Skip to main content
Log in

Two types of bound extracellular polysaccharides and their roles in shaping the size and tightness of Microcystis colonies

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Extracellular polysaccharide (EPS) can be distinguished into soluble or bound types and significantly contributes to colony formation in Microcystis. Depending on the binding strength with cells, the bilayer structure of bound EPS contains loosely or tightly bound EPS (LB-EPS or TB-EPS) and their roles in shaping the size and tightness of Microcystis colonies deserve further investigation. In this study, the influences of two types of bound EPS on the size and tightness of Microcystis colonies were investigated after a series of pretreatment to obtain LB-EPS retaining or stripped samples. Results showed that cells with LB-EPS formed large and loose colonies. Furthermore, the ratios of LB-EPS to TB-EPS, which indicate the size and tightness of the colonies, were higher in the retaining groups than in the stripped groups. Our findings also provide evidence that calcium enrichment is conducive to colony formation in Microcystis. This study provides new insights into the formation and enlargement of Microcystis colonies, which contributes to a better understanding on the role of EPS in Microcystis aggregation and morphology changes.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aktas TS, Takeda F, Maruo C, Chiba N, Nishimura O (2012) A comparison of zeta potentials and coagulation behaviors of cyanobacteria and algae. Desalin Water Treat 48:294–301

    Article  CAS  Google Scholar 

  • Bi X, Zhang S, Dai W, Xing K, Yang F (2013) Effects of lead (II) on the extracellular polysaccharide (EPS) production and colony formation of cultured Microcystis aeruginosa. Water Sci Technol 67:803–809

    Article  CAS  Google Scholar 

  • Duan Z, Tan X, Parajuli K, Upadhyay S, Zhang D, Shu X, Liu Q (2018) Colony formation in two Microcystis morphotypes: effects of temperature and nutrient availability. Harmful Algae 72:14–24

    Article  CAS  Google Scholar 

  • Gan N, Xiao Y, Zhu L, Wu Z, Liu J, Hu C, Song L (2012) The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environ Microbiol 14:730–742

    Article  CAS  Google Scholar 

  • Hadjoudja S, Deluchat V, Baudu M (2010) Cell surface characterisation of Microcystis aeruginosa, and Chlorella vulgaris. J Colloid Interface Sci 342:293–299

    Article  CAS  Google Scholar 

  • Harke MJ, Steffen MM, Gobler CJ, Otten TG, Wilhelm SW, Wood SA, Paerl HW (2016) A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54:4–20

    Article  Google Scholar 

  • Kessel M, Eloff JN (1975) The ultrastructure and development of the colonial sheath of Microcystis marginata. Arch Microbiol 106:209–214

    Article  CAS  Google Scholar 

  • Li X, Yang S (2007) Influence of loosely bound extracellular polymeric substances (EPS) on the flocculation, sedimentation and dewaterability of activated sludge. Water Res 41:1022–1030

    Article  CAS  Google Scholar 

  • Li H, Wen Y, Cao A, Huang J, Zhou Q, Somasundaran P (2012) The influence of additives (Ca2+, Al3+, and Fe3+) on the interaction energy and loosely bound extracellular polymeric substances (EPS) of activated sludge and their flocculation mechanisms. Bioresour Technol 114:188–194

    Article  CAS  Google Scholar 

  • Li L, Zhu W, Wang T, Luo Y, Chen F, Tan X (2013a) Effect of fluid motion on colony formation in Microcystis aeruginosa. Water Sci Eng 6:106–116

    Google Scholar 

  • Li M, Zhu W, Gao L, Lu L (2013b) Changes in extracellular polysaccharide content and morphology of Microcystis aeruginosa at different specific growth rates. J Appl Phycol 25:1023–1030

    Article  CAS  Google Scholar 

  • Li M, Zhu W, Gao L (2014) Analysis of cell concentration, volume concentration, and colony size of Microcystis via laser particle analyzer. Environ Manag 53:947–958

    Article  Google Scholar 

  • Li M, Zhu W, Guo L, Hu J, Chen H, Xiao M (2016) To increase size or decrease density? Different Microcystis species has different choice to form blooms. Sci Rep 6:37056

    Article  CAS  Google Scholar 

  • Liu H, Fang H (2002) Characterization of electrostatic binding sites of extracellular polymers by linear programming analysis of titration data. Biotechnol Bioeng 80:806–811

    Article  CAS  Google Scholar 

  • Lürling M, Eshetu F, Faassen E, Kosten S, Huszar V (2013) Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshw Biol 58:552–559

    Article  Google Scholar 

  • Paerl H, Xu H, McCarthy M, Zhu G, Qin B, Li Y, Gardner W (2011) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Res 45:1973–1983

    Article  CAS  Google Scholar 

  • Qin B, Yang G, Ma J, Deng J, Li W, Wu T, Zhang Y (2016) Dynamics of variability and mechanism of harmful cyanobacteria bloom in Lake Taihu, China. Chin Sci Bull 61:759–770

    Article  Google Scholar 

  • Qu F, Liang H, Wang Z, Wang H, Yu H, Li G (2012) Ultrafiltration membrane fouling by extracellular organic matters (EOM) of Microcystis aeruginosa in stationary phase: influences of interfacial characteristics of foulants and fouling mechanisms. Water Res 46:1490–1500

    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 

  • 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. Freshw Biol 56:1065–1080

    Article  CAS  Google Scholar 

  • Sheng G, Yu H, Li X (2010) Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnol Adv 28:882–894

    Article  CAS  Google Scholar 

  • Stanier R, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171–205

    Article  CAS  Google Scholar 

  • Tang J, Wu Y, Esquivel-Elizondo S, Sørensen JS, Rittmann EB (2018) How microbial aggregates protect against nanoparticle toxicity. Trends Biotechnol 36:1171–1182

    Article  CAS  Google Scholar 

  • Visser PM, Passarge J, Mur LR (1997) Modelling vertical migration of the cyanobacterium Microcystis. Hydrobiologia 349:99–109

    Article  Google Scholar 

  • Vogelaar JCT, De Keizer A, Spijker S, Lettinga G (2005) Bioflocculation of mesophilic and thermophilic activated sludge. Water Res 39:37–46

    Article  CAS  Google Scholar 

  • Wang Y, Zhao J, Li J, Li S, Zhang L, Wu M (2011) Effects of calcium levels on colonial aggregation and buoyancy of Microcystis aeruginosa. Curr Microbiol 62:679–683

    Article  CAS  Google Scholar 

  • Wu Z, Song L (2008) Physiological comparison between colonial and unicellular forms of Microcystis aeruginosa Kütz (Cyanobacteria). Phycologia 47:98–104

    Article  CAS  Google Scholar 

  • Xiao M, Willis A, Burford MA, Li M (2017) A meta-analysis comparing cell-division and cell-adhesion in Microcystis colony formation. Harmful Algae 67:85–91

    Article  CAS  Google Scholar 

  • Xu H, He P, Wang G, Shao L (2010) Three-dimensional excitation emission matrix fluorescence spectroscopy and gel-permeating chromatography to characterize extracellular polymeric substances in aerobic granulation. Water Sci Technol 61:2931–2942

    Article  CAS  Google Scholar 

  • Xu H, Cai H, Yu G, Jiang H (2013) Insights into extracellular polymeric substances of cyanobacterium Microcystis aeruginosa using fractionation procedure and parallel factor analysis. Water Res 47:2005–2014

    Article  CAS  Google Scholar 

  • Xu H, Jiang H, Yu G, Yang L (2014) Towards understanding the role of extracellular polymeric substances in cyanobacterial Microcystis, aggregation and mucilaginous bloom formation. Chemosphere 117:815–822

    Article  CAS  Google Scholar 

  • Xu F, Zhu W, Xiao M, Li M (2016) Interspecific variation in extracellular polysaccharide content and colony formation of Microcystis spp. cultured under different light intensities and temperatures. J Appl Phycol 28:1533–1541

    Article  CAS  Google Scholar 

  • Yamamoto Y, Nakahara H (2009) Seasonal variations in the morphology of bloom-forming cyanobacteria in a eutrophic pond. Limnology 10:185–193

    Article  Google Scholar 

  • Yamamoto Y, Shiah F, Chen Y (2011) Importance of large colony formation in bloom-forming cyanobacteria to dominate in eutrophic ponds. Ann Limnol Int J Lim 47:167–173

    Article  Google Scholar 

  • Yang Z, Kong F (2012) Formation of large colonies: a defense mechanism of Microcystis aeruginosa under continuous grazing pressure by flagellate Ochromonas sp. J Limnol 71:e5

    Article  Google Scholar 

  • Yang Z, Kong F, Shi X, Cao H (2006) Morphological response of Microcystis aeruginosa to grazing by different sorts of zooplankton. Hydrobiologia 563:225–230

    Article  Google Scholar 

  • Yang Z, Kong F, Shi X, Zhang M, Xing P, Cao H (2008) Changes in the morphology and polysaccharide content of Microcystis aeruginosa (Cyanobacteria) during flagellate grazing. J Phycol 44:716–720

    Article  Google Scholar 

  • Yang Z, Geng L, Wang W, Zhang J (2012) Combined effects of temperature, light intensity, and nitrogen concentration on the growth and polysaccharide content of Microcystis aeruginosa in batch culture. Biochem Syst Ecol 41:130–135

    Article  CAS  Google Scholar 

  • Ye H, Yuan X, Ge M, Li J, Sun H (2010) Water chemistry characteristics and controlling factors in the northern rivers in the Taihu Basin. Ecol Environ Sci 19:23–27

    Google Scholar 

  • Yu G, He P, Shao L (2009) Characteristics of extracellular polymeric substances (EPS) fractions from excess sludges and their effects on bioflocculability. Bioresour Technol 100:3193–3198

    Article  CAS  Google Scholar 

Download references

Funding

This study was sponsored by the National Natural Science Foundation of China (31470507), the Fundamental Research Funds for the Central Universities (2019B14014), and PAPD, the National Water Pollution Control and Treatment Science and Technology Major Project (2017ZX07603).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiao Tan.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(PDF 187 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tan, X., Shu, X., Duan, Z. et al. Two types of bound extracellular polysaccharides and their roles in shaping the size and tightness of Microcystis colonies. J Appl Phycol 32, 255–262 (2020). https://doi.org/10.1007/s10811-019-01937-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-019-01937-z

Keywords

Navigation