Skip to main content
Log in

Interspecific variation in extracellular polysaccharide content and colony formation of Microcystis spp. cultured under different light intensities and temperatures

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

Abstract

Single cells of five different Microcystis species (M. ichthyoblabe, M. viridis, M. flos-aquae, M. wesenbergii, and M. aeruginosa) were batch-cultured at different temperatures and light intensities: (a) 25 °C and 50 μmol photons m−2 s−1 (control culture); (b) 25 °C and 10 μmol photons m−2 s−1; and (c) 15 °C and 50 μmol photons m−2 s−1. The extracellular polysaccharide content was significantly higher in treatments b and c than in the control treatment. All Microcystis species existed as single cells under the control treatment but formed colonies in treatments b and c. All of the colonies were irregular with indistinct margins. M. ichthyoblabe, M. viridis, M. flos-aquae, and M. wesenbergii formed colonies with similar morphologies and their cells were loosely aggregated. In contrast, M. aeruginosa formed denser colonies with no distinct holes. The colony morphologies differed from the classic morphology of M. ichthyoblabe field-grown colonies but resembled that of small colonies found in Lake Taihu (Yangtze Delta Plain, China) during early spring. This indicates that field- and laboratory-grown colonies are governed by similar formation processes. We suggest that in laboratory and field environments, M. ichthyoblabe (or M. flos-aquae) colonies are representative of small colonies formed from single Microcystis cells, whereas the morphology of older colonies evolves to resemble M. wesenbergii and M. aeruginosa colonies.

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Amano Y, Hosoi T, Machida M, Imazeki F (2013) Effects of extracellular polymeric substances (EPS) and iron ion on colony formation of unicellular Microcystis aeruginosa. J Jpn Soc Civil Eng 69:39–44

    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  PubMed  Google Scholar 

  • Burkert U, Hyenstrand P, Drakare S, Blomqvist P (2001) Effects of the mixotrophic flagellate Ochromonas sp. on colony formation in Microcystis aeruginosa. Aquat Ecol 35:11–17

    Article  Google Scholar 

  • Cao H, Yang Z (2010) Variation in colony size of Microcystis aeruginosa in a eutrophic lake during recruitment and bloom formation. J Freshw Ecol 25:331–335

    Article  Google Scholar 

  • Chalifour A, Juneau P (2011) Temperature-dependent sensitivity of growth and photosynthesis of Scenedesmus obliquus, Navicula pelliculosa and two strains of Microcystis aeruginosa to the herbicide atrazine. Aquat Toxicol 103:9–17

    Article  CAS  PubMed  Google Scholar 

  • e Mello MM, Soares MCS, Roland F, Lürling M (2012) Growth inhibition and colony formation in the cyanobacterium Microcystis aeruginosa induced by the cyanobacterium Cylindrospermopsis raciborskii. J Plankton Res 34:987–994

    Article  Google Scholar 

  • Forni C, Telo FR, Caiola MG (1997) Comparative analysis of the polysaccharides produced by different species of Microcystis (Chroococcales, Cyanophyta). Phycologia 36:181–185

    Article  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  PubMed  Google Scholar 

  • Imai H, Chang KH, Nakano SI (2009a) Growth responses of harmful algal species Microcystis (Cyanophyceae) under various environmental conditions. In: Obatashi Y, Isobe T, Subramanian A, Suzuki S, Tanabe S (eds) Interdisciplinary studies on environmental chemistry-environmental research in Asia. Terrapub, Tokyo, pp 269–275

    Google Scholar 

  • Imai H, Chang KH, Kusaba M, Nakano SI (2009b) Temperature-dependent dominance of Microcystis (Cyanophyceae) species: M. aeruginosa and M. wesenbergii. J Plankton Res 31:171–178

    Article  Google Scholar 

  • Li M, Zhu W, Gao L, Huang J, Li L (2013a) Seasonal variations of morphospecies composition and colony size of Microcystis in a shallow hypertrophic lake (Lake Taihu, China). Fresenius Environ Bull 22:3474–3483

    CAS  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, Nkrumah P, Xiao M (2014a) Biochemical composition of Microcystis aeruginosa related to specific growth rate: insight into the effects of abiotic factors. Inland Waters 4:357–362

    Article  Google Scholar 

  • Li M, Zhu W, Gao L (2014b) 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, Sun Q (2014c) Solubilisation of mucilage induces changes in Microcystis colonial morphology. N Z J Mar Freshw Res 48:38–47

    Article  CAS  Google Scholar 

  • Ma J, Brookes JD, Qin B, Paerl HW, Gao G, Wu P, Zhang W, Deng J, Zhu G, Zhang Y (2014) Environmental factors controlling colony formation in blooms of the cyanobacteria Microcystis spp. in Lake Taihu, China. Harmful Algae 31:36–142

    Article  Google Scholar 

  • Marinho MM, Souza MBG, Lürling M (2013) Light and phosphate competition between Cylindrospermopsis raciborskii and Microcystis aeruginosa is strain dependent. Microbial Ecol 66:479–488

  • Otsuka S, Suda S, Li R, Matsumoto S, Watanabe MM (2000) Morphological variability of colonies of Microcystis morphospecies in culture. J Gen Appl Microbiol 46:39–50

    Article  CAS  PubMed  Google Scholar 

  • Ozawa K, Fujioka H, Muranaka M, Yokoyama A, Katagami Y, Homma T, Ishikawa K, Tsujimura S, Kumagai M, Watanabe MF (2005) Spatial distribution and temporal variation of Microcystis species composition and microcystin concentration in Lake Biwa. Environ Toxicol 20:270–276

    Article  CAS  PubMed  Google Scholar 

  • Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microbial Ecol 65:995–1010

    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 

  • Shirai M, Matumaru K, Ohotake A, Takamura Y, Aida T, Nakano M (1989) Development of a solid medium for growth and isolation of axenic Microcystis strains (cyanobacteria). Appl Environ Microbiol 55:2569–2571

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, CohenBazire G (1971) Purification and properties of unicellular bluegreen algae (Order Chroococcales). Bacteriol Rev 35:171–205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Q, Zhu W, Li M, Tan X (2015) Morphological changes of Microcystis aeruginosa colonies in culture. J Limnol. doi:10.4081/jlimnol.2015.1225

    Google Scholar 

  • Timothy WD, Berry DL, Boyer GL, Gobler CJ (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8:715–725

    Article  Google Scholar 

  • Tsujimura S, Tsukada H, Nakahara H, Nakajima T, Nishino M (2000) Seasonal variations of Microcystis populations in sediments of Lake Biwa, Japan. Hydrobiologia 434:183–192

    Article  Google Scholar 

  • Wang C, Kong H, He S, Zheng X, Li C (2010a) The inverse correlation between growth rate and cell carbohydrate content of Microcystis aeruginosa. J Appl Phycol 22:105–107

    Article  Google Scholar 

  • Wang W, Liu Y, Yang Z (2010b) Combined effects of nitrogen content in media and Ochromonas sp. grazing on colony formation of cultured Microcystis aeruginosa. J Limnol 69:193–198

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Li G, Li G, Li D (2012) The decline process and major pathways of Microcystis bloom in Taihu Lake, China. Chin J Oceanol Limnol 30:37–46

    Article  CAS  Google Scholar 

  • Wu X, Kong F (2009) Effects of light and wind speed on the vertical distribution of Microcystis aeruginosa colonies of different sizes during a summer bloom. Int Rev Hydrobiol 94:258–266

    Article  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 

  • 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 71:61–66

    Article  CAS  Google Scholar 

  • Yang Z, Kong F (2013) Abiotic factors in colony formation: effects of nutrition and light on extracellular polysaccharide production and cell aggregates of Microcystis aeruginosa. Chin J Oceanol Limnol 31:796–802

    Article  CAS  Google Scholar 

  • Yang Z, Kong F, Shi X (2005) Effects of filtered lake water on colony formation and growth rate in Microcystis aeruginosa of different physiological phases. J Freshw Ecol 20:425–429

    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, Xing P, Zhang M (2007) Effects of Daphnia-associated infochemicals on the morphology, polysaccharides content and PSII-efficiency in Scenedesmus obliquus. Int Rev Hydrobiol 92:618–625

    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  PubMed  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 

  • Zhai C, Song S, Zou S, Liu C, Xue Y (2013) The mechanism of competition between two bloom-forming Microcystis species. Freshw Biol 58:1831–1839

    Article  CAS  Google Scholar 

  • Zhu W, Li M, Luo Y, Dai X, Guo L, Xiao M, Huang J, Tan X (2014a) Vertical distribution of Microcystis colony size in Lake Taihu: Its role in algal blooms. J Great Lakes Res 40:949–955

    Article  Google Scholar 

  • Zhu W, Dai X, Li M (2014b) Relationship between extracellular polysaccharide (EPS) content and colony size of Microcystis is colonial morphology dependent. Biochem Syst Ecol 55:346–350

    Article  CAS  Google Scholar 

  • Zhu W, Li M, Dai X, Xiao M (2015a) Differences in vertical distribution of Microcystis morphospecies composition in a shallow hypertrophic lake (Lake Taihu, China). Environ Earth Sci 73:5721–5730

    Article  CAS  Google Scholar 

  • Zhu W, Sun Q, Chen F, Li M (2015b) Cellular N:P ratio of Microcystis as an indicator of nutrient limitation - implications and applications. Environ Earth Sci. doi:10.1007/s12665-015-4707-x

    Google Scholar 

Download references

Acknowledgments

This study was sponsored by the National Natural Science Foundation of China (Grant 51409216), the Program on Furtherance of Scientific Research of Japan, Fundament C (15K00630) and the China Postdoctoral Science Foundation (Grant 2014M562459).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ming Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, F., Zhu, W., Xiao, M. et al. 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 (2016). https://doi.org/10.1007/s10811-015-0707-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-015-0707-1

Keywords

Navigation