|
|
Cite this paper: |
|
|
PENG Guotao, Steven W. WILHELM, LIN Sijie, WANG Xiangrong. Response of Microcystis aeruginosa FACHB-905 to different nutrient ratios and changes in phosphorus chemistry[J]. Journal of Oceanology and Limnology, 2018, 36(4): 1040-1052 |
|
|
|
|
|
|
|
Response of Microcystis aeruginosa FACHB-905 to different nutrient ratios and changes in phosphorus chemistry |
|
| PENG Guotao1,2, Steven W. WILHELM3, LIN Sijie1, WANG Xiangrong2 |
|
1 College of Environmental Science and Engineering, State Key Laboratory of Pollution Control and Resource Reuse, Tongji University, Shanghai 200092, China;
2 Department of Environmental Science and Engineering, Fudan University, Shanghai 200433, China;
3 Department of Microbiology, University of Tennessee, Knoxville, TN 37920, USA |
|
| Abstract: |
| Cyanobacterial blooms are a global problem, with their occurrence tightly tied to nutrient loading. We cultured Microcystis aeruginosa FACHB-905 in growth medium with either inorganic (orthophosphate) or organic (β-glycerophosphate or polyphosphate) phosphorus and at different N:P ratios with 50:1, 30:1, 16:1, 4:1 and 1:4, serving as the phosphorus source. Fluorescence parameters were measured to determine the response of cellular responses to nutrient stress. Scanning electron microscopy (SEM) and estimates of antioxidant activity were employed to examine potential mechanisms of physical change. The results demonstrate that inorganic phosphorus was more bioavailable to M. aeruginosa relative to organic phosphorus in culture. The highest cell concentration (2.21×106 cells/mL), chlorophyll-a (0.39 pg/cell) and phycocyanin (1.57 pg/cell) quotas and high levels of chlorophyll fluorescence parameters (rETR, Ek, α, φPSⅡ and Fv/Fm) were obtained when phosphorus was supplied as K2HPO4 at a N:P ratio of 16-30. Organic sources of phosphorus (β-glycerophosphate and polyphosphate) were bioavailable to M. aeruginosa. In addition, too concentrated orthophosphate (N:P=1:4) resulted in the oxidative stress and lipid peroxidation of cell membrane (identified by the antioxidant system activity), and the photosynthetic activity declined consequently. This study has demonstrated the effects of different phosphorus chemistries and N:P ratios on the cyanobacterial growth, photosynthetic activity and cell physiology, which could be an effective tool for predicting cyanobacterial dominance or N-deficiency in natural lakes (due to the superior ability of cyanobacteria for dissolved N and fix atmospheric N in some cases). |
|
| Key words:
antioxidant system|chlorophyll fluorescence parameters|Microcystis|nutrient stress|photosynthesis
|
|
| Received: 2017-03-04 Revised: |
|
|
|
|
References:
Anderson J M, Chow W S, Park Y I. 1995. The grand design of photosynthesis:acclimation of the photosynthetic apparatus to environmental cues. Photosynthesis Research, 46(1-2):129-139.
Antal T K, Matorin D N, Ilyash L V, Volgusheva A A, Osipov V, Konyuhov I V, Krendeleva T E, Rubin A B. 2009.Probing of photosynthetic reactions in four phytoplanktonic algae with a PEA fluorometer.Photosynthesis Research, 102(1):67-76.
Baker D B, Confesor R, Ewing D E, Johnson L T, Kramer J W, Merryfield B J. 2014. Phosphorus loading to Lake Erie from the Maumee, Sandusky and Cuyahoga rivers:the importance of bioavailability. Journal of Great Lakes Research, 40(3):502-517.
Baker N R. 2008. Chlorophyll fluorescence:a probe of photosynthesis in vivo. Annual Review of Plant Biology, 59(1):89-113.
Baldia S F, Evangelista A D, Aralar E V, Santiago A E. 2007.Nitrogen and phosphorus utilization in the cyanobacterium Microcystis aeruginosa isolated from Laguna de Bay, Philippines. Journal of Applied Phycology, 19(6):607-613.
Bulgakov N G, Levich A P. 1999. The nitrogen:phosphorus ratio as a factor regulating phytoplankton community structure. Archiv für Hydrobiologie, 146(1):3-22.
Bullerjahn G S, Mckay R M, Davis T W, Baker D B, Boyer G L, D'Anglada L V, Doucette G J, Ho, J C, Irwin E G, Kling C L, Kudela R M, Kurmayer R, Michalak A M, Ortiz J D, Otten T G, Paerl H W, Qin B Q, Sohngen B L, Stumpf R P, Visser P M, Wilhelm S W. 2016. Global solutions to regional problems:collecting global expertise to address the problem of harmful cyanobacterial blooms. A Lake Erie case study. Harmful Algae, 54:223-238.
Cao X Y, Song C L, Zhou Y Y. 2010. Limitations of using extracellular alkaline phosphatase activities as a general indicator for describing P deficiency of phytoplankton in Chinese shallow lakes. Journal of Applied Phycology, 22(1):33-41.
Chen J Y, Qian Y, Li H R, Cheng Y H, Zhao M R. 2015. The reduced bioavailability of copper by nano-TiO2 attenuates the toxicity to Microcystis aeruginosa. Environmental Science and Pollution Research, 22(16):12 407-12 414.
Chróst R J, Overbeck J. 1987. Kinetics of alkaline phosphatase activity and phosphorus availability for phytoplankton and bacterioplankton in lake plußsee (North German Eutrophic Lake). Microbial Ecology, 13(3):229-248.
Collier J L, Grossman A R. 1994. A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. The EMBO Journal, 13(5):1 039-1 047.
Da Costa M V J, Sharma P K. 2016. Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa. Photosynthetica, 54(1):110-119.
Demmig-Adams B, Adams W W Ⅲ. 1992. Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology, 43(1):599-626.
Ding L P, Ma Y Y, Huang B X, Chen S W. 2013. Effects of seawater salinity and temperature on growth and pigment contents in Hypnea cervicornis J. Agardh (Gigartinales, Rhodophyta). BioMed Research International, 2013:Article ID 594308.
Ding Y, Qin B, Xu H, Wang X. 2016. Effects of sediment and turbulence on alkaline phosphatase activity and photosynthetic activity of phytoplankton in the shallow hyper-eutrophic Lake Taihu, China. Environmental Science and Pollution Research, 23(16):16 183-16 193.
Geider R J, MacIntyre H L, Kana T M. 1997. Dynamic model of phytoplankton growth and acclimation:responses of the balanced growth rate and the chlorophyll a:carbon ratio to light, nutrient-limitation and temperature. Marine Ecology Progress, 148(1-3):187-200.
Goldman J C. 1986. On phytoplankton growth rates and particulate C:N:P ratios at low light. Limnology and Oceanography, 31(6):1 358-1 363.
Guildford S J, Hecky R E. 2000. Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans:is there a common relationship? Limnology and Oceanography, 45(6):1 213-1 223.
Hafeman D G, Sunde R A, Hoekstra W G. 1974. Effect of dietary selenium on erythrocyte and liver glutathione peroxidase in the rat. The Journal of Nutrition, 104(5):580-587.
Harke M J, Gobler C J. 2013. Global transcriptional responses of the toxic cyanobacterium, Microcystis aeruginosa, to nitrogen stress, phosphorus stress, and growth on organic matter. PLoS One, 8(7):e69834.
Harke M J, Steffen M M, Gobler C J, Otten T G, Wilhelm S W, Wood S A, Paerl H W. 2016. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae, 54:4-20.
Healey F P. 1973. Characteristics of phosphorus deficiency in Anabaena. Journal of Phycology, 9(4):383-394.
Hecky R E, Kilham P. 1988. Nutrient limitation of phytoplankton in freshwater and marine environments:a review of recent evidence on the effects of enrichment.Limnology and Oceanography, 33(4part2):796-822.
Hu M H, Wu F L, Yuan M Z, Li Q Z, Gu Y D, Wang Y J, Liu Q G. 2015. Antioxidant responses of triangle sail mussel Hyriopsis cumingii exposed to harmful algae Microcystis aeruginosa and hypoxia. Chemosphere, 139:541-549.
Hu Z Q, Liu Y D, Li D H, Dauta A. 2005. Growth and antioxidant system of the cyanobacterium Synechococcus elongatus in response to microcystin-RR. Hydrobiologia, 534(1-3):23-29.
Huang H M, Xiao X, Ghadouani A, Wu J P, Nie Z Y, Peng C, Xu X H, Shi J Y. 2015. Effects of natural flavonoids on photosynthetic activity and cell integrity in Microcystis aeruginosa. Toxins, 7(1):66-80.
Huang Y, Bai Y, Wang Y, Kong H. 2013. Allelopathic effects of the extracts from an invasive species Solidago canadensis L. on Microcystis aeruginosa. Letters in Applied Microbiology, 57(5):451-458.
Hyenstrand P, Blomqvist P, Pettersson A. 1998. Factors determining cyanobacterial success in aquatic systems:a literature review. Archiv für Hydrobiologie:Special Issues Advances in Linmology, 51:41-62.
Jacobson L, Halmann M. 1982. Polyphosphate metabolism in the blue-green alga Microcystis aeruginosa. Journal of Plankton Research, 4(3):481-488.
Juneau P, Green B R, Harrison P J. 2005. Simulation of PulseAmplitude-Modulated (PAM) fluorescence:limitations of some PAM-parameters in studying environmental stress effects. Photosynthetica, 43(1):75-83.
Kane D D, Conroy J D, Richards R P, Baker D B, Culver D A. 2014. Re-eutrophication of Lake Erie:correlations between tributary nutrient loads and phytoplankton biomass. Journal of Great Lakes Research, 40(3):496-501.
Kromkamp J, van den Heuvel A, Mur L R. 1989. Phosphorus uptake and photosynthesis by phosphate-limited cultures of the cyanobacterium Microcystis aeruginosa. British Phycological Journal, 24(4):347-355.
Kuniyoshi T M, Sevilla E, Bes M T, Fillat M F, Peleato M L. 2013. Phosphate deficiency (N/P 40:1) induces mcyD transcription and microcystin synthesis in Microcystis aeruginosa PCC7806. Plant Physiology and Biochemistry, 65:120-124.
Li H Y, Xie P, Zhang D W, Chen, J. 2009. The first study on the effects of microcystin-RR on gene expression profiles of antioxidant enzymes and heat shock protein-70 in Synechocystis sp. PCC6803. Toxicon, 53(6):595-601.
Li X Y, Liu Y D, Song L R, Liu J T. 2003. Responses of antioxidant systems in the hepatocytes of common carp(Cyprinus carpio L.) to the toxicity of microcystin-LR.Toxicon, 42(1):85-89.
Liu Y, Chen S, Zhang J, Gao B Y. 2015. Nitrogen-regulated interactions between Microcystis aeruginosa and spiramycin contaminant. Water, Air, & Soil Pollution, 226(5):135.
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.
McCarthy M J, James R T, Chen Y W, East T L, Gardner W S. 2009. Nutrient ratios and phytoplankton community structure in the large, shallow, eutrophic, subtropical Lakes Okeechobee (Florida, USA) and Taihu (China).Limnology, 10(3):215-227.
Moisander P H, Ochiai M, Lincoff A. 2009. Nutrient limitation of Microcystis aeruginosa in northern California Klamath River reservoirs. Harmful Algae, 8(6):889-897.
Nalewajko C, Murphy T P. 2001. Effects of temperature, and availability of nitrogen and phosphorus on the abundance of Anabaena and Microcystis in Lake Biwa, Japan:an experimental approach. Limnology, 2(1):45-48.
Okubo Y, Inoue T, Yokota K. 2012. Estimating bioavailability of soil particulate phosphorus to Microcystis aeruginosa.Journal of Applied Phycology, 24(6):1 503-1 507.
Padgett M P, Krogmann D W. 1987. Large scale preparation of pure phycobiliproteins. Photosynthesis Research, 11(3):225-235.
Paerl H W, Otten T G. 2013. Harmful cyanobacterial blooms:causes, consequences, and controls. Microbial Ecology, 65(4):995-1 010.
Paerl H W, Scott J T, McCarthy M J, Newell S E, Garner W S, Havens K E, Hoffman D K, Wilhelm S W, Wurtsbaugh W A. 2016. It takes two to tango:when and where dual nutrient (N & P) reductions are needed to protect lakes and downstream ecosystems. Environmental Science & Technology, 50(20):10 805-10 813.
Parsons T R, Maita Y, Lalli C M. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford.
Peng G T, Fan Z Q, Wang X R, Chen C. 2016. Photosynthetic response to nitrogen source and different ratios of nitrogen and phosphorus in toxic cyanobacteria, Microcystis aeruginosa FACHB-905. Journal of Limnology, 75(3):560-570.
Peng G T, Fan Z Q, Wang X R, Sui X, Chen C. 2015.Photodegradation of microcystin-LR catalyzed by metal phthalocyanines immobilized on TiO2-SiO2 under visiblelight irradiation. Water Science & Technology, 72(10):1 824-1 831.
Petrou K, Kranz S A, Doblin M A, Ralph P J. 2012.Photophysiological responses of Fragilariopsis cylindrus(bacillariophyceae) to nitrogen depletion at two temperatures. Journal of Phycology, 48(1):127-136.
Pierangelini M, Stojkovic S, Orr P T, Beardall J, Lindell D. 2014. Photosynthetic characteristics of two Cylindrospermopsis raciborskii strains differing in their toxicity. Journal of Phycology, 50(2):292-302.
Placer Z A, Cushman L L, Johnson B C. 1966. Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Analytical Biochemistry, 16(2):359-364.
Platt T, Gallegos C, Harrison W. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Astronomical Society of Japan, 57(57):341-345.
Prasad S M, Dubey G. 2011. Growth, pigments and photosynthetic responses of two cyanobacteria adapted to varying light intensities. Plant Archives, 11(2):621-629.
Qian H F, Li J J, Pan X J, Sun Z Q, Ye C B, Jin G Q, Fu Z W. 2012. Effects of streptomycin on growth of algae Chlorella vulgaris and Microcystis aeruginosa. Environmental Toxicology, 27(4):229-237.
Rippka R, Deruelles J, Waterbury J B, Herdman M, Stanier R Y. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology, 111(1):1-61.
Schindler D W, Hecky R E, Findlay D L, Stainton M P, Parker B R, Paterson M J, Beaty K G, Lyng M, Kasian S E M. 2008. Eutrophication of lakes cannot be controlled by reducing nitrogen input:results of a 37-year wholeecosystem experiment. Proceedings of the National Academy of Sciences of the United States of America, 105(32):11 254-11 258.
Shelly K, Roberts S, Heraud P, Beardall J. 2005. Interactions between UV-B exposure and phosphorus nutrition. I.Effects on growth, phosphate uptake, and chlorophyll fluorescence. Journal of Phycology, 41(6):1 204-1 211.
Shi X L, Qian S Q, Kong F X, Zhang M, Yu Y. 2011. Differences in growth and alkaline phosphatase activity between Microcystis aeruginosa and Chlorella pyrenoidosa in response to media with different organic phosphorus.Journal of Limnology, 70(1):21-25.
Shi X L, Yang L Y, Niu X J, Xiao L, Kong Z M, Qin B Q, Gao G. 2003. Intracellular phosphorus metabolism of Microcystis aeruginosa under various redox potential in darkness. Microbiological Research, 158(4):345-352.
Shun Y, McKelvie I D, Hart B T. 1994. Determination of alkaline phosphatase-hydrolyzable phosphorus in natural water systems by enzymatic flow injection. Limnology and Oceanography, 39(8):1 993-2 000.
Singh V P, Srivastava P K, Prasad S M. 2012. Differential effect of UV-B radiation on growth, oxidative stress and ascorbate-glutathione cycle in two cyanobacteria under copper toxicity. Plant Physiology and Biochemistry, 61:61-70.
Steffen M M, Belisle B S, Watson S B, Boyer G L, Wilhelm S W. 2014a. Status, causes and controls of cyanobacterial blooms in Lake Erie. Journal of Great Lakes Research, 40(2):215-225.
Steffen M M, Dearth S P, Dill B D, Li Z, Larsen K M, Campagna S R, Wilhelm S W. 2014b. Nutrients drive transcriptional changes that maintain metabolic homeostasis but alter genome architecture in Microcystis.The ISME Journal, 8(10):2 080-2 092.
Steglich C, Behrenfeld M, Koblizek M, Claustre H, Penno S, Prasil O, Partensky F, Hess W R. 2001. Nitrogen deprivation strongly affects photosystem Ⅱ but not phycoerythrin level in the divinyl-chlorophyll bcontaining cyanobacterium Prochlorococcus marinus.Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1503(3):341-349.
Ting C S, Owens T G. 1992. Limitations of the pulse-modulated technique for measuring the fluorescence characteristics of algae. Plant Physiology, 100(1):367-373.
Wang Z C, Li D H, Li G W, Liu Y D. 2010. Mechanism of photosynthetic response in Microcystis aeruginosa PCC7806 to low inorganic phosphorus. Harmful Algae, 9(6):613-619.
White S, Anandraj A, Bux F. 2011. PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids. Bioresource Technology, 102(2):1 675-1 682.
Wiedner C, Visser P M, Fastner J, Metcalf J S, Codd G A, Mur L R. 2003. Effects of light on the microcystin content of Microcystis strain PCC 7806. Applied & Environmental Microbiology, 69(3):1 475-1 481.
Wilhelm S W, DeBruyn J M, Gillor O, Twiss M R, Livingston K, Bourbonniere R A, Pickell L D, Trick C G, Dean A L, McKay R M L. 2003. Effect of phosphorus amendments on present day plankton communities in pelagic Lake Erie. Aquatic Microbial Ecology, 32:275-285.
Winterbourn C C, Hawkins R E, Brian M, Carrell R W. 1975.The estimation of red cell superoxide dismutase activity.The Journal of Laboratory and Clinical Medicine, 85(2):337-341.
Yang Z, Kong F X, Shi X L, Yu Y, Zhang M. 2014. UV-B radiation and phosphorus limitation interact to affect the growth, pigment content, and photosynthesis of the toxic cyanobacterium Microcystis aeruginosa. Journal of Applied Phycology, 26(4):1 669-1 674.
|
|
|
|