Skip to main content

Advertisement

SpringerLink
Log in

Effects of rice straw on the cell viability, photosynthesis, and growth of Microcystis aeruginosa

  • Biology
  • Published:
Chinese Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

Rice straw is supposed to be an environment-friendly biomaterial for inhibiting the growth of harmful blooms of the cyanobacterium Microcystis aeruginosa. However, its potential mechanism is not well known. To explore this mechanism, the growth, cell viability (esterase activity, membrane potential, and membrane integrity), photosynthesis, and cell size of M. aeruginosa were determined using flow cytometry and Phyto-PAM after exposure to rice straw extracts (RSE). The results show that doses from 2.0 to 10.0 g/L of RSE efficiently inhibited the alga for 15 days, while the physiologic and morphologic responses of the cyanobacteria were time-dependent. RSE interfered with the cell membrane potential, cell size, and in vivo chlorophyll-a fluorescence on the first day. After 7 days of exposure, RSE was transported into the cytosol, which disrupted enzyme activity and photosynthesis. The cyanobacteria then started to repair its physiology (enzyme activity, photosynthesis) and remained viable, suggesting that rice straw act as an algistatic agent.

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

Similar content being viewed by others

References

  • Amor K B, Breeuwer P, Verbaarschot P, Rombout F M, Akermans A D L, De Vos W M, Abee T. 2002. Muliparametric flow cytometry and cell sorting for the assessment of viable, injured, and dead bifidobacterium cells during bile salt stress. Appl. Environ. Microbiol., 68(11): 5 209–5 216.

    Article  Google Scholar 

  • Anderson D M, Kaoru Y, White A W. 2000. Estimated annual economic impacts from harmful algal blooms (HABs) in the United States. WHOI-2000-11Woods Hole Oceanogr Inst, Woods Hole, Massachusetts. http://www.whoi.edu/redtide/pertinentinfo/Economics_report.pdf. Accessed on 2012-10-10.

    Google Scholar 

  • Bailey S, Clokie M R, Millard A, Mann N H. 2004. Cyanophage infection and photoinhibition in marine cyanobacteria. Res. Microbiol., 155: 720–725.

    Article  Google Scholar 

  • Brookes J D, Geary S M, Ganf G G, Burch M D. 2000. Use of FDA and flow cytometry to assess metabolic activity as an indicator of nutrient status in phytoplankton. Mar. Freshwater Res., 51: 817–823.

    Article  Google Scholar 

  • Choe S, Jung I H. 2002. Growth inhibition of freshwater algae by ester compounds released from rotted plants. J. Ind. Eng. Chem., 8: 297–304.

    Google Scholar 

  • Chung I M, Ali M, Ahmad A, Chun S C, Kim J T, Sultana S. 2007. Steroidal constituents of rice (Oryza sativa) hulls with algicidal and herbicidal activity against blue-green algae and duckweed. Phytochem. Anal., 18: 133–145.

    Article  Google Scholar 

  • Daniel E T, Ferrier M D, Armbrester E A, Anlauf K A. 2002. Inhibition of dinoflagellate growth by extracts of barley straw (Hordeum vulgare). J. Appl. Phycol., 14: 275–280.

    Article  Google Scholar 

  • Emily K P, Tracey L M. 2008. Effects of harmful algal blooms on competitors: allelopathic mechanisms of the red tide dinoflagellate Karenia brevis. Limnol. Oceanogr., 53(2): 531–541.

    Article  Google Scholar 

  • Feng J, Zhu Q, Wu W Z. 2008. Mechanisms of algal inhibition by rice straw extract. Environ. Sci., 29(12): 3 376–3 381. (in Chinese with English abstract)

    Google Scholar 

  • Ferrier M, Butler B, Terlizzi D, Lacouture R. 2005. The effects of barley straw on the growth of freshwater algae. Bioresour. Technol., 96: 1 788–1 795.

    Article  Google Scholar 

  • Gibson M, Welch I, Barrett P R F, Ridge I. 1990. Barley straw as an inhibitor of algal growth II: laboratory studies. J. Appl. Phycol., 2: 241–248.

    Article  Google Scholar 

  • Hagström J A, Sengco M R, Villareal T A. 2010. Potential methods for managing Prymnesium parvum blooms and toxicity, with emphasis on clay and barley straw: a review. J. Am. Water. Resour. Assoc., 46(1): 187–198.

    Article  Google Scholar 

  • Jochem F J. 1999. Dark survival strategies in marine phytoplankton assessed by cytometric measurement of metabolic activity with fluorescein diacetate. Mar. Biol., 135(4): 721–728.

    Article  Google Scholar 

  • Johnson I. 1998. Fluorescent probes for living cells. The Histochemical Journal, 30: 123–140.

    Article  Google Scholar 

  • Jüttner F, Wu J T. 2000. Evidence of allelochemical activity in subtropical cyanobacterial biofilms of Taiwan. Archiv. Für. Hydrobiologie, 147(4): 505–517.

    Google Scholar 

  • Lawrence J E, Brussaard C P D, Suttle C A. 2006. Virusspecific responses of Heterosigma akashiwo to infection. Appl. Environ. Microb., 72: 7 829–7 834.

    Article  Google Scholar 

  • Legrand C, Rengefors K, Fistarol G O, Granėli E. 2003. Allelopathy in phytoplankton-biochemical, ecological and evolutionary aspects. Phycologia, 42(4): 406–419.

    Article  Google Scholar 

  • Li F M, Hu H Y. 2005. Isolation and characterization of novel antialgal allelochemical from Phragmites communis. Appl. Environ. Microbiol., 71(11): 6 545–6 553.

    Article  Google Scholar 

  • Liu J S, Yang W D, Gao J. 2007. Inhibitory effects of rice straw and barely straw on the growth on Phaeocystis globosa. Acta Ecological Sinica, 27(11): 4 498–4 505. (in Chinese with English abstract)

    Google Scholar 

  • Millennium Ecosystem Assessment. 2005. Ecosystems and Human Well-Being: Synthesis. Island Press, Washington DC USA. p.1–15.

    Google Scholar 

  • Monfort P, Baleux B. 1996. Cell cycle characteristics and changes in membrane potential during growth of Escherichia coli as determined by a cyanine fluorescent dye and flow cytometry. J. Microbiol. Methods, 25(1): 79–86.

    Article  Google Scholar 

  • Muller S, Ullrich S, Losche A, Loffhagen N, Babel W. 2000. Flow cytometric techniques to characterise physiological states of Acinetobacter calcoaceticus. J. Microbiol. Meth., 40: 67–77.

    Article  Google Scholar 

  • Murray D, Jefferson B, Jarvis P, Parsons S A. 2010. Inhibition of three algae species using chemicals released from barley straw. Environ. Technol., 31(4): 455–466.

    Article  Google Scholar 

  • Newman J R, Barrett P R F. 1993. Control of Microcystis aeruginosa by decomposing barley straw. J. Aquat. Plant. Manage., 31: 203–206.

    Google Scholar 

  • Novo D J, Perlmutter N G, Hunt R H, Shapiro H M. 2000. Multiparameter flow cytometric analysis of antibiotic effects on membrane potential, membrane permeability, and bacterial counts of Staphylococcus aureus and Micrococcus luteus. Antimicrob. Agents Chemother., 44: 827–834.

    Article  Google Scholar 

  • Pan G, Zou H, Chen H, Yuan X. 2006. Removal of harmful cyanobacterial blooms in Taihu Lake using local soils III. Factors affecting the removal efficiency and an in situ field experiment using chitosan-modified local soils. Environ. Pollut., 141: 206–212.

    Article  Google Scholar 

  • Park M H, Han M S, Ahn C Y, Kim H S, Yoon B D. 2006. Growth inhibition of bloom — forming cyanobacterium Microcystis aeruginosa by rice straw extract. Lett. Appl. Microbiol., 43: 307–312.

    Article  Google Scholar 

  • Park M H, Chung I M, Ahmad A, Kim B H, Hwang S J. 2009a. Growth inhibition of unicellular and colonial Microcystis strains (Cyanophyceae) by compounds isolated from rice (Oryza sativa) hulls. Aquat. Bot., 90: 309–314.

    Article  Google Scholar 

  • Park M H, Kim B H, Chung I M, Hwang S J. 2009b. Selective bactericidal potential of rice (Oryza sativa L. var. japonica) hull extract on Microcystis strains in comparison with green algae and zooplankton. Bull. Environ. Contam. Toxicol., 83: 97–101.

    Article  Google Scholar 

  • Penyige A, Matkó J, Deák E, Bodnár A, Barabás G. 2002. Depolarization of the membrane potential by β-Lactams as a singal to induce autolysis. Biochem. Biophys. Res. Commun., 290: 1 169–1 175.

    Article  Google Scholar 

  • Prado R, García R, Rioboo C, Herrero C, Abalde J, Cid A. 2009. Comparison of the sensitivity of different toxicity test endpoints in a microalga exposed to the herbicide paraquat. Environ. Int., 35: 240–247.

    Article  Google Scholar 

  • Rippka R, Deruelles J, Waterbury J B, Herdman M, Stanier R Y. 1979. Genetic assignments, stain histories and properties of pure culture of cyanobacteria. J. Gen. Microbiol., 111: 1–61.

    Article  Google Scholar 

  • Schenk M, Raffellini S, Guerrero S, Blanco G A, Alzamora S M. 2011. Inactivation of Escherichia coli, Listeria innocua and Saccharomyces cerevisiae by UV-C light: study of cell injury by flow cytometry. LWT-Food. Sci. Technol., 44: 191–198.

    Article  Google Scholar 

  • Shapiro H M. 2000. Membrane potential estimation by flow cytometry. Methods, 21: 271–279.

    Article  Google Scholar 

  • Street M. 1978. Research on the improvement of gravel pits for waterfowl by adding straw. Game. Conserv. Annu. Rev., 10: 56–61.

    Google Scholar 

  • Suggett D J, Borowitzka M A, Prášil O. 2010. Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications. Springer, London. p.427–433.

    Book  Google Scholar 

  • Thompson P A, Harrison P J, Parslow J S. 1991. Influence of irradiance on cell-volume and carbon quota for 10 species of marine-phytoplankton. J. Phycol., 27: 351–360.

    Article  Google Scholar 

  • Tiffany L W, Park S W, Vivanco M J. 2004. Biochemical and physiological mechanisms mediated by allelochemicals. Curr. Opin. Plant. Biol., 7: 472–479.

    Article  Google Scholar 

  • Ueckert J, Breeuwer P, Abee T, Stephens P, Nebe von Caron G, ter Steeg P F. 1995. Flow cytometry applications in physiological study and detection of foodborne microorganisms. Int. J. Food Microbiol., 28: 317–326.

    Article  Google Scholar 

  • Veldhuis M J W, Kraay G W. 2000. Application of flow cytometry in marine phytoplankton research: current applications and future perspectives. Sci. Mar., 64: 121–134.

    Article  Google Scholar 

  • Vives-Rego J, Lebaron P, Nebe von Caron G. 2000. Current and future applications of flow cytometry in aquatic microbiology. Fems. Micvrobiol. Rev., 24: 429–448.

    Article  Google Scholar 

  • Xiao X, Chen Y, Liang X, Lou L, Tang X. 2010. Effects of Tibetan hulless barley on bloom-forming cyanobacterium (Microcystis aeruginosa) measured by different physiological and morphologic parameters. Chemosphere, 81: 1 118–1 123.

    Article  Google Scholar 

  • Yu J Q, Matsui Y. 1997. Effects of root exudates of cucumber (Cucumis sativus) and allelochemicals on ion uptake by cucumber seedlings. J. Chem. Ecol., 23(3): 817–827.

    Article  Google Scholar 

  • Yu Y, Kong F, Wang M, Qian L, Shi X. 2007. Determination of short-term copper toxicity in a multispecies microalgal population using flow cytometry. Ecotox. Environ. Safe, 66: 49–56.

    Article  Google Scholar 

  • Zhang M, Kong F, Tan X, Yang Z, Cao H S, Xing P. 2007a. Biochemical, morphological and genetical variations in Microcystis aeruginosa due to colony disaggregation. World J. Microb. Biot., 23(5): 663–670.

    Article  Google Scholar 

  • Zhang M, Kong F X, Xing P, Tan X. 2007b. Effects of interspecific interactions between Microcystis aeruginosa and Chlorella pyrenoidosa on their growth and physiology. Int. Rev. Hydrobiol., 92: 281–290.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. State Key Laboratory of Lake & Environment Science, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, 210008, China

    Wen Su  (苏文), Yuhong Jia  (贾育红), Yaping Lu  (卢亚萍) & Fanxiang Kong  (孔繁翔)

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Wen Su  (苏文)

  3. Ecology and Evolution in Microbial Model Systems, EEMiS, School of Natural Sciences, Linnaeus University, 39182, Kalmar, Sweden

    Johannes A. Hagström

Authors
  1. Wen Su  (苏文)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johannes A. Hagström
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuhong Jia  (贾育红)
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yaping Lu  (卢亚萍)
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fanxiang Kong  (孔繁翔)
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fanxiang Kong  (孔繁翔).

Additional information

Supported by the National Basic Research Program of China (973 Program) (No. 2008CB418002), the National Major Science and Technology Program for Water Pollution Control and Treatment (No. 2012ZX07103-002), the CAS/SAFEA International Partnership Program for Creative Research Teams of Chinese Academy of Sciences (No. KZZDEW-TZ-08-01), and the National Natural Science Foundation of China (No. 20807043)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Su, W., Hagström, J.A., Jia, Y. et al. Effects of rice straw on the cell viability, photosynthesis, and growth of Microcystis aeruginosa . Chin. J. Ocean. Limnol. 32, 120–129 (2014). https://doi.org/10.1007/s00343-014-3063-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-014-3063-0

Keyword

Search

Navigation