Strategies of phosphorus utilization in an astaxanthin-producing green alga Haematococcus pluvialis, a comparison with a bloom-forming cyanobacterium Microcystis wesenbergii

Hydrobiological Bulletin - Tập 53 - Trang 679-688 - 2019
Dongbo Ding1, Shasha Chen1, Shuiping Peng1, Changyu Jiang1, Lingling Zheng2, Jie Li1
1Hunan Key Laboratory of Animal Models for Human Diseases, School of Life Sciences, Central South University, Changsha, China
2State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China

Tóm tắt

Haematococcus pluvialis is a unicellular green alga with great commercial value, due to its synthesis of powerful antioxidant astaxanthin. H. pluvialis was mainly distributed in small water bodies but was also observed in eutrophicated lakes, and even coexisted with Microcystis. However, Haematococcus cells never prevail in eutrophicated water bodies. Phosphorus is the main limiting factor in most aquatic ecosystems and may have a role in the distribution of H. pluvialis. Here, we focused on the physiological responses of H. pluvialis to various phosphorus conditions (0.002, 0.02, 0.2, and 2 mM), and compared with a bloom-forming cyanobacterium Microcystis wesenbergii. Growth determination suggested that high phosphorus conditions (0.2 mM and 2 mM) favor the growth of H. pluvialis cells, but H. pluvialis cells have a shorter duration of log phase than M. wesenbergii cells. Growth determination also indicated H. pluvialis cells had lower tolerability to low phosphorus (0.002 mM). Qualitative comparisons from long-term and short-term phosphorus uptake experiments, polyphosphate accumulation and extracellular alkaline phosphatase expression analysis suggested two different phosphorus utilization strategies in the two species. H. pluvialis cells were characterized with the induction of extracellular alkaline phosphatase to survive phosphorus-deficient condition, while M. wesenbergii cells were characterized with quick uptake of phosphorus and accumulation more of polyphosphate in phosphorus-replete conditions. To our knowledge, this is the first study to demonstrate features of phosphorus uptake and utilization in H. pluvialis, which will increase our understanding in the distribution of H. pluvialis.

Tài liệu tham khảo

Borowitzka MA, Huisman JM, Osborn A (1991) Culture of the astaxanthin-producing green alga Haematococcus pluvialis 1. Effects of nutrients on growth and cell type. J Appl Phycol 3:295–304 Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 108:111–117 Boussiba S, Vonshak A (1991) Astaxanthin accumulation in the green alga Haematococcus pluvialis. Plant Cell Physiol 32:1077–1082 Brookes JD, Ganf GG (2001) Variations in the buoyancy response of Microcystis aeruginosa to nitrogen, phosphorus and light. J Plankton Res 23:1399–1411 Bru S, Jimenez J, Canadell D, Arino J, Clotet J (2017) Improvement of biochemical methods of polyP quantification. Microb Cell 4:6–15 Cao X, Štrojsová A, Znachor P, Zapomělová E, Liu G, Vrba J, Zhou Y (2005) Detection of extracellular phosphatases in natural spring phytoplankton of a shallow eutrophic lake (Donghu, China). Eur J Phycol 40:251–258 Chen W, Peng L, Wan N, Song L (2009) Mechanism study on the frequent variations of cell-bound microcystins in cyanobacterial blooms in Lake Taihu: implications for water quality monitoring and assessments. Chemosphere 77:1585–1593 Chrisostomou A, Moustaka-Gouni M, Sgardelis S, Lanaras T (2009) Air-dispersed phytoplankton in a mediterranean river-reservoir system (Aliakmon-Polyphytos, Greece). J Plankton Res 31:877–884 Chu FF, Chu PN, Cai PJ, Li WW, Lam PKS, Zeng RJ (2013) Phosphorus plays an important role in enhancing biodiesel productivity of Chlorella vulgaris under nitrogen deficiency. Bioresour Technol 134:341–346 Conley DJ et al (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323:1014–1015 Friebele ES, Correll DL, Faust MA (1978) Relationship between phytoplankton cell size and the rate of orthophosphate uptake: in situ observations of an estuarine population. Mar Biol 45:39–52 Genitsaris S, Stefanidou N, Katsiapi M, Vardaka E, Kormas KA, Sommer U, Moustaka-Gouni M (2016) Haematococcus: a successful air-dispersed colonist in ephemeral waters is rarely found in phytoplankton communities. Turk J Bot 40:427–438 Guerin M, Huntley ME, Olaizola M (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol 21:210–216 Guerrini F, Cangini M, Boni L, Trost P, Pistocchi R (2000) Metabolic responses of the diatom Achnanthes brevipes (Bacillariophyceae) to nutrient limitation. J Phycol 36:882–890 Harke MJ, Steffen MM, Gobler CJ, Otten TG, Wilhelm SW, Wood SA, Paerl HW (2016) A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54:4–20 Harker M, Tsavalos AJ, Young AJ (1996) Factors responsible for astaxanthin formation in the Chlorophyte Haematococcus pluvialis. Bioresour Technol 55:207–214 He P, Duncan J, Barber J (2007) Astaxanthin accumulation in the green alga Haematococcus pluvialis: effects of cultivation parameters. J Integr Plant Biol 49:447–451 Imamoglu E, Dalay MC, Sukan FV (2009) Influences of different stress media and high light intensities on accumulation of astaxanthin in the green alga Haematococcus pluvialis. New Biotechnol 26:199–204 Jimenez J, Bru S, Ribeiro MPC, Clotet J (2017) Polyphosphate: popping up from oblivion. Curr Genet 63:15–18 Kakizono T, Kobayashi M, Nagai S (1992) Effect of carbon/nitrogen ratio on encystment accompanied with astaxanthin formation in a green alga, Haematococcus pluvialis. J Ferment Bioeng 74:403–405 Konopka AE, Klemer AR, Walsby AE, Ibelings BW (1993) Effects of macronutrients upon buoyancy regulation by metalimnetic Oscillatoria agardhii in Deming Lake, Minnesota. J Plankton Res 15:1019–1034 Kulakova AN, Hobbs D, Smithen M, Pavlov E, Gilbert JA, Quinn JP, McGrath JW (2011) Direct quantification of inorganic polyphosphate in microbial cells using 4′-6-diamidino-2-phenylindole (DAPI). Environ Sci Technol 45:7799–7803 Le Jeune AH et al (2007) Planktonic microbial community responses to added copper. Aquat Toxicol 83:223–237 Lin SJ, Litaker RW, Sunda WG (2016) Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton. J Phycol 52:10–36 Lindemann C, Fiksen Ø, Andersen KH, Aksnes DL (2016) Scaling laws in phytoplankton nutrient uptake affinity. Front Mar Sci 3:26 Lürling M, Mello MME, van Oosterhout F, de Senerpont Domis L, Marinho MM (2018) Response of natural cyanobacteria and algae assemblages to a nutrient pulse and elevated temperature. Front Microbiol 9:1851 Markou G, Angelidaki I, Georgakakis D (2012) Microalgal carbohydrates: an overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Appl Microbiol Biotechnol 96:631–645 Martin P, Dyhrman ST, Lomas MW, Poulton NJ, Van Mooy BAS (2014) Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus. Proc Natl Acad Sci USA 111:8089–8094 O’Neil J, Davis T, Burford M, Gobler C (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334 Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microbial Ecol 65:995–1010 Pandey M, Tiwari D (2003) Characteristics of alkaline phosphatase in cyanobacterial strains and in an APase def mutant of Nostoc muscorum. World J Microbiol Biotechnol 19:279–284 Pettersson K (1980) Alkaline phosphatase activity and algal surplus phosphorus as phosphorus-deficiency indicators in Lake Erken. Arch Hydrobiol 89:54–87 Powell N, Shilton A, Chisti Y, Pratt S (2009) Towards a luxury uptake process via microalgae—defining the polyphosphate dynamics. Water Res 43:4207–4213 Proctor VW (1957) Some controlling factors in the distribution of Haematococcus pluvialis. Ecology 38:457–462 Reynolds CS (2007) Variability in the provision and function of mucilage in phytoplankton: facultative responses to the environment. Hydrobiologia 578:37–45 Romans KM, Carpenter EJ, Bergman B (1994) Buoyancy regulation in the colonial diazotrophic Cyanobacterium Trichodesmium tenue: ultrastructure and storage of carbohydrate, polyphosphate, and nitrogen. J Phycol 30:935–942 Scibilia L, Girolomoni L, Berteotti S, Alboresi A, Ballottari M (2015) Photosynthetic response to nitrogen starvation and high light in Haematococcus pluvialis. Algal Res 12:170–181 Senthilkumar R, Sivakumar K (2008) Studies on phytoplankton diversity in response to abiotic factors in Veeranam lake in the Cuddalore district of Tamil Nadu. J Environ Biol 29:747–752 Shah MMR, Liang Y, Cheng JJ, Daroch M (2016) Astaxanthin-producing green microalga Haematococcus pluvialis: from single cell to high value commercial products. Front Plant Sci 7:531 Shen H, Song L (2007) Comparative studies on physiological responses to phosphorus in two phenotypes of bloom-forming Microcystis. Hydrobiologia 592:475–486 Smith VH, Schindler DW (2009) Eutrophication science: where do we go from here? Trends Ecol Evol 24:201–207 Steffen MM et al (2017) Ecophysiological examination of the Lake Erie Microcystis bloom in 2014: linkages between biology and the water supply shutdown of Toledo, OH. Environ Sci Technol 51:6745–6755 Thompson PA, Oh HM, Rhee G (1994) Storage of phosphorus in nitrogen-fixing Anabaena flos-aquae (Cyanophyceae). J Phycol 30:267–273 Tocquin P, Fratamico A, Franck F (2012) Screening for a low-cost Haematococcus pluvialis medium reveals an unexpected impact of a low N/P ratio on vegetative growth. J Appl Phycol 24:365–373 Van Mooy BA et al (2009) Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458:69 Vandergucht DM, Sereda JM, Davies J-M, Hudson JJ (2013) A comparison of phosphorus deficiency indicators with steady state phosphate in lakes. Water Res 47:1816–1826 Werner TP, Amrhein N, Freimoser FM (2005) Novel method for the quantification of inorganic polyphosphate (iPoP) in Saccharomyces cerevisiae shows dependence of iPoP content on the growth phase. Arch Microbiol 184:129–136 Wu Z, Shi J, Li R (2009) Comparative studies on photosynthesis and phosphate metabolism of Cylindrospermopsis raciborskii with Microcystis aeruginosa and Aphanizomenon flos-aquae. Harmful Algae 8:910–915 Xu Y et al (2008) Non-microcystin producing Microcystis wesenbergii (Komarek) Komarek (Cyanobacteria) representing a main waterbloom-forming species in Chinese waters. Environ Pollut 156:162–167 Zhang W, Wang J, Wang J, Liu T (2014) Attached cultivation of Haematococcus pluvialis for astaxanthin production. Bioresour Technol 158:329–335 Zhu S, Wang Y, Xu J, Shang C, Wang Z, Xu J, Yuan Z (2015) Luxury uptake of phosphorus changes the accumulation of starch and lipid in Chlorella sp. under nitrogen depletion. Bioresour Technol 198:165–171