceanography, 51(3): 1401–1409, DOI: https://doi.org/10.2307/3841186.
Brussaard, C. P. D., Bratbak, G., Baudoux, A. C., and Ruardij, P., 2007. Phaeocystis and its interaction with viruses. Biogeochemistry, 83(1–3): 201–215, DOI: https://doi.org/10.1007/s10533-007-9096-0.
Brussaard, C. P. D., Kuipers, B., and Veldhuis, M. J. W., 2005. A mesocosm study of Phaeocystis globosa, population dynamics: I. Regulatory role of viruses in bloom control. Harmful Algae, 4(5): 859–874, DOI: https://doi.org/10.1016/j.hal.2004.12.012.
Buchanan, B. B., and Balmer, Y., 2005. Redox regulation: A broadening horizon. Annual Review of Plant Biology, 56(1): 187–220, DOI: https://doi.org/10.1146/annurev.arplant.56.032604.144246.
Chen, J. F., Xu, N., Jiang, T. J., Wang, Y., Wang, Z. H., and Qi, Y. Z., 1999. Phaeocystis globosa, a newly recorded species of red tide in China. Journal of Jinan University (Natural Science Edition), 20(3): 124–129, DOI: https://doi.org/10.1088/0256-307X/16/12/025.
Chen, Y. Q., Wang, N, Zhang, P., Hui, Z., and Qu, L. H., 2002. Molecular evidence identifies bloom-forming Phaeocystis (Prymnesiophyta) from coastal waters of southeast China as Phaeocystis globosa. Biochemical Systematics and Ecology, 30(1): 15–22, DOI: https://doi.org/10.1016/S0305-1978(01)00054-0.
Couet, D., Pringault, O., Bancon-Montigny, C., Briant, N., Elbaz, F. P., Delpoux, S., et al., 2018. Effects of copper and butyltin compounds on the growth, photosynthetic activity and toxin production of two HAB dinoflagellates: The planktonic Alexandrium catenella and the benthic Ostreopsis cf. ovata. Aquatic Toxicology, 196(1): 154–167, DOI: https://doi.org/10.1016/j.aquatox.2018.01.005.
Figueroa, R. I., Estrada, M., and Garcés, E., 2018. Life histories of microalgal species causing harmful blooms: Haploids, diploids and the relevance of benthic stages. Harmful Algae, 73: 44–57, DOI: https://doi.org/10.1016/j.hal.2018.01.006.
Gaillard, S., Jacquet, H., Vavasseur, A., Leonhardt, N., and Forestier, C., 2008. AtMRP6/AtABCC6, an ATP-binding cassette transporter gene expressed during early steps of seedling development and up-regulated by cadmium in Arabidopsis thaliana. BMC Plant Biology, 8(1): 22, DOI: https://doi.org/10.1186/1471-2229-8-22.
Gu, S., Xiao, S. W., Zheng, J. W., Li, H. Y., Liu, J. S., and Yang, W. D., 2019. ABC transporters in Prorocentrum lima and their expression under different environmental conditions including okadaic acid production. Marine Drugs, 17(259): 1–16, DOI: https://doi.org/10.3390/md17050259.
Gügi, B. L., Costaouec, T., Burel, C., Lerouge, P., Helbert, W., and Bardor, M., 2015. Diatom-specific oligosaccharide and polysaccharide structures help to unravel biosynthetic capabilities in diatoms. Marine Drugs, 13: 5993–6018, DOI: https://doi.org/10.3390/md13095993.
Guillard, R. R. L., and Ryther, J. H., 1962. Studies of marine planktonic diatoms: iii. Some effects of temperature on respiration of five species. Canadian Journal of Microbiology, 8(4): 447–453, DOI: https://doi.org/10.1139/m62-058.
Hamm, C. E., 2000. Architecture, ecology and biogeochemistry of Phaeocystis colonies. Journal of Sea Research, 43(3): 307–315, DOI: https://doi.org/10.1016/S1385-1101(00)00014-9.
Henkes, S., Sonnewald, U., Badur, R., and Stitt, F. M., 2001. A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. The Plant Cells, 13(3): 535–551, DOI: https://doi.org/10.1105/tpc.13.3.535.
Howard, T. P., Lloy, J. C., and Raines, C. A., 2011. Inter-species variation in the oligomeric states of the higher plant Calvin cycle enzymes glyceraldehyde-3-phosphate dehydrogenase and phosphoribulokinase. Journal of Experimental Botany, 62(11): 3799–3805, DOI: https://doi.org/10.1093/jxb/err057.
Jakobsen, H. H., and Tang, K. W., 2002. Effect of protozoan grazing on colony formation in Phaeocystis globosa (Prymnesiophyceae) and the potential costs and benefits. Aquatic Microbial Ecology, 27(13): 261–273, DOI: https://doi.org/10.3354/ame027261.
Kaczmarzyk, D., and Fulda, M., 2010. Fatty acid activation in cyanobacteria mediated by acyl-acyl carrier protein synthetase enables fatty acid recycling. Plant Physiology, 152(3): 1598–1610, DOI: https://doi.org/10.2307/25680760.
Kates, M., and Baxter, R. M., 1962. Lipid composition of mesophilic and psychrophilic yeasts (Candida species) as influenced by environmental temperature. Canadian Journal of Biochemistry and Physiology, 40(9): 1213–1227, DOI: https://doi.org/10.1139/o62-136.
Lancelot, C., Keller, M. D., Rousseau, V., Smith, W., and Mathot, S., 1998. Autecology of the marine Haptophyte Phaeocystis sp. NatoAsi, 16(1): 209–224, DOI: https://doi.org/978-3540641179.
Li, B., Li, W. L., Li, T. S., and Li, M. M., 2015. Variation of environmental factors during Phaeocystis globosa blooms and its implications for the bloom. Journal of Biology, 34(5): 1351–1358, DOI: https://doi.org/10.13292/j.1000-4890.20150311.050.
Long, C., Luo, W. C., Zhou, H. Y., Shi, Y. F., Gao, C. H., and Huang, R. M., 2016. Isolation of toxic compounds from wild Phaeocystis globosa. Chinese Chemical Letters, 27(2): 247–250, DOI: https://doi.org/10.1016/j.cclet.2015.10.005.
López-Romero, E., BalcázarOrozco, R., CalvoMéndez, C., and FloresCarreón, A., 2004a. Partial purification and biochemical characterization of a soluble alpha-glucosidase ii-like activity from Candida albicans. Fems Microbiology Letters, 236(1): 123–138, DOI: https://doi.org/10.1111/j.1574-6968.2004.tb09637.x.
López-Romero, P., Gómez, M. J., Gómez-Puertas, P., and Valencia, A., 2004b. Prediction of functional sites in proteins by evolutionary methods. Methods in proteome and protein analysis. Principles and Practice, 3: 319–340, DOI: https://doi.org/10.1007/978-3-662-08722-0_22.
Love, M. I., Huber, W., and Anders, S., 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq 2. Genome Biology, 15: 550, DOI: https://doi.org/10.1186/s13059-014-0550-8.
Lu, N., Wei, D., Jiang, X. L., Chen, F., and Yang, S. T., 2012. Fatty acids profiling and biomarker identification in snow alga Chlamydomonas nivalis by NaCl stress using GC/MS and multivariate statistical analysis. Analytical Letters, 45(10): 1172–1183, DOI: https://doi.org/10.1080/00032719.2012.673094.
Mars-Brisbin, M., and Mitarai, S., 2019. Differential gene expression supports a resource-intensive, defensive role for colony production in the bloom-forming haptophyte, Phaeocystis globosa. Journal of Eukaryotic Microbiology, 66(5): 788–801, DOI: https://doi.org/10.1111/jeu.12727.
Nakamura, Y., and Yamada, M., 1979. The light-dependent step of de novo synthesis of long chain fatty acids in spinach chloroplasts. Plant Science Letters, 14(4): 291–295, DOI: https://doi.org/10.1016/S0304-4211(79)90173-1.
Nejstgaard, J. C., Tang, K. W., Steinke, M., Dutz, J., Koski, M., Antajan, E., et al., 2007. Zooplankton grazing on Phaeocystis: A quantitative review and future challenges. Biogeochemistry (Dordrecht), 83(1–3): 147–172, DOI: https://doi.org/10.1007/s10533-007-9098-y.
Nuruzzaman, M., Zhang, R., Cao, H. Z., and Luo, Z. Y., 2014. Plant pleiotropic drug resistance transporters: Transport mechanism, gene expression, and function. Journal of Integrative Plant Biology, 56: 729–740, DOI: https://doi.org/10.1111/jipb.12196.
Okazaki, Y., Shimojima, M., Sawada, Y., Toyooka, K., Narisawa, T., Mochida, K., et al., 2009. A chloroplastic UDP-glucose pyrophosphorylase from Arabidopsis is the committed enzyme for the first step of sulfolipid biosynthesis. Plant Cell, 21(3): 892–909, DOI: https://doi.org/10.1016/j.disopt.2008.10.003.
Parke, M., Green, J. C., and Manton, I., 1971. Observations on the fine structure of zoids of the genus Phaeocystis (Haptophyceae). Journal of the Marine Biological Association of the UK, 51: 927–941, DOI: https://doi.org/10.1017/S0025315400018063.
Pavlov, A. K., Taskjelle, T., Kauko, H. M., Hamre, B., Hudson, S. R., Assmy, P., et al., 2017. Altered inherent optical properties and estimates of the underwater light field during an Arctic under-ice bloom of Phaeocystis pouchetii. Journal of Geophysical Research — Oceans, 122: 4939–4961, DOI: https://doi.org/10.1002/2016JC012471.
Peperzak, L., Colijn, F., Vrieling, E. G., Gieskes, W. W. C., and Peeters, J. C. H., 2000. Observations of flagellates in colonies of Phaeocystis globosa (Prymnesiophyceae): A hypothesis for their position in the life cycle. Journal of Plankton Research, 22: 2181–2203, DOI: https://doi.org/10.1093/plankt/22.12.2181.
Platt, T., Gallegos, C. L., and Harrison, W. G., 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Reserach, 38: 687–701, DOI: https://doi.org/10.1093/pasj/57.2.341.
Ploug, H., Stolte, W., and Bo, B. J., 1999. Diffusive boundary layers of the colony-forming plankton alga, Phaeocystis sp. — Implications for nutrient uptake and cellsular growth. Limnology Oceanography, 44(8): 1959–1967, DOI: https://doi.org/10.4319/lo.1999.44.8.1959.
Rees, D. C., Johnson, E., and Lewinson, O., 2009. ABC transporters: The power to change. Nature Reviews Molecular Cell Biology, 10(3): 218–227, DOI: https://doi.org/10.1038/nrm2646.
Riegman, R., Noordeloos, A., and Cadée, G. C., 1992. Phaeoystis blooms and eutrophication of the continental coastal zones of the North Sea. Marine Biology, 112(3): 479–484, DOI: https://doi.org/10.1007/BF00356293.
Rousseau, V., Chrétiennot-Dinet, M. J., Jacobsen, A., Verity, P., and Whipple, S., 2007. The life cycle of Phaeocystis: State of knowledge and presumptive role in ecology. Biogeochemistry, 83(1–3): 29–47, DOI: https://doi.org/10.1007/s10533-007-9085-3.
Rousseau, V., Lantoine, F., Rodriguez, F., Legall, F., Chrétiennot-Dinet, Marie-Josèphe., et al., 2013. Characterization of Phaeocystis globosa (Prymnesiophyceae), the blooming species in the southern North Sea. Journal of Sea Research, 76: 105–113, DOI: https://doi.org/10.1016/j.seares.2012.07.011.
Rousseau, V., Vaulot, D., Casotti, R., Cariou, V., Lenz, J., Gunkel, J., et al., 1994. The life cycle of Phaeocystis (Prymnesiophyceae): Evidence and hypotheses. Journal of Marine Systems, 5(1): 23–39, DOI: https://doi.org/10.1016/0924-7963(94)90014-0.
Schoemann, V., Becquevort, S., and Stefels, J., 2005. Phaeocystis blooms in the global ocean and their controlling mechanisms: A review. Journal of Sea Research, 53(1–2): 43–66, DOI: https://doi.org/10.1016/j.seares.2004.01.008.
Smith, W. O., Liu, X., Tang, K. W., Delizo, L. M., Doan, N. H., Nguyen, N. L., et al., 2014. Giantism and its role in the harmful algal bloom species Phaeocystis globosa. Deep Sea Research Part II: Topical Studies in Oceanography, 101(3): 95–106, DOI: https://doi.org/10.1016/j.dsr2.2012.12.005.
Smith, W., Codispoti, L. A., Nelson, D. M., Manley, T., Buskey, E. J., Niebauer, H. J., et al., 1991. Importance of Phaeocystis blooms in the high-latitude ocean carbon cycle. Nature, 352(6335): 514–516, DOI: https://doi.org/10.1038/352514a0.
Stukkens, Y. A., Bultreys, A., Grec, S., Trombik, T., Vanham, D., and Boutry, M., 2005. NpPDR1, a pleiotropic drug resistancetype ATP-binding cassette transporter from Nicotiana plumbaginifolia, plays a major role in plant pathogen defense. Plant Physiology, 139: 341–352, DOI: https://doi.org/10.1104/pp.105.062372.
Underwood, G. J. C., and Paterson, D. M., 2003. The importance of extracellsular carbohydrate production by marine epipelic diatoms. Advances in Botanical Research, 40: 184–241, DOI: https://doi.org/10.1016/S0065-2296(05)40005-1.
Van-Leeuwe, M. A., Stefels, J., Belviso, S., Lancelot, C., Verity, P. G., and Gieskes, W. W. C., 2007. Phaeocystis, major link in the biogeochemical cycling of climate-relevant elements. Bio-geochemistry, 83(1–3): 1–22, DOI: https://doi.org/10.1007/978-1-4020-6214-8.
Verity, P. G., Whipple, S. J., Nejstgaard, J. C., and Alderkamp, A. C., 2007. Colony size, cell number, carbon and nitrogen contents of Phaeocystis pouchetii from western Norway. Journal of Plankton Research, 29(4): 359–367, DOI: https://doi.org/10.1093/plankt/fbm021.
Von-Dassow, P., and Montresor, M., 2011. Unveiling the mysteries of phytoplankton life cycles: Patterns and opportunities behind complexity. Journal of Plankton Research, 33(1): 3–12, DOI: https://doi.org/10.1093/planktfbq137.
Wang, X., Wang, Y., Ou, L., He, X., and Chen, D., 2015. Allocation costs associated with induced defense in Phaeocystis globosa (Prymnesiophyceae): The effects of nutrient availability. Scientific Reports, 5(1): 10850, DOI: https://doi.org/10.1038/srep10850.
Ward, B. A., Dutkiewicz, S., Barton, A. D., and Follows, A. M. J., 2011. Biophysical aspects of resource acquisition and competition in algal mixotrophs. The American Naturalist, 178(1): 98–112, DOI: https://doi.org/10.1086/660284.
Xing, G. L., Yuan, H. L., Yang, J. S., Li, J. Y., Gao, Q. X., Li, W. L., et al., 2018. Integrated analyses of transcriptome, proteome and fatty acid profilings of the oleaginous microalga Auxenochlorella protothecoides, utex 2341 reveal differential reprogramming of fatty acid metabolism in response to low and high temperatures. Algal Research, 33: 16–27, DOI: https://doi.org/10.1016/j.algal.2018.04.028.
Youvan, D. C., and Marrs, B. L., 1987. Molecular mechanisms of photosynthesis. Scientific American, 256(6): 42–48, DOI: https://doi.org/10.1038/scientificamerican0687-42.
Zhang, S. F., Zhang, K., Cheng, H. M., Lin, L., and Wang, D. Z., 2020. Comparative transcriptomics reveals colony formation mechanism of a harmful algal bloom species Phaeocystis globosa. Science of the Total Environment, 719: 137454, DOI: https://doi.org/10.1016/j.scitotenv.2020.137454.
Acknowledgements
This work was supported by the National Key R&D Program of China (No. 2017YFC1404300), the National Natural Science Foundation of China (Nos. 41976082, 41676144 and 31670266), the Natural Science Foundation of Guangdong Province (No. 2017A030313115). We thank Prof. Paul Giller (University College Cork, Ireland) for English editing of the manuscript.
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Liang, D., Wang, X., Huo, Y. et al. Differences Between Solitary Cells and Colonial Cells in the Heteromorphic Life Cycle of Phaeocystis globosa: Morphology, Physiology, and Transcriptome. J. Ocean Univ. China 20, 939–948 (2021). https://doi.org/10.1007/s11802-021-4684-5
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DOI: https://doi.org/10.1007/s11802-021-4684-5