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Use of lactic acid bacteria as a biological agent against the cyanobacterium Anabaena flos-aquae

Abstract

In the present study, we assessed whether lactic acid bacteria (LAB) with antimicrobial activity could be used to effectively control Anabaena flos-aquae growth. In our screening of cyanobacteriacidal bacteria from 14 LAB strains belonging to 11 species, we selected six candidate strains that could lyse 90 % or more A. flos-aquae cells compared with a control. Of those, Lactobacillus paraplantarum KCTC 5045T had the strongest cyanobacteriacidal activity showing complete lysis of cyanobacterial cells at the initial densities of ≥104 cells mL−1. A host range assay revealed that L. paraplantarum strongly inhibited A. flos-aquae, Anabaena crassa, Stephanodiscus hantzschii, and Peridinium bipes but weakly inhibited or stimulated the growth of Scenedesmus actus, Pediastrum sp., Cyclotella meneghiniana, Coelastrum reticulatum, Chlamydomonas sp., and Microcystis aeruginosa. In the microcosm experiment using natural freshwater including abundant phytoplankton assemblage, moreover, the LAB under inoculation of about 105 cells mL−1 could completely terminate the co-growth of A. flos-aquae, A. crassa, Anabaena circinalis, and other Anabaena spp. (over 104 cells mL−1) without a secondary bloom by another algal and cyanobacterial species. Our observation revealed that the cyanobacteriacidal bacterium releases two or more extracellular compounds possessing cyanobacteriacidal activity without cell-to-cell contact when the host cyanobacterium necessarily exits in surrounding water. Property study of cyanobacteriacidal substance revealed the release of heat stable and hydrophobic chemical substances that do not appear to be protein and peptide compound. Taken together, our results indicate that LAB may be a potential bio-agent for future use in controlling freshwater Anabaena blooms without causing the problem of pathogenicity if there is no secondary bloom by a resistant species to this bacterium.

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References

  • Beakes G, Canter HM, Jaworski GHM (1988) Zoospores ultrastructure of Zygorhizidium affluens Canter and Z. planktonicum Canter, two hytrids parasitizing the diatom Asterionella Formosa. Hassall. Can J Bot 66:1054–1067

    Article  Google Scholar 

  • Berg KA, Lyra C, Sivonen K, Paulin L, Suomalainen S, Tuomi P, Rapala J (2009) High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms. ISME J 3:314–325

    CAS  Article  PubMed  Google Scholar 

  • Billkova A, Kinova Sepova H, Bukovsky M, Bezakova L (2011) Antibacterial potential of lactobacilli isolated from a lamb. Vet Med 56:319–324

    Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  Article  PubMed  Google Scholar 

  • Bringel F, Castioni A, Olukoya DK, Fekis GE, Torriani S, Dellaglio F (2005) Lactobacillus plantarum subsp. argentoratensis subsp. nov., isolated from vegetable matrices. Int J Syst Evol Microbiol 55:1629–1634

  • Carmichael WW (1992) A status report of planktonic cyanobacteria (blue-green algae and their toxins). #EPA/600/R-92/079. United States Environmental Protection Agency, Washington, DC, USA

  • Choi H-J, Kim B-H, Kim J-D, Han M-S (2005) Streptomyces neyagawaensis as a control for the hazardous biomass of Microcystis aeruginosa (Cyanobacteria) in eutrophic freshwater. Biol Control 33:335–343

    Article  Google Scholar 

  • Curk M-C, Hubert J-C, Bringel F (1996) Lactobacillus paraplantarum sp. nov., a new species related to Lactobacillus platarum. Int J Syst Bacteriol 46:595–598

    CAS  Article  PubMed  Google Scholar 

  • de Man JD, Rogosa M, Sharpe ME (1960) A medium for the cultivation of Lactobacilli. J Appl Bacteriol 23:130–135

    Article  Google Scholar 

  • de Vuyst L, Vandamme EJ (1994) Antimicrobial potential of lactic acid bacteria. In: DeVuyst L, Vandamme EJ (eds) Bacteriocins of lactic acid bacteria: microbiology, genetics and applications, 1st edn. Blackie Academic, London, pp 1–8

    Chapter  Google Scholar 

  • Fraleigh PC, Burnham JC (1988) Myxococcal predation on cyanobacterial populations: nutrient effects. Limnol Oceanogr 33:476–483

    CAS  Article  Google Scholar 

  • Giraud E, Gosselin L, Raimbault M (1992) Degradation of cassava linamarin by lactic acid bacteria. Biotechnol Lett 14:593–598

    CAS  Article  Google Scholar 

  • Gueguen Y, Chemardin P, Labrot P, Arnaud A, Galzy P (1997) Purification and characterization of an intracellular β-glucosidase from a new strain of Leuconostoc mesenteroides isolated from cassava. J Appl Microbiol 82:469–476

    CAS  Article  Google Scholar 

  • Gumbo JR, Ross G, Cloete TE (2010) The isolation and identification of predatory bacteria from a Microcystis algal bloom. Afr J Biotechnol 9:663–671

    CAS  Google Scholar 

  • Haarman M, Jan K (2006) Quantitative real-time PCR analysis of fecal Lactobacillus species in infants receiving a prebiotic infant formula. Appl Environ Microbiol 72:2359–2365

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Imai I, Ishida Y, Hata Y (1993) Killing of marine phytoplankton by a gliding bacterium Cytophaga sp., isolated from the coastal sea of Japan. Mar Biol 116:527–532

    Article  Google Scholar 

  • Kang Y-H, Kim J-D, Kim B-H, Kong DS, Han M-S (2005) Isolation and characterization of a bio-agent antagonistic to diatom, Stephanodiscus hantzschii. J Appl Microbiol 98:1030–1038

    CAS  Article  PubMed  Google Scholar 

  • Kang Y-H, Kim B-R, Choi H-J, Seo JG, Kim B-H, Han M-S (2007) Enhancement of algicidal activity by immobilization of algicidal bacteria antagonistic to Stephanodiscus hantzschii (Bacillariophyceae). J Appl Microbiol 103:1983–1994

    CAS  Article  PubMed  Google Scholar 

  • Kang Y-H, Jung SW, Jo S-H, Han M-S (2011) Field assessment of the potential of algicidal bacteria against diatom blooms. Biocontrol Sci Tech 21:969–984

    Article  Google Scholar 

  • Kang Y-H, Jung SW, Joo J-H, Han M-S (2012a) Use of immobilized algicidal bacteria to control natural freshwater diatom blooms. Hydrobiologia 683:151–162

    CAS  Article  Google Scholar 

  • Kang Y-H, Park C-S, Han M-S (2012b) Pseudomonas aeruginosa UCBPP-PA14 as a useful bacterium capable of lysing M. aeruginosa cells and degrading microcystins. J Appl Phycol 24:1517–1525

  • Kim J-D, Han M-S (2004) Enzyme profiles of alga-lytic bacterial strain AK-13 related with elimination of cyanobacterium Anabaena cylindrica. Kor J Environ Biol 22:184–191

    Google Scholar 

  • Kim M, Lee S-J, Seul K-J, Park Y-M, Ghim S-Y (2009) Characterization of antimicrobial substance produced by Lactobacillus paraplantarum HNUC25 isolated from kimchi. Kor J Microbiol Biotechnol 37:24–32

    CAS  Google Scholar 

  • Koss AM, Snyder WE (2004) Alternative prey disrupt biocontrol by guild of generalist predators. Biol Control 10:1–9

    Google Scholar 

  • Lee J-H, Kim M, Um S (2004) PCR-based detection and identification of Lactobacillus plantarum, Lactobacillus pentosus, and Lactobacillus paraplantarum in kimchi. Food Sci Biotechnol 13:754–757

    CAS  Google Scholar 

  • Leia V, Amoa-Awuab WKA, Brimerc L (1999) Degradation of cyanogenic glycosides by Lactobacillus plantarum strains from spontaneous cassava fermentation and other microorganisms. Int J Food Microbiol 53:169–184

    Article  Google Scholar 

  • Lovejoy C, Bowman JP, Hallegraeff GM (1998) Algicidal effects of a novel marine Pseudoalteromonas isolated (class Proteobacteria, Gamma subdivision) on harmful algal bloom species of the genera Chatonella, Gymnodinium, and Heterosigma. Appl Environ Microbiol 64:2806–2813

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manage PM, Kawabata Z, Nakano S (2000) Algicidal effect of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat Microb Ecol 22:111–117

    Article  Google Scholar 

  • NIES (2004) Microalgae and Protozoa. In: Watanabe MM, Hiroki M, Kasai F, Kawachi M, Shimizu A, Erata M, Mori F, Yumoto K (eds) NIES-collection: list of strains, 6th edn. National Institute for Environmental Studies, Tsukuba, Japan, pp 50–51

    Google Scholar 

  • Park YT, Park JB, Chung SY, Song BC, Lim WA, Kim CH, Lee WJ (1998) Isolation and algicidal properties of Micrococcus sp. LG-1 possessing killing activity for harmful Dinoflagellate Cochlodinium polykrikoides. J Kor Fish Soc 31:767–773

    Google Scholar 

  • Park BS, Baek SH, Ki J-S, Cattolico RA, Han M-S (2012) Assessment of EvaGreen-based quantitative real-time PCR assay for enumeration of the microalgae Heterosigma and Chattonella (Raphidophyceae). J Appl Phycol 24:1555–1567

    CAS  Article  Google Scholar 

  • Reim RL, Shane MS, Cannon RE (1974) The characterization of a Bacillus capable of blue-green bactericidal activity. Can J Microbiol 20:981–986

    CAS  Article  PubMed  Google Scholar 

  • Ren H, Zhang P, Liu C, Xue Y, Lian B (2010) The potential use of bacterium strain R219 for controlling of the bloom-forming cyanobacteria in freshwater lake. World J Microbiol Biotechnol 26:465–472

    CAS  Article  Google Scholar 

  • Rubenchik L I, Bershova O I, Knizhnik ZP (1965) On the interrelationship of Anabaena with bacteria and actinomycetes. In: Ecologia i physiologia sinezelenych vodorosleiy. Nauka Moscow: 223–226

  • Saarisalo E, Skytta E, Haikara A, Jalava T, Jaakkola S (2007) Screening and selection of lactic acid bacteria strains suitable for ensiling grass. J Appl Microbiol 102:327–336

    CAS  Article  PubMed  Google Scholar 

  • Shilo M (1970) Lysis of blue green algae by myxobacter. J Bacteriol 104:453–461

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sigee DC, Glenn R, Andrews MJ, Bellinger EG, Butler RD, Epton HAS, Hendry RD (1999) Biological control of cyanobacteria: principles and possibilities. Hydrobiologia 395/396:161–172

  • Soomro AH, Masud T, Anwaar K (2002) Role of latic acid bacteria (LAB) in food preservation and human health—a review. Pak J Nutr 1(1):20–24

    Article  Google Scholar 

  • Torriani S, Clementi F, Vancanneyt M, Hoste B, Dellaglio F, Kersters K (2001) Differentiation of Lactobacillus plantarum, L. pentosus and L. paraplantarum species by RAPD-PCR and AFLP. Syst Appl Microbiol 24:554–560

    CAS  Article  PubMed  Google Scholar 

  • Walker HL, Patrick CL (1998) Method of isolating and propagating microorganisms and viruses. U.S. Patent No. 5,739,019

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Acknowledgments

This project was supported by the Korea Ministry of Environment (2013001470001 to M.-S. H.) and by National Research Foundation of Korea (NRF) grants funded by the Korea government (MSIP) Grants (NRF-2011-0017199 to J.-W. L.). We specially thank our colleagues of the Monitoring and Analysis Division, Wonju Regional Environmental Office, Ministry of Environment for their technical assistance.

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Correspondence to Jin-Won Lee or Myung-Soo Han.

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Yoon-Ho Kang and Su-Kyung Kang contributed equally to this work.

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Kang, YH., Kang, SK., Park, CS. et al. Use of lactic acid bacteria as a biological agent against the cyanobacterium Anabaena flos-aquae . J Appl Phycol 28, 1747–1757 (2016). https://doi.org/10.1007/s10811-015-0701-7

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  • DOI: https://doi.org/10.1007/s10811-015-0701-7

Keywords

  • Lactic acid bacteria
  • Cyanobacteriacidal bacteria
  • Anabaena flos-aquae
  • Biological control