Skip to main content
SpringerLink
Log in

Response of extracellular and intracellular alkaline phosphatase in Microcystis aeruginosa to organic phosphorus

  • Cyanobacterial blooms and water ecological restoration
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Cyanobacterial blooms caused by Microcystis have become a menace to public health and water quality in the global freshwater ecosystem. Alkaline phosphatases (APases) produced by microorganisms play an important role in the mineralization of dissolved organic phosphorus (DOP) into orthophosphate (Pi) to promote cyanobacterial blooms. However, the response of extracellular and intracellular alkaline phosphatase activity (APA) of Microcystis to different DOP sources is poorly understood. In this study, we compared the growth of M. aeruginosa on two DOP substrates (β-glycerol-phosphate (β-GP) and lecithin (LEC)) and monitored the changes of P fractions and the extra- and intracellular APA under different P sources and concentrations. M. aeruginosa can utilize both β-GP and LEC to sustain its growth, and the bioavailability of LEC was greater than β-GP. For the β-GP treatment, there was no significant difference in the algal growth at different concentrations (P > 0.05), while the algal growth in the LEC treatment groups was significantly affected by concentrations (P < 0.05). The results showed that intracellular APA of M. aeruginosa could be detected in all DOP treatment groups and generally higher than extracellular APA. In addition, the intracellular APA per cell increased first and then decreased in all DOP treatment groups. Compared with the β-GP treatment, M. aeruginosa in the LEC groups could secret more extracellular APA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Antelmann H, Scharf C, Hecker M (2000) Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J. Bacteriol. 182:4478–4490

    Article  CAS  Google Scholar 

  • Apel AK, Sola-Landa A, Rodriguez-Garcia A, Martin JF (2007) Phosphate control of phoA, phoC and phoD gene expression in Streptomyces coelicolor reveals significant differences in binding of PhoP to their promoter regions. Microbiology-Sgm 153:3527–3537

    Article  CAS  Google Scholar 

  • Cao XY, Strojsova A, Znachor P, Zapomelova E, Liu GX, Vrba J, Zhou YY (2005) Detection of extracellular phosphatases in natural spring phytoplankton of a shallow eutrophic lake (Donghu, China). European Journal of Phycology 40:251–258

    Article  CAS  Google Scholar 

  • Carpenter SR (2008) Phosphorus control is critical to mitigating eutrophication. Proceedings of the National Academy of Sciences of the United States of America 105:11039–11040

    Article  CAS  Google Scholar 

  • Dai JY, Gao G, Wu SQ, Wu XF, Zhou J, Xue WY, Yang QQ, Chen D (2016) Bacterial alkaline phosphatases and affiliated encoding genes in natural waters: a review. J. Lake. Sci. 28(6):1153–1166

    Article  Google Scholar 

  • Feng S, Qin BQ, Gao G (2008): The relationships between phosphorus-transmuting bacteria and phosphorus forms in Lake Taihu. Lake Sci. 20(4), 428-436(Chinese)

  • Fernando SB (2015) The Pho regulon: a huge regulatory network in bacteria. Front. Microbiol. 6:402

    Google Scholar 

  • Geider RJ, La Roche J (2002) Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. European Journal of Phycology 37:1–17

    Article  Google Scholar 

  • Hadas O, Pinkas R (1997) Arylsulfatase and alkaline phosphatase (Apase) activity in sediments of Lake Kinneret, Israel. Water Air & Soil Pollution 99(1-4):671–679

    Article  CAS  Google Scholar 

  • Halemejko GZ, Chrost RJ (1984) The role of phosphatases in phosphorus mineralization during decomposition of lake phytoplankton blooms. Archiv fur Hydrobiologie 101(4):489–502

    CAS  Google Scholar 

  • Harke MJ, Berry DL, Ammerman JW, Gobler CJ (2012) Molecular response of the bloom-forming cyanobacterium, Microcystis aeruginosa, to phosphorus limitation. Microbial Ecology 63:188–198

    Article  CAS  Google Scholar 

  • Ho JC, Michalak AM, Pahlevan N (2019) Widespread global increase in intense lake phytoplankton blooms since the 1980s. Nature 574:667–670

    Article  CAS  Google Scholar 

  • Huang BQ, Ou LJ, Hong HS (2005) Bioavailability of dissolved organic phosphorus compounds to typical harmful dinoflagellate prorocentrum donghaiense Lu. Mar. Pollut. Bull. 51:38–844

    Article  Google Scholar 

  • Jin XC, Tu QY (1990) The standard methods for observation and analysis of lake eutrophication, Second edn. China Environmental Science Press, China

  • Labry C, Delmas D, Herbland A (2005) Phytoplankton and bacterial alkaline phosphatase activities in relation to phosphate and DOP availability within the Gironde plume waters (Bay of Biscay). Journal of Experimental Marine Biology and Ecology 318:213–225

    Article  CAS  Google Scholar 

  • Li B, Brett MT (2013) The influence of dissolved phosphorus molecular form on recalcitrance and bioavailability. Environmental Pollution 182:37–44

    Article  CAS  Google Scholar 

  • Li JH, Wang ZW, Cao X, Wang ZF, Zheng Z (2015) Effect of orthophosphate and bioavailability of dissolved organic phosphorous compounds to typically harmful cyanobacterium Microcystis aeruginosa. Mar. Pollut. Bull. 92:52–58

    Article  CAS  Google Scholar 

  • Luo HW, Benner R, Long RA, Hu JJ (2009) Subcellular localization of marine bacterial alkaline phosphatases. Proceedings of the National Academy of Sciences of the United States of America 106:21219–21223

    Article  CAS  Google Scholar 

  • Markou G, Vandamme D, Muylaert K (2014) Microalgal and cyanobacterial cultivation: the supply of nutrients. Water Research 65:186–202

    Article  CAS  Google Scholar 

  • Martinez J, Smith DC, Steward GF, Azam F (1996) Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea. Aquatic Microbial Ecology 10(3):223–230

    Article  Google Scholar 

  • McMahon KD, Read EK (2013): Microbial contributions to phosphorus cycling in eutrophic lakes and wastewater. In: Gottesman S (Editor), Annual Review of Microbiology, Vol 67. Annual Review of Microbiology. Annual Reviews, Palo Alto, 199-219

  • Paerl HW, Xu H, McCarthy MJ, Zhu GW, Qin BQ, Li YP, Gardner WS (2011) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Research 45:1973–1983

    Article  CAS  Google Scholar 

  • Pang Y, Nie SH, Chu ZS (2016) Effects of different kinds of phosphorus sources on growth and alkaline phosphatase activity (APA) of Karenia mikimotoi Hansen. Marine Sciences 17

  • Read EK, Ivancic M, Hanson P, Cade-Menun BJ, McMahon KD (2014): Phosphorus speciation in a eutrophic lake by 31PNMR spectroscopy. Water Research 62(oct.1), 229-240

  • Reichardt W, Overbeck J, Steubing L (1967) Free dissolved enzymes in lake waters. Nature 216(5122):1345–1347

    Article  CAS  Google Scholar 

  • Ren LX, Wang PF, Wang C, Chen J, Hou J, Qian J (2017) Algal growth and utilization of phosphorus studied by combined mono-culture and co-culture experiments. Environ. Pollut. 220:274–285

    Article  CAS  Google Scholar 

  • Sato M, Amano Y, Machida M, Imazeki F (2017) Colony formation of highly dispersed Microcystis aeruginosa by controlling extracellular polysaccharides and calcium ion concentrations in aquatic solution. Limnology 18:111–119

    Article  CAS  Google Scholar 

  • Schindler DW, Carpenter SR, Chapra SC, Hecky RE, Orihel DM (2016) Reducing Phosphorus to Curb Lake Eutrophication is a Success. Environ. Sci. Technol. 50:8923–8929

    Article  CAS  Google Scholar 

  • Sondergaard M, Jensen JP, Jeppesen E (2003) Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506:135–145

    Article  Google Scholar 

  • Suzuki S, Ferjani A, Suzuki I, Murata N (2004) The SphS-SphR two component system is the exclusive sensor for the induction of gene expression in response to phosphate limitation in Synechocystis. J. Biol. Chem. 279:13234–13240

    Article  CAS  Google Scholar 

  • Tiwari B, Singh S, Kaushik MS, Mishra AK (2015) Regulation of organophosphate metabolism in cyanobacteria. A review. Microbiology 84(3):291–302

    CAS  Google Scholar 

  • Van Moorleghem C, Schutter ND, Smolders E, Merckx R (2013) The bioavailability of colloidal and dissolved organic phosphorus to the alga Pseudokirchneriella subcapitata in relation to analytical phosphorus measurements. Hydrobiologia 709:41–53

    Article  CAS  Google Scholar 

  • Vershinina OA, Znamenskaya LV (2002) The Pho regulons of bacteria. Microbiology 71:497–511

    Article  CAS  Google Scholar 

  • Wang S, Zhang XL, Cui LB, Shang K, Qu LY (2015) Diversity and characteristics of culturable phosphate-solubilizing bacteria of Indian Ocean. Microbiology China 042(010):1847–1857

    CAS  Google Scholar 

  • Watanabe M, Kohata K, Kunugi M (1987) 31P nuclear magnetic resonances study of intracellular phosphate pools and polyphosphate metabolism in Heterosigam akashiwo (hada) HADA (Raphidophyceae). J. Phycol. 23:54–62

    Article  CAS  Google Scholar 

  • Weiss MS, Abele U, Weckesser J, Welte W, Schiltz E, Schulz GE (1991) Molecular architecture and electrostatic properties of a bacterial porin. Science 254:1627–1630

    Article  CAS  Google Scholar 

  • Wetzel RG (1999) Organic phosphorus mineralization in soils and sediments. Phosphorus biogeochemistry in subtropical ecosystems:225–245

  • White AE (2009) New insights into bacterial acquisition of phosphorus in the surface ocean. Proceedings of the National Academy of Sciences of the United States of America 106:21013–21014

    Article  CAS  Google Scholar 

  • Yang CB (2014) Research on organophosphate-dissolving bacteria from the rhizosphere soil of Chinese pine. Inner Mongolia Agricultural University

  • Yang Z, Kong FX (2013) Abiotic factors in colony formation: effects of nutrition and light on extracellular polysaccharide production and cell aggregates of Microcystis aeruginosa. Chinese Journal of Oceanology and Limnology 31:796–802

    Article  CAS  Google Scholar 

  • Yi W, Jin X, Chu Z, Hu X, Ma Z, Wang G, Zhang S (2004): Effect of different P mass concentrations on growth and P-in-cell of Microcystis aeruginosa. Research of Environmental Sciences 17(suppl.), 58-61

  • Zhang P, Feng J, Li Z (2015) Alkaline phosphatase activity and its kinetics in Lake Gaoyang, Pengxi River during high water level. J. Lake Sci. 27(4):629–636

    Article  CAS  Google Scholar 

  • Zhang SF, Yuan CJ, Chen Y, Lin L (2019) Wang DZ (2019): Transcriptomic response to changing ambient phosphorus in the marine dinoflagellate Prorocentrum donghaiense. Science of the total environment 692:1037–1047

    Article  CAS  Google Scholar 

  • Zhao DD (2015) Cyanobacter is phosphatase gene diversity and its response to phosphorus. South China University of Technology (Chinese)

  • Zhou XS, Ma SL, Shang ZM (2016): Determination of cell density of Microcystis aeruginosa by spectrophotometry. Technology Supervision in Water Resource 24(5), 50-51(Chinese)

  • Zhu W, Sun QQ, Chen FL, Li M (2015) Cellular N:P ratio of Microcystis as an indicator of nutrient limitation-implications and applications. Environmental Earth Sciences 74:4023–4030

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We greatly thank Prof. Li J.H. from Nanjing Normal University for guidance on experimental protocols and methods, as well as students Liu L.W. and Zu Y. for help with algae inoculation. We greatly thank Dr. Malott T.M. from Mascoma LLC for the paper revise.

Funding

This work was funded by National Natural Science Foundation of China (Nos. 41303058, 31971561).

Author information

Author notes

  1. Rongda Yu and Mengyao Qin contributed equally to this work.

Authors and Affiliations

  1. School of Environment, Nanjing Normal University, Nanjing, 210023, China

    Tingxi Zhang, Xiaoran Lu, Rongda Yu, Mengyao Qin & Chao Wei

  2. Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, Nanjing, 210023, China

    Tingxi Zhang

  3. Jiangsu Provincial Key Laboratory of Materials Cycling and Pollution Control, Nanjing, 210023, China

    Tingxi Zhang

  4. School of Life Sciences, Nanjing Normal University, Nanjing, 210046, China

    Sujuan Hong

Authors
  1. Tingxi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoran Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rongda Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mengyao Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chao Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sujuan Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tingxi Zhang.

Ethics declarations

Competing interests

The authors declare that there are no competing interests.

Additional information

Responsible Editor: Vitor Manuel Oliveira Vasconcelos

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, T., Lu, X., Yu, R. et al. Response of extracellular and intracellular alkaline phosphatase in Microcystis aeruginosa to organic phosphorus. Environ Sci Pollut Res 27, 42304–42312 (2020). https://doi.org/10.1007/s11356-020-09736-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-09736-7

Keywords

Search

Navigation