Iron is a vital micronutrient for growth of bloom-forming Microcystis aeruginosa and competition with other algae, and its availability is affected by humic acid. The effect of iron and humic acid on growth and competition between M. aeruginosa and Scenedesmus obliquus was assessed. The results showed the growth of M. aeruginosa and S. obliquus in mono-cultures was inhibited by humic acid at low iron concentrations (0.01 mg/L); the maximum inhibition ratios were 67.84% and 38.31%, respectively. The inhibition of humic acid on the two species was significantly alleviated when iron concentrations were 1.00 mg/L, with the maximum inhibition rate reduced to 5.82% for M. aeruginosa and to 23.06% for S. obliquus. S. obliquus was the dominant species in mixed cultures, and the mutual inhibition between M. aeruginosa and S. obliquus at low iron concentration was greater than that at high iron concentration. The inhibition of S. obliquus on M. aeruginosa was reduced at low iron concentrations; it increased at high iron concentrations, as concentrations of humic acid rose.
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Agirbas E, Feyzioglu A M, Kopuz U, Llewellyn C A. 2015. Phytoplankton community composition in the southeastern Black Sea determined with pigments measured by HPLC-CHEMTAX analyses and microscopy cell counts. Journal of the Marine Biological Association of the United Kingdom, 95 (1): 35–52, https://doi.org/10.1017/S0025315414001040.
Alexova R, Fujii M, Birch D, Cheng J, Waite T D, Ferrari B C, Neilan B A. 2011. Iron uptake and toxin synthesis in the bloom-forming Microcystis aeruginosa under iron limitation. Environmental Microbiology, 4 (4): 13 4–1 064, https://doi.org/10.1111/j.1462-2920.2010.02412.x.
Andersen R A, Bidigare R R, Keller M D, Latasa M. 1996. A comparison of HPLC pigment signatures and electron microscopic observations for oligotrophic waters of the North Atlantic and Pacific Oceans. Deep Sea Research Part II: Topical Studies in Oceanography, 43 (2-3): 517–537, https://doi.org/10.1016/0967-0645(95)00095-X.
Backer L C, McNeel S V, Barber T, Kirkpatrick B, Williams C, Irvin M, Zhou Y, Johnson T B, Nierenberg K, Aubel M, LePrell R, Chapman A, Foss A, Corum S, Hill V R, Kieszak S M, Cheng Y S. 2010. Recreational exposure to microcystins during algal blooms in two California lakes. Toxicon, 55 (5): 909–921, https://doi.org/10.1016/j.toxicon.2009.07.006.
Benderliev K M, Ivanova N I. 1994. High-affinity siderophoremediated iron-transport system in the green alga Scenedesmus incrassatulus. Planta, 193 (2): 163–166, https://doi.org/10.1007/BF00192525.
Bidigare R R, Prezelin B B, Smith R C. 1992. Bio-optical models and the problems of scaling. In: Falkowski P G, Woodhead A D, Vivirito K, eds. Primary Productivity and Biogeochemical Cycles in the Sea. Boston: Springer. p.175–212, https://doi.org/10.1007/978-1-4899-0762-2_11.
Bittencourt-Oliveira M C, Chia M A, de Oliveira H S B, Araújo M K C, Molica R J R, Dias C T S. 2015. Allelopathic interactions between microcystin-producing and nonmicrocystin- producing cyanobacteria and green microalgae: implications for microcystins production. Journal of Applied Phycology, 27 (1): 275–284, https://doi.org/10.1007/s10811-014-0326-2.
Boopathi T, Ki J S. 2014. Impact of environmental factors on the regulation of cyanotoxin production. Toxins, 7 (7): 6 7–1 951, https://doi.org/10.3390/toxins6071951.
Brand L E. 1991. Minimum iron requirements of marine phytoplankton and the implications for the biogeochemical control of new production. Limnology and Oceanography, 8 (8): 36 8–1 756, https://doi.org/10.4319/lo.19188.8.131.526.
Brussaard C P D, Thyrhaug R, Marie D, Bratbak G. 1999. Flow cytometric analyses of viral infection in two marine phytoplankton species, Micromonas pusilla (Prasinophyceae) and Phaeocystis pouchetii (Prymnesiophyceae). Journal of Phycology, 35 (5): 941–948, https://doi.org/10.1046/j.1529-8817.1999.3550941.x.
Cao D J, Yue Y D, Huang X M, Wei M. 2004. Environmental quality assessment of Pb, Cu, Fe pollution in Chaohu Lake waters. China Environmental Science, 24 (4): 509–512. (in Chinese with English abstract)
Carey C C, Ibelings B W, Hoffmann E P, Hamilton D P, Brookes J D. 2012. Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Research, 5 (5): 46 5–1 394, https://doi.org/10.1016/j.watres.2011.12.016.
Chu Z S, Jin X C, Iwami N, Inamori Y. 2007. The effect of temperature on growth characteristics and competitions of Microcystis aeruginosa and Oscillatoria mougeotii in a shallow, eutrophic lake simulator system. In: Qin B, Liu Z, Havens K eds. Eutrophication of Shallow Lakes with Special Reference to Lake Taihu, China. Dordrecht: Springer. p.217–223, https://doi.org/10.1007/978-1-4020-6158-5_24.
Duan H T, Ma R H, Xu X F, Kong F X, Zhang S X, Kong W J, Hao J Y, Shang L L. 2009. Two-decade reconstruction of algal blooms in China’s Lake Taihu. Environmental Science and Technology, 10 (10): 43 10–3 522, https://doi.org/10.1021/es8031852.
Efteland S P. 2004. The Effects of Iron on Growth and Physiology of the Cyanobacterium Microcystis aeruginosa. University of Tennessee, Knoxville.
Fujimoto N, Sudo R, Sugiura N, Inamori Y. 1997. Nutrientlimited growth of Microcystis aeruginosa and Phormidium tenue and competition under various N:P supply ratios and temperatures. Limnology and Oceanography, 42 (2): 250–256, https://doi.org/10.4319/lo.1997.42.2.0250.
Gieskes W W C, Kraay G W. 1983. Dominance of cryptophyceae during the phytoplankton spring bloom in the central North Sea detected by HPLC analysis of pigments. Marine Biology, 75 (2-3): 179–185, https://doi.org/10.1007/BF00406000.
Guillard R R L, Murphy L S, Foss P, Liaaen-Jensen S. 1985. Synechococcus spp. as likely zeaxanthin-dominant ultraphytoplankton in the North Atlantic1. Limnology and Oceanography, 30 (2): 412–414, https://doi.org/10.4319/10.1985.30.2.0412.
Hallegraeff G M, Jeffrey S W. 1984. Tropical phytoplankton species and pigments of continental shelf waters of North and North-West Australia. Marine Ecology Progress Series, 20 (1): 59–74, https://doi.org/10.3354/meps020059.
Hallegraeff G M. 1981. Seasonal study of phytoplankton pigments and species at a coastal station off Sydney: importance of diatoms and the nanoplankton. Marine Biology, 61 (2-3): 107–118, https://doi.org/10.1007/BF00386650.
Ibelings B W, Backer L C, Kardinaal W E A, Chorus I. 2014. Current approaches to cyanotoxin risk assessment and risk management around the globe. Harmful Algae, 40: 63–74, https://doi.org/10.1016/j.hal.2014.10.002.
Imai A, Fukushima T, Matsushige K. 1999. Effects of iron limitation and aquatic humic substances on the growth of Microcystis aeruginosa. Canadian Journal of Fisheries and Aquatic Sciences, 10 (10): 56 10–1 929, https://doi.org/10.1139/f99-131.
Jeffrey S W, Hallegraeff G M. 1980. Studies of phytoplankton species and photosynthetic pigments in a warm core eddy of the East Australian Current. I. Summer population. Marine Ecology Progress Series, 3: 285–294, https://doi.org/10.3354/meps003285.
Jeffrey S W, Hallegraeff G M. 1987. Phytoplankton pigments, species and light climate in a complex warm-core eddy of the East Australian Current. Deep - Sea Research Part A. Oceanographic Research Papers, 34 (5-6): 649–673, https://doi.org/10.1016/0198-0149(87)90029-X.
Jeffrey S W. 1976. A report of green algal pigments in the central North Pacific Ocean. Marine Biology, 37 (1): 33–37, https://doi.org/10.1007/BF00386776.
Kerndorff H, Schnitzer M. 1980. Sorption of metals on humic acid. Geochimica et Cosmochimica Acta, 11 (11): 44 11–1 701, https://doi.org/10.1016/0016-7037(80)90221-5.
Koh C H, Shin H C. 1990. Growth and size distribution of some large brown algae in Ohori, east coast of Korea. Hydrobiologia, 204 (1): 225–231, https://doi.org/10.1007/BF00040238.
Kosakowska A, Lewandowska J, Ston J, Burkiewicz K. 2004. Qualitative and quantitative composition of pigments in Phaeodactylum tricornutum (Bacillariophyceae) stressed by iron. BioMetals, 17 (1): 45–52, https://doi.org/10.1023/A:1024452802005.
Kuhn K M, Maurice P A, Neubauer E, Hofmann T, von der Kammer F. 2014. Accessibility of humic-associated Fe to a microbial siderophore: implications for bioavailability. Environmental Science & Technology, 2 (2): 48 2–1 015, https://doi.org/10.1021/es404186v.
Li H J, Murphy T, Guo J, Parr T, Nalewajko C. 2009. Ironstimulated growth and microcystin production of Microcystis novacekii UAM 250. Limnologica, 39 (3): 255–259, https://doi.org/10.1016/j.limno.2008.08.002.
Llewellyn C A, Fishwick J R, Blackford J C. 2005. Phytoplankton community assemblage in the English Channel: a comparison using chlorophyll a derived from HPLC-CHEMTAX and carbon derived from microscopy cell counts. Journal of Plankton Research, 27 (1): 103–119, https://doi.org/10.1093/plankt/fbh158.
Lürling M, Roessink I. 2006. On the way to cyanobacterial blooms: impact of the herbicide metribuzin on the competition between a green alga ( Scenedesmus ) and a cyanobacterium (Microcystis). Chemosphere, 65 (4): 618–626, https://doi.org/10.1016/j.chemosphere.2006.01.073.
Lyck S, Gjølme N, Utkilen H. 1996. Iron starvation increases toxicity of Microcystis aeruginosa CYA 228/1 (Chroococcales, Cyanophyceae). Phycologia, 35 (S6): 120–124, https://doi.org/10.2216/i0031-8884-35-6S-120.1.
Mackey D J, Higgins H W, Mackey M D, Holdsworth D. 1998. Algal class abundances in the western equatorial Pacific: estimation from HPLC measurements of chloroplast pigments using CHEMTAX. Deep - Sea Research Part I: Oceanographic Research Papers, 45 (9):nyealcourt: 1 441–1 468, https://doi.org/10.1016/S0967-0637(98)00025-9.
Medrano E A, Uittenbogaard R E, Pires L M D, Van De Wiel B J H, Clercx H J H. 2013. Coupling hydrodynamics and buoyancy regulation in Microcystis aeruginosa for its vertical distribution in lakes. Ecological Modelling, 248: 41–56, https://doi.org/10.1016/j.ecolmodel.2012.08.029.
Meneely J P, Elliott C T. 2013. Microcystins: measuring human exposure and the impact on human health. Biomarkers, 18 (8): 639–649, https://doi.org/10.3109/1354750X.2013.841756.
Millie D F, Paerl H W, Hurley J P. 1993. Microalgal pigment assessments using high-performance liquid chromatography: a synopsis of organismal and ecological applications. Canadian Journal of Fisheries and Aquatic Sciences, 11 (11): 50 11–2 513, https://doi.org/10.1139/f93-275.
Murphy T P, Lean D R, Nalewajko C. 1976. Blue-green algae: their excretion of iron-selective chelators enables them to dominate other algae. Science, 192 (4242): 900–902, https://doi.org/10.1126/science.818707.
Nagai T, Imai A, Matsushige K, Fukushima T. 2007. Growth characteristics and growth modeling of Microcystis aeruginosa and Planktothrix agardhii under iron limitation. Limnology, 8 (3): 261–270, https://doi.org/10.1007/s10201-007-0217-1.
Nielsen S L. 2006. Size-dependent growth rates in eukaryotic and prokaryotic algae exemplified by green algae and cyanobacteria: comparisons between unicells and colonial growth forms. Journal of Plankton Research, 28 (5): 489–498, https://doi.org/10.1093/plankt/fbi134.
Rodriguez F, Varela M, Zapata M. 2002. Phytoplankton assemblages in the Gerlache and Bransfield Straits (Antarctic Peninsula) determined by light microscopy and CHEMTAX analysis of HPLC pigment data. Deep Sea Research Part II: Topical Studies in Oceanography, 49 (4-5): 723–747, https://doi.org/10.1016/S0967-0645(01)00121-7.
Rueler J G, Ades D R. 1987. The role of iron nutrition in photosynthesis and nitrogen assimilation in Scenedesmus quadricauda (Chlorophyceae). Journal of Phycology, 23 (3): 452–457, https://doi.org/10.1111/j.1529-8817.1987tb02531.x..
Schlesinger D A, Molot L A, Shuter B J. 1981. Specific growth rates of freshwater algae in relation to cell size and light intensity. Canadian Journal of Fisheries and Aquatic Sciences, 9 (9): 38 9–1 052, https://doi.org/10.1139/f81-145.
Shen H, Niu Y, Xie P, Tao M, Yang X. 2011. Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria. Freshwater Biology, 6 (6): 56 6–1 065, https://doi.org/10.1111/j.1365-2427.2010.02551.x.
Song K S, Shang Y X, Wen Z D, Jacinthe P A, Liu G, Lyu L, Fang C. 2019. Characterization of CDOM in saline and freshwater lakes across China using spectroscopic analysis. Water Research, 150: 403–417, https://doi.org/10.1016/j.watres.2018.12.004.
Sun B K, Tanji Y, Unno H. 2005. Infl uences of iron and humic acid on the growth of the cyanobacterium Anabaena circinalis. Biochemical Engineering Journal, 24 (3): 195–201, https://doi.org/10.1016/j.bej.2005.02.014.
Trainor F R. 1998. Biological aspects of Scenedesmus (Chlorophyceae)-phenotypic plasticity. In: Nova Hedwigia: Beihefte 117. Berlin: J. Cramer.
Verstreate D R, Storch T A, Dunham V L. 1980. A comparison of the infl uence of iron on the growth and nitrate metabolism of Anabaena and Scenedesmus. Physiologia Plantarum, 50 (1): 47–51, https://doi.org/10.1111/j.1399-3054.1980.tb02682.x.
Volterra V. 1926. Fluctuations in the abundance of a species considered mathematically. Nature, 118 (2972): 558–560, https://doi.org/10.1038/118558a0.
Wang Y W, Wu M, Yu J, Zhang J J, Zhang R F, Zhang L, Chen G X. 2014. Differences in growth, pigment composition and photosynthetic rates of two phenotypes Microcystis aeruginosa strains under high and low iron conditions. Biochemical Systematics and Ecology, 55: 112–117, https://doi.org/10.1016/j.bse.2014.02.019.
Wilhelm C, Rudolph I, Renner W. 1991. A quantitative method based on HPLC-aided pigment analysis to monitor structure and dynamics of the phytoplankton assemblage-a study from Lake Meerfelder Maar (Eifel, Germany). Archiv Fur Hydrobiologie, 123 (1): 21–35.
Wright S W, Thomas D P, Marchant H J, Higgins H W, Mackey M D, Mackey D J. 1996. Analysis of phytoplankton of the Australian sector of the Southern Ocean: comparisons of microscopy and size frequency data with interpretations of pigment HPLC data using the ‘CHEMTAX’ matrix factorisation program. Marine Ecology Progress Series, 144: 285–298, https://doi.org/10.3354/meps144285.
Xie L Q, Xie P, Li S X, Tang H J, Liu H. 2003. The low TN:TP ratio, a cause or a result of Microcystis blooms? Water Research, 9 (9): 37 9–2 073, https://doi.org/10.1016/S0043-1354(02)00532-8.
Xing W, Huang W M, Li D H, Liu Y D. 2007. Effects of iron on growth, pigment content, photosystem II efficiency, and siderophores production of Microcystis aeruginosa and Microcystis wesenbergii. Current Microbiology, 55 (2): 94–98, https://doi.org/10.1007/s00284-006-0470-2.
Xu H, Zhu G W, Qin B Q, Paerl H W. 2013. Growth response of Microcystis spp. to iron enrichment in different regions of Lake Taihu, China. Hydrobiologia, 700 (1): 187–202, https://doi.org/10.1007/s10750-012-1229-3.
Yu G Y, Zhang X H, Liang X M, Xu X Q. 2000. Biogeochemical characteristics of metal elements in water-plant system of lake Dianchi. Acta Hydrobiologica Sinica, 24 (2): 172–177, https://doi.org/10.3321/j.issn:1000-3207.2000.02.012. (in Chinese with English abstract)
Zhang P, Zhai C M, Wang X X, Liu C H, Jiang J H, Xue Y R. 2013. Growth competition between Microcystis aeruginosa and Quadrigula chodatii under controlled conditions. Journal of Applied Phycology, 25 (2): 555–565, https://doi.org/10.1007/s10811-012-9890-5.
Zhang Z P, Zhu G W, Sun X J, Chi Q Q. 2008. Seasonal variation of colloidal trace-metal concentration in Lake Taihu water body. China Environmental Science, 28 (6): 556–560. (in Chinese with English abstract)
Zhou T, Wang Z H, Hu Q, Liu L F, Luo K S. 2016. Effects of Fe2+ and Fe3+ on algal proliferation in a natural mixed algal colony in algae-rich raw water in Southern China. Journal of Residuals Science & Technology, 13 (1): 15–22, https://doi.org/10.12783/issn.1544-8053/13/1/3.
Zhu W, Chen H M, Guo L L, Li M. 2016. Effects of linear alkylbenzene sulfonate (LAS) on the interspecific competition between Microcystis and Scenedesmus. Environmental Science and Pollution Research, 16 (16): 23 16–16 194, https://doi.org/10.1007/s11356-016-6809-8.
We thank Elaine Monaghan, BSc (Econ), from Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), for editing the English text of draft of this manuscript.
Supported by the Sichuan Science and Technology Program (No. 2019YFH0127), the Joint Foundation of Shaanxi (No. 2019JLM-59), the Scientifi c and Technological Innovation Team of Water Ecological Security for Water Source Region of Mid-line of South-to-North Diversion Project of Henan Province (No. 17454)
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Zhao, M., He, Q., Chen, C. et al. Effects of iron and humic acid on competition between Microcystis aeruginosa and Scenedesmus obliquus revealed by HPLC analysis of pigments. J. Ocean. Limnol. (2020). https://doi.org/10.1007/s00343-020-0012-y
- humic acid