Cyanobacterial extracellular alkaline phosphatase: detection and ecological function

Lingling WAN; Chunlei SONG; Yiyong ZHOU; Xiuyun CAO

doi:10.1007/s00343-022-2112-3

Your Location：

Home >

Browse articles >

Cyanobacterial extracellular alkaline phosphatase: detection and ecological function

Special Section: Cyanobacterial blooms in China: ecology, toxicity, and treatment | Updated：2023-05-19

- Cyanobacterial extracellular alkaline phosphatase: detection and ecological function
- Journal of Oceanology and Limnology Vol. 40, Issue 5, Pages: 1840-1854(2022)
- Affiliations：
  
  Key Laboratory of Algal Biology, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China
- Author bio：
  
  Xiuyun CAO,caoxy@ihb.ac.cn
- Funds：
- DOI：10.1007/s00343-022-2112-3
  CLC：
- Received：11 March 2022，
  
  Accepted：15 April 2022，
  
  Online First：01 July 2022，
  
  Published：2022-09
- Accepted：
Scan QR Code
Lingling WAN, Chunlei SONG, Yiyong ZHOU, et al. Cyanobacterial extracellular alkaline phosphatase: detection and ecological function[J]. Journal of Oceanology and Limnology, 2022, 40(5): 1840-1854.
DOI：

Lingling WAN, Chunlei SONG, Yiyong ZHOU, et al. Cyanobacterial extracellular alkaline phosphatase: detection and ecological function[J]. Journal of Oceanology and Limnology, 2022, 40(5): 1840-1854. DOI： 10.1007/s00343-022-2112-3.

摘要

Abstract

Dissolved inorganic phosphorus is an important form of directly bioavailable phosphorus for cyanobacteria in natural water. Dissolved organic phosphorus could be used by cyanobacteria via alkaline phosphatase

which is produced mainly by bacteria and also cyanobacteria itself. Herein

we review the current knowledge of extracellular phosphatase excreted by cyanobacteria

highlighting the development of detection method and its ecological roles in regulating phosphorus cycling in freshwater systems

which is based on reports for around 100 species of cyanobacteria. Recommendations are suggested concerning the extracellular phosphatase produced by bloom-forming cyanobacteria in terms of the ecological role

followed by a discussion of the future prospects for the study.

关键词

Keywords

references

Accoroni S, Totti C, Razza E et al. 2017. Phosphatase activities of a microepiphytic community during a bloom of Ostreopsis cf. ovata in the northern Adriatic Sea. Water Research , 120 : 272-279, https://doi.org/10.1016/j.watres.2017.05.004.

Aguilera A, Aubriot L, Echenique R O et al. 2019. Raphidiopsis mediterranea (Nostocales) exhibits a flexible growth strategy under light and nutrient fluctuations in contrast to Planktothrix agardhii (Oscillatoriales). Hydrobiologia , 839 (1): 145-157, https://doi.org/10.1007/s10750-019-04002-5.

Asencio A D, Morte A, García-Carmona F et al. 2012. Partial purification and characterization of a calcium-dependent alkaline phosphatase from the cyanobacterium Arthrospira platensis . Journal of Phycology , 48 (2): 347-354, https://doi.org/10.1111/j.1529-8817.2012.01119.x.

Bai F, Liu R, Yang Y J et al. 2014. Dissolved organic phosphorus use by the invasive freshwater diazotroph cyanobacterium, Cylindrospermopsis raciborskii . Harmful Algae , 39 : 112-120, https://doi.org/10.1016/j.hal.2014.06.015.

Bai X L, Zhou Y K, Ye W N et al. 2021. Response of organic phosphorus in lake water to environmental factors: a simulative study. Science of the Total Environment , 785 : 147275, https://doi.org/10.1016/j.scitotenv.2021.147275.

Baken S, Nawara S, Van Moorleghem C et al. 2014. Iron colloids reduce the bioavailability of phosphorus to the green alga Raphidocelis subcapitata . Water Research , 59 : 198-206, https://doi.org/10.1016/j.watres.2014.04.010.

Bar-Yosef Y, Sukenik A, Hadas O et al. 2010. Enslavement in the water body by toxic Aphanizomenon ovalisporum , inducing alkaline phosphatase in phytoplanktons. Current Biology , 20 (17): 1557-1561, https://doi.org/10.1016/j.cub.2010.07.032.

Bentzen E, Taylor W D, Millard E S. 1992. The importance of dissolved organic phosphorus to phosphorus uptake by limnetic plankton. Limnology and Oceanography , 37 (2): 217-231, https://doi.org/10.4319/lo.1992.37.2.0217.

Berman T. 1970. Alkaline phosphatases and phosphorus availability in Lake Kinneret. Limnology and Oceanography , 15 (5): 663-674, https://doi.org/10.4319/lo.1970.15.5.0663.

Björkman K, Karl D M. 1994. Bioavailability of inorganic and organic phosphorus compounds to natural assemblages of microorganisms in Hawaiian coastal waters. Marine Ecology Progress Series , 111 (3): 265-273, https://doi.org/10.3354/meps111265.

Cao X Y, Song C L, Li Q M et al. 2007. Dredging effects on P status and phytoplankton density and composition during winter and spring in Lake Taihu, China. Hydrobiologia , 581 : 287-295, https://doi.org/10.1007/s10750-006-0516-2.

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, https://doi.org/10.1007/s10811-009-9422-0.

Cao X Y, Štrojsová, Znachor P et al. 2005. Detection of extracellular phosphatases in natural spring phytoplankton of a shallow eutrophic lake (Donghu, China). European Journal of Phycology , 40 (3): 251-258, https://doi.org/10.1080/09670260500192760.

Cao X Y, Wan L L, Xiao J et al. 2018. Environmental effects by introducing Potamogeton crispus to recover a eutrophic lake. Science of the Total Environment , 621 : 360-367, https://doi.org/10.1016/j.scitotenv.2017.11.267.

Cembella A D, Antia N J, Harrison P J. 1982. The utilization of inorganic and organic phosphorous compounds as nutrients by eukaryotic microalgae: a multidisciplinary perspective: part Ⅰ. CRC Critical Reviews in Microbiology , 10 (4): 317-391, https://doi.org/10.3109/10408418209113567.

Chen X Y, Dolinova I, Sevcu A et al. 2020. Strategies adopted by Aphanizomenon flos - aquae in response to phosphorus deficiency and their role on growth. Environmental Sciences Europe , 32 (1): 45, https://doi.org/10.1186/s12302-020-00328-3.

Chróst R J, Siuda W, Halemejko G Z. 1984. Longterm studies on alkaline phosphatase activity (APA) in a lake with fish-aquaculture in relation to lake eutrophication and phosphorus cycle. Archiv für Hydrobiologie , 70 (1): 1-32.

Chróst R J. 1991. Environmental control of the synthesis and activity of aquatic microbial ectoenzymes. In : Chróst R J ed. Microbial Enzymes in Aquatic Environments. Springer, New York. p. 29-59, https://doi.org/10.1007/978-1-4612-3090-8_3 https://doi.org/10.1007/978-1-4612-3090-8_3 .

Chuai X M, Ding W, Chen X F et al. 2011. Phosphorus release from cyanobacterial blooms in Meiliang Bay of Lake Taihu, China. Ecological Engineering , 37 (6): 842-849, https://doi.org/10.1016/j.ecoleng.2011.01.001.

Cotner J B, Wetzel R G. 1992. Uptake of dissolved inorganic and organic bphosphorus compounds by phytoplankton and bacterioplankton. Limnology and Oceanography , 37 (2): 232-243, https://doi.org/10.4319/lo.1992.37.2.0232.

Cox A D, Saito M A. 2013. Proteomic responses of oceanic Synechococcus WH8102 to phosphate and zinc scarcity and cadmium additions. Frontiers in Microbiology , 4 : 387, https://doi.org/10.3389/fmicb.2013.00387.

Dai J Y, Chen D, Wu S Q et al. 2018. Dynamics of phosphorus and bacterial phoX genes during the decomposition of Microcystis blooms in a mesocosm. PLoS One , 13 (5): e0195205, https://doi.org/10.1371/journal.pone.0195205.

de Souza Santos K R, Jacinavicius F R, Sant'Anna C L. 2011. Effects of the pH on growth and morphology of Anabaenopsis elenkinii Miller (Cyanobacteria) isolated from the alkaline shallow lake of the Brazilian Pantanal. Fottea , 11 (1): 119-126, https://doi.org/10.5507/fot.2011.012.

Degerholm J, Gundersen K, Bergman B et al. 2006. Phosphorus-limited growth dynamics in two Baltic Sea cyanobacteria, Nodularia sp. and Aphanizomenon sp. FEMS Microbiology Ecology , 58 (3): 323-332, https://doi.org/10.1111/j.1574-6941.2006.00180.x.

Diaz-de-Quijano D, Palacios P, Horňák K et al. 2014. 3D restoration microscopy improves quantification of enzyme-labeled fluorescence-based single-cell phosphatase activity in plankton. Cytometry Part A , 85 (10): 841-853, https://doi.org/10.1002/cyto.a.22486.

Diaz-de-Quijano D, Stratmann C N, Berger S A. 2020. DIY enzyme labelled fluorescence alcohol (ELFA) standard production protocol to quantify single-cell phosphatase activity (SCPA) of microplankton. Heliyon , 6 (11): e05582, https://doi.org/10.1016/j.heliyon.2020.e05582.

Dignum M, Hoogveld H L, Floris V et al. 2004a. Flow cytometric detection of phosphatase activity combined with 13 C-CO 2 tracer-based growth rate assessment in phytoplankton populations from a shallow lake. Aquatic Microbial Ecology , 37 (2): 159-169, https://doi.org/10.3354/ame037159.

Dignum M, Hoogveld H L, Matthijs H C P et al. 2004b. Detecting the phosphate status of phytoplankton by enzyme-labelled fluorescence and flow cytometry. FEMS Microbiology Ecology , 48 (1): 29-38, https://doi.org/10.1016/j.femsec.2003.12.007.

Dobronoki D, B-Béres V, Vasas G et al. 2019. Potential role of the cellular matrix of Aphanizomenon strains in the effects of cylindrospermopsin-an experimental study. Journal of Applied Phycology , 31 (3): 1805-1817, https://doi.org/10.1007/s10811-018-1699-4.

Doonan B B, Jensen T E. 1980. Physiological aspects of alkaline phosphatase in selected cyanobacteria. Microbios , 29 (117-118): 185-207.

Dyhrman S T, Palenik B. 1999. Phosphate stress in cultures and field populations of the dinoflagellate Prorocentrum minimum detected by a single-cell alkaline phosphatase assay. Applied and Environmental Microbiology , 65 (7): 3205-3212, https://doi.org/10.1128/aem.65.7.3205-3212.1999.

Dyhrman S T, Ruttenberg K C. 2006. Presence and regulation of alkaline phosphatase activity in eukaryotic phytoplankton from the coastal ocean: implications for dissolved organic phosphorus remineralization. Limnology and Oceanography , 51 (3): 1381-1390.

Dyhrman S. 2005. Ectoenzymes in Prorocentrum minimum . Harmful Algae , 4 (3): 619-627, https://doi.org/10.1016/j.hal.2004.08.011.

Fang F, Gao Y, Gan L et al. 2018. Effects of different initial pH and irradiance levels on cyanobacterial colonies from Lake Taihu, China. Journal of Applied Phycology , 30 (3): 1777-1793, https://doi.org/10.1007/s10811-018-1394-5.

Feng W Y, Yang F, Zhang C et al. 2020. Composition characterization and biotransformation of dissolved, particulate and algae organic phosphorus in eutrophic lakes. Environmental Pollution , 265 : 114838, https://doi.org/10.1016/j.envpol.2020.114838.

Fernández-Juárez V, Bennasar-Figueras A, Tovar-Sanchez A et al. 2019. The role of iron in the p-acquisition mechanisms of the unicellular N 2 -fixing cyanobacteria Halothece sp., found in association with the Mediterranean Seagrass Posidonia oceanica . Frontiers in Microbiology , 10 : 1903, https://doi.org/10.3389/fmicb.2019.01903.

Feuillade J, Feuillade M, Blanc P. 1990. Alkaline-phosphatase activity fluctuations and associated factors in a eutrophic lake dominated by Oscillatoria - rubescens . Hydrobiologia , 207 : 233-240, https://doi.org/10.1007/Bf00041461.

Fitzgerald G P, Nelson T C. 1975. Extractive and enzymatic analyses for limiting or surplus phosphorus in algae. Journal of Phycology , 11 (S1): 32-37, https://doi.org/10.1111/j.1529-8817.1975.tb04539.x.

Fonseca-De-Souza A L, Dick C F, Dos Santos A L A et al. 2008. A Mg 2+ -dependent ecto-phosphatase activity on the external surface of Trypanosoma rangeli modulated by exogenous inorganic phosphate. Acta Tropica , 107 (2): 153-158, https://doi.org/10.1016/j.actatropica.2008.05.017.

Francko D A, Wetzel R G. 1982. The isolation of cyclic adenosine 3'-5'-monophosphate (camp) from lakes of differing trophic status: correlation with planktonic metabolic variables. Limnology and Oceanography , 27 (1): 27-38, https://doi.org/10.4319/lo.1982.27.1.0027.

Francko D A. 1984. Relationships between phosphorus functional classes and alkaline phosphatase activity in reservoir lakes. Journal of Freshwater Ecology , 2 (6): 541-547, https://doi.org/10.1080/02705060.1984.9664636.

Gao G, Zhu G W, Qin B Q et al. 2006. Alkaline phosphatase activity and the phosphorus mineralization rate of Lake Taihu. Science in China Series D , 49 (1): 176-185, https://doi.org/10.1007/s11430-006-8117-5.

Gerloff G C, Fitzgerald G P, Skoog F. 1950. The isolation, purification, and culture of blue-green algae. American Journal of Botany , 37 (3): 216-218, https://doi.org/10.2307/2437904.

Giraudet H, Abrial D, Berthon J L et al. 1999. Seasonal variation of the alkaline phosphatase activity of phytoplankton in the hypereutrophic Grangent reservoir (Loire). Annales De Limnologie - International Journal of Limnology , 35 (4): 213-221, https://doi.org/10.1051/limn/1999030.

Giraudet H, Berthon J L, Buisson B. 1997. A comparison of the daily alkaline phosphatase activity of a cyanobacterium ( Microcystis aeruginosa ) and a diatom ( Synedra capitata ). Comptes Rendus De L'académie Des Sciences - Series Ⅲ - Sciences De La Vie , 320 (6): 451-458, https://doi.org/10.1016/s0764-4469(97)81972-5.

Girault M, Arakawa H, Hashihama F. 2013. Phosphorus stress of microphytoplankton community in the western subtropical North Pacific. Journal of Plankton Research , 35 (1): 146-157, https://doi.org/10.1093/plankt/fbs076.

González-Gil S, Keafer B A, Jovine R V M et al. 1998. Detection and quantification of alkaline phosphatase in single cells of phosphorus-starved marine phytoplankton. Marine Ecology Progress Series , 164 : 21-35, https://doi.org/10.3354/meps164021.

Hadas O, Pinkas R, Delphine E et al. 1999. Limnological and ecophysiological aspects of Aphanizomenon ovalisporum bloom in Lake Kinneret, Israel. Journal of Plankton Research , 21 (8): 1439-1453, https://doi.org/10.1093/plankt/21.8.1439.

Harke M J, Berry D L, Ammerman J W et al. 2012. Molecular response of the bloom-forming cyanobacterium, Microcystis aeruginosa , to phosphorus limitation. Microbial Ecology , 63 (1): 188-198, https://doi.org/10.1007/s00248-011-9894-8.

Harke M J, Davis T W, Watson S B et al. 2016. Nutrient-controlled niche differentiation of western lake Erie Cyanobacterial populations revealed via metatranscriptomic surveys. Environmental Science & Technology , 50 (2): 604-615, https://doi.org/10.1021/acs.est.5b03931.

Healey F P, Hendzel L L. 1979a. Indicators of phosphorus and nitrogen deficiency in five algae in culture. Journal of the Fisheries Research Board of Canada , 36 (11): 1364-1369, https://doi.org/10.1139/f79-195.

Healey F P, Hendzel L L. 1979b. Fluorometric measurement of alkaline phosphatase activity in algae. Freshwater Biology , 9 (5): 429-439, https://doi.org/10.1111/j.1365-2427.1979.tb01527.x.

Healey F P, Hendzel L L. 1980. Physiological indicators of nutrient deficiency in lake phytoplankton. Canadian Journal of Fisheries and Aquatic Sciences , 37 (3): 442-453, https://doi.org/10.1139/f80-058.

Healey F P. 1978. Physiological indicators of nutrient deficiency in algae. SIL Communications , 1953 - 1996 , 21 (1): 34-41, https://doi.org/10.1080/05384680.1978.11903948.

Hernández I, Hwang S J, Heath R T. 1996. Measurement of phosphomonoesterase activity with a radiolabelled glucose-6-phosphate. Role in the phosphorus requirement of phytoplankton and bacterioplankton in a temperate mesotrophic lake. Archiv für Hydrobiologie , 137 (2): 265-280, https://doi.org/10.1127/archiv-hydrobiol/137/1996/265.

Hernández I, Whitton B A. 1996. Retention of p-nitrophenol and 4-methylumbelliferone by marine macroalgae and implications for measurement of alkaline phosphatase activity. Journal of Phycology , 32 (5): 819-825, https://doi.org/10.1111/j.0022-3646.1996.00819.x.

Hong S J, Lee C G. 2008. Statistical optimization of culture media for production of phycobiliprotein by Synechocystis sp. PCC 6701. Biotechnology and Bioprocess Engineering , 13 (4): 491-498, https://doi.org/10.1007/s12257-008-0154-9.

Hong S J, Pan Q H, Chen S Y et al. 2021. Identification and characterization of alkaline phosphatase gene phoX in Microcystis aeruginosa PCC7806. 3 Biotech , 11 (5): 218, https://doi.org/10.1007/s13205-021-02774-z.

Hoppe H G. 2003. Phosphatase activity in the sea. Hydrobiologia , 493 (1-3): 187-200, https://doi.org/10.1023/A:1025453918247.

Hsieh Y J, Wanner B L. 2010. Global regulation by the seven-component P i signaling system. Current Opinion in Microbiology , 13 (2): 198-203, https://doi.org/10.1016/j.mib.2010.01.014.

Hynes A M, Chappell P D, Dyhrman S T et al. 2009. Cross-basin comparison of phosphorus stress and nitrogen fixation in Trichodesmium . Limnology and Oceanography , 54 (5): 1438-1448, https://doi.org/10.4319/lo.2009.54.5.1438.

Ihlenfeldt M J A, Gibson J. 1975. Phosphate utilization and alkaline phosphatase activity in Anacystis nidulans ( Synechococcus ). Archives of Microbiology , 102 (1): 23-28, https://doi.org/10.1007/BF00428340.

Istánovics V, Pettersson K, Pierson D et al. 1992. Evaluation of phosphorus deficiency indicators for summer phytoplankton in Lake Erken. Limnology and Oceanography , 37 (4): 890-900, https://doi.org/10.4319/lo.1992.37.4.0890.

Ivančić I, Kraus R, Najdek M et al. 2021. Ecological importance of alkaline phosphatase activity in changing marine environmental conditions. Water , 13 (19): 2750, https://doi.org/10.3390/w13192750.

Jamet D, Amblard C, Devaux J. 2001. Size-fractionated alkaline phosphatase activity in the hypereutrophic Villerest Reservoir (Roanne, France). Water Environment Research , 73 (2): 132-141, https://doi.org/10.2175/106143001X138787.

Jansson M, Olsson H, Pettersson K. 1988. Phosphatases: origin, characteristics and function in lakes. Hydrobiologia , 170 : 157-175, https://doi.org/10.1007/BF00024903.

Jansson M. 1976. Phosphatases in lake water: characterization of enzymes from phytoplankton and zooplankton by gel filtration. Science , 194 (4262): 320-321, https://doi.org/10.1126/science.184531.

Jansson M. 1981. Induction of high phosphatase activity by aluminum in acid lakes. Archiv für Hydrobiologie , 93 (1): 32-44.

Juntarajumnong W, Hirani T A, Simpson J M et al. 2007. Phosphate sensing in Synechocystis sp. PCC 6803: SphU and the SphS-SphR two-component regulatory system. Archives of Microbiology , 188 (4): 389-402, https://doi.org/10.1007/s00203-007-0259-0.

Kageyama H, Tripathi K, Rai A K et al. 2011. An alkaline phosphatase/phosphodiesterase, PhoD, induced by salt stress and secreted out of the cells of Aphanothece halophytica , a halotolerant cyanobacterium. Applied and Environmental Microbiology , 77 (15): 5178-5183, https://doi.org/10.1128/AEM.00667-11.

Kathuria S, Martiny A C. 2011. Prevalence of a calcium-based alkaline phosphatase associated with the marine cyanobacterium Prochlorococcus and other ocean bacteria. Environmental Microbiology , 13 (1): 74-83, https://doi.org/10.1111/j.1462-2920.2010.02310.x.

Kelly L T, Ryan K G, Wood S A. 2019. Differential strain response in alkaline phosphatase activity to available phosphorus in Microcoleus autumnalis . Harmful Algae , 89 : 101664, https://doi.org/10.1016/j.hal.2019.101664.

Koch M S, Kletou D C, Tursi R. 2009. Alkaline phosphatase activity of water column fractions and seagrass in a tropical carbonate estuary, Florida Bay. Estuarine , Coastal and Shelf Science , 83 (4): 403-413, https://doi.org/10.1016/j.ecss.2009.04.007.

Kolowith L C, Ingall E D, Benner R. 2001. Composition and cycling of marine organic phosphorus. Limnology and Oceanography , 46 (2): 309-320, https://doi.org/10.2307/2670868.

Kuenzler E J, Perras J P. 1965. Phosphatases of marine algae. The Biological Bulletin , 128 (2): 271-284, https://doi.org/10.2307/1539555.

Kumar D, Singh J B, Kumar H D. 1992. Effects of low temperature on two cyanobacteria. The Journal of General and Applied Microbiology , 38 (3): 263-270, https://doi.org/10.2323/jgam.38.263.

Lehman J T, Doubek J P, Jackson E W. 2013. Effect of reducing allochthonous P load on biomass and alkaline phosphatase activity of phytoplankton in an urbanized watershed, Michigan. Lake and Reservoir Management , 29 (2): 116-125, https://doi.org/10.1080/10402381.2013.800173.

Li J H, Wang Z W, Cao X et al. 2015a. Effect of orthophosphate and bioavailability of dissolved organic phosphorous compounds to typically harmful cyanobacterium Microcystis aeruginosa . Marine Pollution Bulletin , 92 (1-2): 52-58, https://doi.org/10.1016/j.marpolbul.2015.01.001.

Li T L, Zheng L L, Zhang Q et al. 2015b. Progress of aseptic purification technique of cyanobacteria. Current Biotechnology , 5 (5): 329-334, https://doi.org/110.3969/j.issn.2095-2341.20150.5.01. (in Chinese with English abstract)

Lim J H, Lee C W, Bong C W et al. 2018. Distributions of particulate and dissolved phosphorus in aquatic habitats of Peninsular Malaysia. Marine Pollution Bulletin , 128 : 415-427, https://doi.org/10.1016/j.marpolbul.2018.01.037.

Lin S J, Litaker R W, Sunda W G. 2016. Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton. Journal of Phycology , 52 (1): 10-36, https://doi.org/10.1111/jpy.12365.

Lin W T, Zhao D D, Luo J F. 2018. Distribution of alkaline phosphatase genes in cyanobacteria and the role of alkaline phosphatase on the acquisition of phosphorus from dissolved organic phosphorus for cyanobacterial growth. Journal of Applied Phycology , 30 (2): 839-850, https://doi.org/10.1007/s10811-017-1267-3.

Liu Z Y, Wu C D. 2012. Response of alkaline phosphatases in the cyanobacterium Anabaena sp. FACHB 709 to inorganic phosphate starvation. Current Microbiology , 64 (6): 524-529, https://doi.org/10.1007/s00284-012-0101-z.

Livingstone D, Whitton B A. 1984. Water chemistry and phosphatase activity of the blue-green alga Rivularia in upper Teesdale Streams. The Journal of Ecology , 72 (2): 405-421, https://doi.org/10.2307/2260055.

Lu Z, Lei L M, Lu Y et al. 2021. Phosphorus deficiency stimulates dominance of Cylindrospermopsis through facilitating cylindrospermopsin-induced alkaline phosphatase secretion: integrating field and laboratory-based evidences. Environmental Pollution , 290 : 117946, https://doi.org/https://doi.org/10.1016/j.envpol.2021.117946.

Luo H W, Benner R, Long R A et al. 2009. Subcellular localization of marine bacterial alkaline phosphatases. Proceedings of the National Academy of Sciences of the United States of America , 106 (50): 21219-21223, https://doi.org/10.1073/pnas.0907586106.

Luo M, Guo Y C, Deng J Y et al. 2010. Characterization of a monomeric heat-labile classical alkaline phosphatase from Anabaena sp. PCC7120. Biochemistry ( Moscow ), 75 (5): 655-664, https://doi.org/10.1134/S0006297910050172.

Majumdar A, Ghatak A, Ghosh R K. 2005. Identification of the gene for the monomeric alkaline phosphatase of Vibrio cholerae serogroup O1 strain. Gene , 344 : 251-258, https://doi.org/10.1016/j.gene.2004.11.005.

Malherbe G, Humphreys D P, Dave E. 2019. A robust fractionation method for protein subcellular localization studies in Escherichia coli . Biotechniques , 66 (4): 171-178, https://doi.org/10.2144/btn-2018-0135.

Martland M, Robison R. 1929. The preparation and use of the bone phosphatase. Biochemical Journal , 23 (2): 237-242, https://doi.org/10.1042/bj0230237.

McComb R B, Bowers Jr G N, Posen S. 1979. Purification. In : McComb R B, Bowers G N, Posen S eds. Alkaline Phosphatase. Springer, Boston. p. 153-188, https://doi.org/10.1007/978-1-4613-2970-1_4 https://doi.org/10.1007/978-1-4613-2970-1_4 .

McLaughlin K, Sohm J A, Cutter G A et al. 2013. Phosphorus cycling in the Sargasso Sea: investigation using the oxygen isotopic composition of phosphate, enzyme-labeled fluorescence, and turnover times. Global Biogeochemical Cycles , 27 (2): 375-387, https://doi.org/10.1002/gbc.20037.

Meseck S L, Alix J H, Wikfors G H et al. 2009. Differences in the soluble, residual phosphate concentrations at which coastal phytoplankton species up-regulate alkaline-phosphatase expression, as measured by flow-cytometric detection of ELF-97 Ⓡ fluorescence. Estuaries and Coasts , 32 (6): 1195-1204, https://doi.org/10.1007/s12237-009-9211-7.

Modi N, Bárcena-Uribarri I, Bains M et al. 2013. Role of the central arginine R133 toward the ion selectivity of the phosphate specific channel OprP: effects of charge and solvation. Biochemistry , 52 (33): 5522-5532, https://doi.org/10.1021/bi400522b.

Moegenburg S M, Vanni M J. 1991. Nutrient regeneration by zooplankton: effects on nutrient limitation of phytoplankton in a eutrophic lake. Journal of Plankton Research , 13 (3): 573-588, https://doi.org/10.1093/plankt/13.3.573.

Moisander P H, Daley M C, Shoemaker K M et al. 2022. Nitrogen fixation influenced by phosphorus and nitrogen availability in the benthic bloom-forming cyanobacterium Hydrocoleum sp. identified in a temperate Marine Lagoon. Journal of Phycology , 58 (3): 377-391, https://doi.org/10.1111/jpy.13244.

Monds R D, Newell P D, Schwartzman J A et al. 2006. Conservation of the Pho regulon in Pseudomonas fluorescens Pf0-1. Applied and Environmental Microbiology , 72 (3): 1910-1924, https://doi.org/10.1128/AEM.72.3.1910-1924.2006.

Moore L R, Ostrowski M, Scanlan D J et al. 2005. Ecotypic variation in phosphorus-acquisition mechanisms within marine picocyanobacteria. Aquatic Microbial Ecology , 39 (3): 257-269, https://doi.org/DOI10.3354/ame039257.

Nausch M. 1998. Alkaline phosphatase activities and the relationship to inorganic phosphate in the Pomeranian Bight (southern Baltic Sea). Aquatic Microbial Ecology , 16 (1): 87-94, https://doi.org/10.3354/ame016087.

Nedoma J, Van Wambeke F, Štrojsová et al. 2007. Affinity of extracellular phosphatases for ELF97 phosphate in aquatic environments. Marine and Freshwater Research , 58 (5): 454-460, https://doi.org/10.1071/Mf06211.

Newman S, McCormick P V, Backus J G. 2003. Phosphatase activity as an early warning indicator of wetland eutrophication: problems and prospects. Journal of Applied Phycology , 15 (1): 45-59, https://doi.org/10.1023/A:1022971204435.

Olsen Y, Vadstein O, Andersen T et al. 1989. Competition between Staurastrum Luetkemuellerii (Chlorophyceae) and Microcystis aeruginosa (Cyanophyceae) under varying modes of phosphate supply. Journal of Phycology , 25 (3): 499-508, https://doi.org/10.1111/j.1529-8817.1989. tb00255.x.

Olsson H. 1983. Origin and production of phosphatases in the acid Lake Gårdsjön. Hydrobiologia , 101 (1-2): 49-58, https://doi.org/10.1007/bf00008656.

Ou L J, Huang B Q, Lin L Z et al. 2006. Phosphorus stress of phytoplankton in the Taiwan Strait determined by bulk and single-cell alkaline phosphatase activity assays. Marine Ecology Progress Series , 327 : 95-106, https://doi.org/10.3354/meps327095.

Perry M J. 1972. Alkaline phosphatase activity in subtropical central North Pacific waters using a sensitive fluorometric method. Marine Biology , 15 (2): 113-119, https://doi.org/10.1007/BF00353639.

Pettersson K. 1985. The availability of phosphorus and the species composition of the spring phytoplankton in Lake Erken. Internationale Revue Der Gesamten Hydrobiologie und Hydrographie , 70 (4): 527-546, https://doi.org/10.1002/iroh.19850700407.

Pick F R. 1987. Interpretations of alkaline phosphatase activity in Lake Ontario. Canadian Journal of Fisheries and Aquatic Sciences , 44 (12): 2087-2094, https://doi.org/10.1139/f87-258.

Prentice M J, Hamilton D P, Willis A et al. 2019. Quantifying the role of organic phosphorus mineralisation on phytoplankton communities in a warm-monomictic lake. Inland Waters , 9 (1): 10-24, https://doi.org/10.1080/20442041.2018.1538717.

Rabouille S, Tournier L, Duhamel S et al. 2022. Organic phosphorus scavenging supports efficient growth of diazotrophic cyanobacteria under phosphate depletion. Frontiers in Microbiology , 13 : 848647, https://doi.org/10.3389/fmicb.2022.848647.

Rao N N, Torriani A. 1990. Molecular aspects of phosphate-transport in Escherichiacoli . MolecularMicrobiology , 4 (7): 1083-1090, https://doi.org/10.1111/j.1365-2958.1990.tb00682.x.

Raoui S M, Rachiq S, Chadli N et al. 2002. Seasonal variations of the alkaline phosphatase activity from the bacterial and algal planktonic communities in the mesotrophic reservoir lake Allal El Fassi, Morocco. Annales de Limnologie - International Journal of Limnology , 38 (4): 287-295.

Ray J M, Bhaya D, Block M A et al. 1991. Isolation, transcription, and inactivation of the gene for an atypical alkaline phosphatase of Synechococcus sp. strain PCC 7942. Journal of Bacteriology , 173 (14): 4297-4309, https://doi.org/10.1128/jb.173.14.4297-4309.1991.

Rejmánková E, Komárková J. 2000. A function of cyanobacterial mats in phosphorus-limited tropical wetlands. Hydrobiologia , 431 (2-3): 135-153, https://doi.org/10.1023/A:1004011318643.

Rejmánková E, Komárková J. 2005. Response of cyanobacterial mats to nutrient and salinity changes. Aquatic Botany , 83 (2): 87-107, https://doi.org/10.1016/j.aquabot.2005.05.011.

Rengefors K, Pettersson K, Blenckner T et al. 2001. Species-specific alkaline phosphatase activity in freshwater spring phytoplankton: application of a novel method. Journal of Plankton Research , 23 (4): 435-443, https://doi.org/10.1093/plankt/23.4.435.

Rengefors K, Ruttenberg K C, Haupert C L et al. 2003. Experimental investigation of taxon-specific response of alkaline phosphatase activity in natural freshwater phytoplankton. Limnology and Oceanography , 48 (3): 1167-1175, https://doi.org/10.4319/lo.2003.48.3.1167.

Rose C, Axler R P. 1997. Uses of alkaline phosphatase activity in evaluating phytoplankton community phosphorus deficiency. Hydrobiologia , 361 (1-3): 145-156, https://doi.org/10.1023/A:1003178502883.

Ruiz R G, Hernández I, Lucena J et al. 1997. Preliminary studies on the significance of alkaline phosphatase activity in the diatom Phaeodactylum tricornutum Bohlin. Scientia Marina , 61 (4): 517-525.

Rychtecký P, Řeháková K, Kozlíková E et al. 2015. Light availability may control extracellular phosphatase production in turbid environments. Microbial Ecology , 69 (1): 37-44, https://doi.org/10.1007/s00248-014-0483-5.

Schindler D W. 1977. Evolution of phosphorus limitation in lakes. Science , 195 (4275): 260-262, https://doi.org/10.1126/science.195.4275.260.

Sebastian M, Ammerman J W. 2009. The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. The ISME Journal , 3 (5): 563-572, https://doi.org/10.1038/ismej.2009.10.

Sebastián M, Arístegui J, Montero M F et al. 2004. Alkaline phosphatase activity and its relationship to inorganic phosphorus in the transition zone of the North-western African upwelling system. Progress in Oceanography , 62 (2-4): 131-150, https://doi.org/10.1016/j.pocean.2004.07.007.

Sharma U, Pal D, Prasad R. 2014. Alkaline phosphatase: an overview. Indian Journal of Clinical Biochemistry , 29 (3): 269-278, https://doi.org/10.1007/s12291-013-0408-y.

Singh P K, Shrivastava A K, Chatterjee A et al. 2015. Cadmium toxicity in diazotrophic Anabaena spp. adjudged by hasty up-accumulation of transporter and signaling and severe down-accumulation of nitrogen metabolism proteins. Journal of Proteomics , 127 : 134-146, https://doi.org/10.1016/j.jprot.2015.05.019.

Singh S K, Singh S S, Pandey V D et al. 2006. Factors modulating alkaline phosphatase activity in the diazotrophic rice-field cyanobacterium, Anabaena oryzae . World Journal of Microbiology and Biotechnology , 22 (9): 927-935, https://doi.org/10.1007/s11274-006-9137-1.

Sirová D, Rejmánková E, Carlson E et al. 2013. Current standard assays using artificial substrates overestimate phosphodiesterase activity. Soil Biology and Biochemistry , 56 : 75-79, https://doi.org/10.1016/j.soilbio.2012.02.008.

Sirová D, Vrba J, Rejmánková E. 2006. Extracellular enzyme activities in benthic cyanobacterial mats: comparison between nutrient-enriched and control sites in marshes of northern Belize. Aquatic Microbial Ecology , 44 (1): 11-20, https://doi.org/10.3354/ame044011.

Siuda W. 1984. Phosphatases and their role in organic phosphorus transformation in natural waters: a review. Polskie Archiwum Hydrobiologii , 31 (3): 207-233.

Smith R E H, Kalff J. 1981. The Effect of phosphorus limitation on algal growth rates: evidence from alkaline phosphatase. Canadian Journal of Fisheries and Aquatic Sciences , 38 (11): 1421-1427, https://doi.org/10.1139/f81-188.

Srivastava A, Saavedra D E M, Thomson B et al. 2021. Enzyme promiscuity in natural environments: alkaline phosphatase in the ocean. The ISME Journal , 15 (11): 3375-3383, https://doi.org/10.1038/s41396-021-01013-w.

Steffen M M, Dearth S P, Dill B D et al. 2014. Erratum: nutrients drive transcriptional changes that maintain metabolic homeostasis but alter genome architecture in Microcystis . The ISEM Journal , 8 (10): 2152, https://doi.org/10.1038/ismej.2014.133.

Steiner M. 1938. Zur kenntnis des phosphatkreislaufes in seen. Naturwissenschaften , 26 (44): 723-724.

Stevens R J, Parr M P. 1977. The significance of alkaline phosphatase activity in Lough Neagh. Freshwater Biology , 7 (4): 351-355, https://doi.org/10.1111/j.1365-2427.1977.tb01683.x.

Stihl A, Sommer U, Post A F. 2001. Alkaline phosphatase activities among populations of the colony-forming diazotrophic cyanobacterium Trichodesmium spp. (cyanobacteria) in the Red Sea. Journal of Phycology , 37 (2): 310-317, https://doi.org/10.1046/j.1529-8817.2001.037002310.x.

Stoecker D, Autio R, Rintala J M et al. 2005. Ecto-cellular enzyme activity associated with filamentous cyanobacteria. Aquatic Microbial Ecology , 40 (2): 151-161, https://doi.org/10.3354/ame040151.

Štrojsová, Vrba J, Nedoma J et al. 2005. Extracellular phosphatase activity of freshwater phytoplankton exposed to different in situ phosphorus concentrations. Marine and Freshwater Research , 56 (4): 417-424, https://doi.org/10.1071/MF04283.

Štrojsová, Vrba J, Nedoma N et al. 2003. Seasonal study of extracellular phosphatase expression in the phytoplankton of a eutrophic reservoir. European Journal of Phycology , 38 (4): 295-306, https://doi.org/10.1080/09670260310001612628.

Su Z C, Dam P, Chen X et al. 2003. Computational inference of regulatory pathways in microbes: an application to phosphorus assimilation pathways in Synechococcus sp. WH8102. Genome Informatics , 14 : 3-13, https://doi.org/10.11234/gi1990.14.3.

Su Z C, Olman V, Xu Y. 2007. Computational prediction of Pho regulons in cyanobacteria. BMC Genomics , 8 : 156, https://doi.org/10.1186/1471-2164-8-156.

Subramanian G, Sekar S, Sampoornam S. 1994. Biodegradation and utilization of organophosphorus pesticides by cyanobacteria. International Biodeterioration & Biodegradation , 33 (2): 129-143, https://doi.org/10.1016/0964-8305(94)90032-9.

Tetu S G, Brahamsha B, Johnson D A et al. 2009. Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp. WH8102. The ISME Journal , 3 (7): 835-849, https://doi.org/10.1038/ismej.2009.31.

Thingstad T F, Zweifel U L, Rassoulzadegan F. 1998. P limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean. Limnology and Oceanography , 43 (1): 88-94, https://doi.org/10.4319/lo.1998.43.1.0088.

Tiwari B, Singh S, Kaushik M S et al. 2015. Regulation of organophosphate metabolism in cyanobacteria. A review. Microbiology , 84 (3): 291-302, https://doi.org/10.1134/S0026261715030200.

Vaitomaa J, Repka S, Saari L et al. 2002. Aminopeptidase and phosphatase activities in basins of Lake Hiidenvesi dominated by cyanobacteria and in laboratory grown Anabaena . Freshwater Biology , 47 (9): 1582-1593, https://doi.org/10.1046/j.1365-2427.2002.00901.x.

Vershinina O A, Znamenskaya L V. 2002. The Pho regulons of bacteria. Microbiology , 71 (5): 497-511, https://doi.org/10.1023/A:1020547616096.

Vrba J, Komárkova J, Vyhnálek V. 1993. Enhanced activity of alkaline phosphatases - Phytoplankton response to epilimnetic phosphorus depletion. Water Science and Technology , 28 (6): 15-24, https://doi.org/10.2166/wst.1993.0124.

Wagner K U, Masepohl B, Pistorius E K. 1995. The cyanobacterium Synechococcus sp. strain PCC 7942 contains a second alkaline phosphatase encoded by phoV . Microbiology , 141 (12): 3049-3058, https://doi.org/10.1099/13500872-141-12-3049.

Wan L L, Chen X Y, Deng Q H et al. 2019. Phosphorus strategy in bloom-forming cyanobacteria ( Dolichospermum and Microcystis ) and its role in their succession. Harmful Algae , 84 : 46-55, https://doi.org/10.1016/j.hal.2019.02.007.

Wang C Y, Yang Y Y, Yang B et al. 2021. Causal relationship between alkaline phosphatase activities and phosphorus dynamics in a eutrophic coastal lagoon in Lake Michigan. Science of the Total Environment , 787 : 147681, https://doi.org/10.1016/j.scitotenv.2021.147681.

Wei S J, Zhuang G J, Cheng L R J et al. 2022. The proliferation rule of Microcystis aeruginosa under different initial pH conditions and its influence on the pH value of the environment. Environmental Science and Pollution Research , 29 (10): 13835-13844, https://doi.org/10.1007/s11356-021-16719-9.

White S H, Fabbro L D, Duivenvoorden L J. 2003. Changes in cyanoprokaryote populations, Microcystis morphology, and microcystin concentrations in Lake Elphinstone (Central Queensland, Australia). Environmental Toxicology , 18 (6): 403-412, https://doi.org/10.1002/tox.10142.

Whitton B A, Grainger S L J, Hawley G R W et al. 1991. Cell-bound and extracellular phosphatase activities of cyanobacterial isolates. Microbial Ecology , 21 : 85-98, https://doi.org/10.1007/BF02539146.

Whitton B A, Potts M, Simon J W et al. 1990. Phosphatase activity of the blue-green alga (cyanobacterium) Nostoc commune UTEX 584. Phycologia , 29 (2): 139-145, https://doi.org/10.2216/i0031-8884-29-2-139.1.

Wilkins A S. 1972. Physiological factors in the regulation of alkaline phosphatase synthesis in Escherichia coli . Journal of Bacteriology , 110 (2): 616-623, https://doi.org/10.1128/JB.110.2.616-623.1972.

Willis A, Chuang A W, Dyhrman S et al. 2019. Differential expression of phosphorus acquisition genes in response to phosphorus stress in two Raphidiopsis raciborskii strains. Harmful Algae , 82 : 19-25, https://doi.org/10.1016/j.hal.2018.12.003.

Yadav S, Prajapati R, Atri N. 2016. Effects of UV-B and heavy metals on nitrogen and phosphorus metabolism in three cyanobacteria. Journal of Basic Microbiology , 56 (1): 2-13, https://doi.org/10.1002/jobm.201500504.

Yamaguchi H, Yamaguchi M, Fukami K et al. 2005. Utilization of phosphate diester by the marine diatom Chaetoceros ceratosporus . Journal of Plankton Research , 27 (6): 603-606, https://doi.org/10.1093/plankt/fbi027.

Yates C A, Johnes P J, Owen A T et al. 2019. Variation in dissolved organic matter (DOM) stoichiometry in U.K. freshwaters: assessing the influence of land cover and soil C: N ratio on DOM composition. Limnology and Oceanography , 64 (6): 2328-2340, https://doi.org/10.1002/lno.11186.

Yelloly J M, Whitton B A. 1996. Seasonal changes in ambient phosphate and phosphatase activities of the cyanobacterium Rivularia atra in intertidal pools at Tyne Sands, Scotland. Hydrobiologia , 325 (3): 201-212, https://doi.org/10.1007/Bf00014985.

Yong S C, Roversi P, Lillington J et al. 2014. A complex iron-calcium cofactor catalyzing phosphotransfer chemistry. Science , 345 (6201): 1170-1173, https://doi.org/10.1126/science.1254237.

Young C L, Ingall E D. 2010. Marine dissolved organic phosphorus composition: insights from samples recovered using combined electrodialysis/reverse osmosis. Aquatic Geochemistry , 16 (4): 563-574, https://doi.org/10.1007/s10498-009-9087-y.

Yuan Y J, Bi Y H, Hu Z Y. 2016. Dynamics of alkaline phosphatase activity during the period of cyanobacterial bloom in a tributary of the Three Gorges Reservoir. Fresenius Environmental Bulletin , 25 (11): 4900-4907.

Zaheer R, Morton R, Proudfoot M et al. 2009. Genetic and biochemical properties of an alkaline phosphatase PhoX family protein found in many bacteria. Environmental Microbiology , 11 (6): 1572-1587, https://doi.org/10.1111/j.1462-2920.2009.01885.x.

Zhang T X, Lu X R, Yu R D et al. 2020a. Response of extracellular and intracellular alkaline phosphatase in Microcystis aeruginosa to organic phosphorus. Environmental Science and Pollution Research , 27 (34): 42304-42312, https://doi.org/10.1007/s11356-020-09736-7.

Zhang X H, Lin S J, Liu D Y. 2020b. Transcriptomic and physiological responses of Skeletonema costatum to ATP utilization. Environmental Microbiology , 22 (5): 1861-1869, https://doi.org/10.1111/1462-2920.14944.

Zhang X L, Deng J J, Xue Y M et al. 2016. Stimulus response of Au-NPs@GMP-Tb core-shell nanoparticles: toward colorimetric and fluorescent dual-mode sensing of alkaline phosphatase activity in algal blooms of a freshwater lake. Environmental Science & Technology , 50 (2): 847-855, https://doi.org/10.1021/acs.est.5b04600.

Zhang X Y, Wang Z H, Luo Z X et al. 2022. Insights into the conversion of dissolved organic phosphorus favors algal bloom, arsenate biotransformation and microcystins release of Microcystis aeruginosa . Journal of Environmental Sciences , 125 : 205-214, https://doi.org/10.1016/j.jes.2021.11.025.

Zhang X, Zhang J P, Yuan H M et al. 2021. Seasonal dynamics of phytoplankton phosphorus stress in temperate Jiaozhou Bay, North China. Continental Shelf Research , 231 : 104602, https://doi.org/10.1016/j.csr.2021.104602.

Zhao G Y, Du J J, Jia Y et al. 2012. The importance of bacteria in promoting algal growth in eutrophic lakes with limited available phosphorus. Ecological Engineering , 42 : 107-111, https://doi.org/10.1016/j.ecoleng.2012.02.007.

Zhou J, Han X X, Qin B Q et al. 2021. Responses of alkaline phosphatase activity to wind-driven waves in a large, shallow lake: implications for phosphorus availability and algal blooms. Journal of Environmental Sciences , 99 : 143-150, https://doi.org/10.1016/j.jes.2020.06.022.

Zhou Y Y, Zhou X Y. 1997. Seasonal variation in kinetic parameters of alkaline phosphatase activity in a shallow Chinese freshwater lake (Donghu Lake). Water Research , 31 (5): 1232-1235, https://doi.org/10.1016/S0043-1354(96)00366-1.

Views

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

Physiological and molecular responses of invasive cyanobacteriumRaphidiopsis raciborskiito ambient phosphorus deficiency

Influences of aeration induced turbulence on growth and competition of Microcystis and Scenedesmus in the presence of sediments with varying particle sizes

Observation and simulation of 2-methylisoborneol in the Qingcaosha Reservoir, Changjiang estuary

Polyphasic examination on Merismopedia tenuissima CHAB 7021 from Ganjiang River, China revealed the polyphyly of the genus Merismopedia (Cyanobacteria)

Molecular detection of microbial communities associated with Microcystis vs Synechococcus dominated waters in Tianjin, China

Related Author

Junqiong SHI

Shuhan HE

Lu ZHAO

Lulu JI

Songqi YANG

Zhongxing WU

Qiang HE

Yiyao WANG

Related Institution

Key Laboratory of Eco-environments in Three Gorges Reservoir Region (Ministry of Education), Chongqing Key Laboratory of Plant Ecology and Resources Research in Three Gorges Reservoir Region, School of Life Sciences, Southwest University

College of Natural Resources and Environment, Northwest A&F University, Yangling

Chengdu Environmental Protection Research Institute

State Key Laboratory of Estuarine and Coastal Research, East China Normal University

Shanghai Academy of Environmental Sciences

Address：Editorial Office of JOL, 88 Haijun Rd. Qingdao, 266000, China
Tel：+86-532-82898754 Email：jol@qdio.ac.cn
Technical support is provided by Beijing Founder electronics co., LTD 京ICP备09064830号-19 京公网安备11010802024621
It is recommended to read the content of this site in Chrome&IE9+. Please switch to extreme mode in browser 360.
Cookies We use cookies to help provide and enhance our service and tailor content. By continuing, you agree to the use of cookies.

⁰