Abstract
Biological control of cyanobacteria is a well-researched area with a central focus on laboratory-scale studies. Numerous reports have been made on algicidal isolates, with bacteria as a major component of the antagonists. The research in this review draws a brief summary of what is currently known in the area of freshwater cyanobacteria being inhibited by bacterial isolates. Proteobacteria, Bacteroidetes and Firmicutes are among the most commonly reported phyla of bacteria associated with or employed in this research area. However, there are limited reports of upscaling these control measures beyond the laboratory scale. Lytic control agents are the most commonly reported in the literature with subsequent cyanotoxin release. From a water quality perspective, this is not feasible. Based on the available literature, temperature, pH and nutrient changes have been explored in this short review as possible contributors to less optimal bacterial performance. Moreover, the investigation into optimising some of these parameters may lead to increased bacterial performance and, therefore, viability for upscaling this biological control. Through the compilation of current research, this review offers insight to live predator-prey cell interactions between cyanobacteria and algicidal bacteria.
Similar content being viewed by others
References
Adam B, Klawonn I, Sveden JB, Bergkvist J, Nahar N, Walve J, Littmann S, Whitehouse MJ, Lavik G, Kuypers MMM, Ploug H (2016) N2-fixation, ammonium release and N-transfer to the microbial and classical food web within a plankton community. ISME J 10:450–459. https://doi.org/10.1038/ismej.2015.126
Atalah J, Hopkins GA, Fletcher LM, Castinel A, Forrest BM (2015) Concepts for biocontrol in marine environments: is there a way forward? Manag Biol Invasion 6:1–12. https://doi.org/10.3391/mbi.2015.6.1.01
Bagatini IL, Eiler A, Bertilsson S, Klaveness D, Tessarolli LP, Vieira AAH (2014) Host-specificity and dynamics in bacterial communities associated with bloom-forming freshwater phytoplankton. PLoS One 9:e85950. https://doi.org/10.1371/journal.pone.0085950
Bouvy M, Pagano M, Troussellier M (2001) Effects of a cyanobacterial bloom (Cylindrospermopsis raciborskii) on bacteria and zooplankton communities in Ingazeira reservoir (Northeast Brazil). Aquat Microb Ecol 25:215–227. https://doi.org/10.3354/ame025215
Cai H, Jiang H, Krumholz LR, Yang Z (2014) Bacterial community composition of size-fractioned aggregates within the phycosphere of cyanobacterial blooms in a eutrophic freshwater lake. PLoS One 9. https://doi.org/10.1371/journal.pone.0102879
Cellamare M, Rolland A, Jacquet S (2010) Flow cytometry sorting of freshwater phytoplankton. J Appl Phycol 22:87–100. https://doi.org/10.1007/s10811-009-9439-4
Chapman IJ (2016) Developing new approaches for monitoring and controlling the toxic cyanobacterium Microcystis through flow-cytometric analysis. Dissertation, Bornemouth University
Chen WM, Sheu FS, Sheu SY (2011) Novel l-amino acid oxidase with algicidal activity against toxic cyanobacterium Microcystis aeruginosa synthesized by a bacterium Aquimarina sp. Enzym Microb Technol 49:372–379. https://doi.org/10.1016/j.enzmictec.2011.06.016
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 freshwaters. Biol Control 33:335–343. https://doi.org/10.1016/j.biocontrol.2005.03.007
Demeke A (2016) Cyanobacteria blooms and biological control methods. Int J Fauna Biol Studies 3(1):32–38
Eiler A, Bertilsson S (2004) Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ Microbiol 6:1228–1243. https://doi.org/10.1111/j.1462-2920.2004.00657.x
Fraleigh PC, Burnham JC (1988) Myxococcal predation on cyanobacterial populations: nutrient effects. Limnol Oceanogr 33:476–483. https://doi.org/10.2307/2837020
Gao E-B, Gui J-F, Zhang Q-Y (2012a) A novel cyanophage with a cyanobacterial nonbleaching protein a gene in the genome. J Virol 86:236–245. https://doi.org/10.1128/JVI.06282-11
Gao Y, Cornwell JC, Stoecker DK, Owens MS (2012b) Effects of cyanobacterial-driven pH increases on sediment nutrient fluxes and coupled nitrification-denitrification in a shallow fresh water estuary. Biogeosciences 9:2697–2710
Geng L, Qin B, Yang Z (2013) Unicellular Microcystis aeruginosa cannot revert back to colonial form after short-term exposure to natural conditions. Biochem Syst Ecol 51:104–108. https://doi.org/10.1016/j.bse.2013.08.027
Graumann PL, Marahiel MA (1999) Cold shock response in Bacillus subtilis. J Mol Microbiol Biotechnol 1:203–209
Gumbo JR, Ross G, Cloete ET (2008) Biological control of Microcystis dominated harmful algal blooms. Afr J Biotechnol 7:4765–4773
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. https://doi.org/10.4314/ajb.v9i5
Gumbo JR, Cloete TE, van Zyl GJJ, Sommerville JEM (2014) The viability assessment of Microcystis aeruginosa cells after co-culturing with Bacillus mycoides B16 using flow cytometry. Phys Chem Earth 72:24–33. https://doi.org/10.1016/j.pce.2014.09.004
Hajdu S, Holinka J, Reichmann S, Hirschl AM, Graninger W, Presterl E (2010) Increased temperature enhances the antimicrobial effects of daptomycin, vancomycin, tigecycline, fosfomycin, and cefamandole on staphylococcal biofilms. Antimicrob Agents Chemother 54:4078–4084. https://doi.org/10.1128/AAC.00275-10
Heisler J, Glibert PM, Burkholder JM, Anderson DM, Cochlan W, Dennison WC, Dortch Q, Gobler CJ, Heil CA, Humphries E, Lewitus A, Magnien R, Marshall HG, Sellner K, Stockwell DA, Stoecker DK, Suddleson M (2008) Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8:3–13. https://doi.org/10.1016/j.hal.2008.08.006
Ji RP, Lu XW, Li XN, Pu YP (2009) Biological degradation of algae and microcystins by microbial enrichment on artificial media. Ecol Eng 35:1584–1588. https://doi.org/10.1016/j.ecoleng.2008.12.031
Ji X, Verspagen JMH, Stomp M, Huisman J (2017) Competition between cyanobacteria and green algae at low versus elevated CO2: who will win, and why? J Exp Bot 68:3815–3828
Jia W, Huang X, Li C (2014) A preliminary study of the algicidal mechanism of bioactive metabolites of Brevibacillus laterosporus on Oscillatoria in prawn ponds. Sci World J 2014:869149–869111. https://doi.org/10.1155/2014/869149
Jung SW, Kim BH, Katano T, Kong DS, Han MS (2008) Pseudomonas fluorescens HYK0210-SK09 offers species-specific biological control of winter algal blooms caused by freshwater diatom Stephanodiscus hantzschii. J Appl Microbiol 105:186–195. https://doi.org/10.1111/j.1365-2672.2008.03733.x
Kim B-H, Sang M, Hwang S-J, Han M-S (2008) In situ bacterial mitigation of the toxic cyanobacterium Microcystis aeruginosa: implications for biological bloom control. Limnol Oceanogr Methods 6:513–522. https://doi.org/10.4319/lom.2008.6.513
Leitão E, Ger KA, Panosso R (2018) Selective grazing by a tropical copepod (Notodiaptomus iheringi) facilitates Microcystis dominance. Front Microbiol 9:301
Lin S, Pan J, Li Z, Liu X, Tan J, Yang H (2014) Characterization of an algicidal bacterium Brevundimonas J4 and chemical defense of Synechococcus sp. BN60 against bacterium J4. Harmful Algae 37:1–7. https://doi.org/10.1016/j.hal.2014.05.002
Louati I, Pascault N, Debroas D, Bernard C, Humbert JF, Leloup J (2015) Structural diversity of bacterial communities associated with bloom-forming freshwater cyanobacteria differs according to the cyanobacterial genus. PLoS One 10:e0140614. https://doi.org/10.1371/journal.pone.0140614
Luo J, Wang Y, Tang S, Liang J, Lin W, Luo L (2013) Isolation and identification of algicidal compound from Streptomyces and algicidal mechanism to Microcystis aeruginosa. PLoS One 8:1–14. https://doi.org/10.1371/journal.pone.0076444
Lürling M, Waajen G, de Senerpont Domis LN (2016) Evaluation of several end-of-pipe measures proposed to control cyanobacteria. Aquat Ecol 50:499–519. https://doi.org/10.1007/s10452-015-9563-y
Man X, Ming L, RC S (2018) Colony formation in the cyanobacterium Microcystis. Biol Rev 0:1399–1420. https://doi.org/10.1111/brv.12401
Manage PM, Kawabata Z, Nakano S (2000) Algicidal effect of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat Microb Ecol 22:111–117
Manage PM, Edwards C, Singh BK, Lawton LA (2009) Isolation and identification of novel microcystin-degrading bacteria. Appl Environ Microbiol 75:6924–6928. https://doi.org/10.1128/AEM.01928-09
Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51:139–144. https://doi.org/10.1111/j.1550-7408.2004.tb00538.x
Membré J-M, Leporq B, Vialette M, Mettler E, Perrier L, Thuault D, Zwietering M (2005) Temperature effect on bacterial growth rate: quantitative microbiology approach including cardinal values and variability estimates to perform growth simulations on/in food. Int J Food Microbiol 100:179–186. https://doi.org/10.1016/j.ijfoodmicro.2004.10.015
Mialet B, Majdi N, Tackx M, Azémar F, Buffan-Dubau E (2013) Selective feeding of bdelloid rotifers in river biofilms. PLoS One 8:e75352. https://doi.org/10.1371/journal.pone.0075352
Mohamed ZA, Hashem M, Alamri SA (2014) Growth inhibition of the cyanobacterium Microcystis aeruginosa and degradation of its microcystin toxins by the fungus Trichoderma citrinoviride. Toxicon 86:51–58. https://doi.org/10.1016/j.toxicon.2014.05.008
Movahedi S, Waites W (2002) Cold shock response in sporulating Bacillus subtilis and its effect on spore heat resistance. J Bacteriol 184:5275–5281. https://doi.org/10.1128/JB.184.19.5275-5281.2002
Mu R m, Fan Z q, Pei H y, Yuan X l, Liu S x, Wang X r (2007) Isolation and algae-lysing characteristics of the algicidal bacterium B5. J Environ Sci. https://doi.org/10.1016/S1001-0742(07)60218-6
Nakamura N, Nakano K, Sugiura N, Matsumura M (2003) A novel cyanobacteriolytic bacterium, Bacillus cereus, isolated from a eutrophic lake. J Biosci Bioeng 95:179–184
Ndlela LL, Oberholster PJ, Van Wyk JH, Cheng PH (2016) An overview of cyanobacterial bloom occurrences and research in Africa over the last decade. Harmful Algae 60:11–26. https://doi.org/10.1016/j.hal.2016.10.001
Nedwell DB (1999) Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbiol Ecol 30:101–111. https://doi.org/10.1111/j.1574-6941.1999.tb00639.x
Nybom S (2013) Biodegradation of cyanobacterial toxins. In: Petre M (ed) InTech, Rijeka, p Ch. 7
Oberholster PJ, Botha AM (2010) Use of remote sensing and molecular markers to detect toxic cyanobacterial hyperscum crust: a case study on Lake Hartbeespoort, South Africa. Afr J Biotechnol 9:8791–8799
Oberholster PJ, Botha A, Myburgh JG (2009) Linking climate change and progressive eutrophication to incidents of clustered animal mortalities in different geographical regions of South Africa. J Biotechnol 8:5825–5832
Oberholster PJ, Jappie S, Cheng PH, Botha AM, Matthews MW (2015) First report of an Anabaena bory strain containing microcystin-LR in a freshwater body in Africa. Afr J Aquat Sci 40:21–36. https://doi.org/10.2989/16085914.2014.993583
Osman OA, Beier S, Grabherr M, Bertilsson S (2017) Interactions of freshwater cyanobacteria with bacterial antagonists. Appl Environ Microbiol 83. https://doi.org/10.1128/AEM.02634-16
Paerl HW, Gardner WS, Havens KE, Joyner AR, McCarthy MJ, Newell SE, Qin B, Scott JT (2016) Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae 54:213–222. https://doi.org/10.1016/j.hal.2015.09.009
Park J, Church J, Son Y, Kim K-T, Lee WH (2017) Recent advances in ultrasonic treatment: challenges and field applications for controlling harmful algal blooms (HABs). Ultrason Sonochem 38:326–334. https://doi.org/10.1016/j.ultsonch.2017.03.003
Patke, Dey (1998) Proteolytic activity from a thermophilic Streptomyces megasporus strain SDP4. Lett Appl Microbiol 26:171–174. https://doi.org/10.1046/j.1472-765X.1998.00300.x
Pei H y, Hu W r, Mu R m, Li X c (2007) Alga-lysing bioreactor and dominant bacteria strain. J Environ Sci. https://doi.org/10.1016/S1001-0742(07)60091-6
Phankhajon K, Somdee A, Somdee T (2016) Algicidal activity of an actinomycete strain, Streptomyces rameus, against Microcystis aeruginosa. Water Sci Technol 74:1398 LP–1391408
Pietikäinen J, Pettersson M, Bååth E (2005) Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol Ecol 52:49–58
Pomeroy LR, Wiebe WJ, Deibel D, Thompson RJ, Rowe GT, Pakulski JD (1991) Bacterial responses to temperature and substrate concentration during the Newfoundland spring bloom. Mar Ecol Prog Ser 75:143–159
Rampelotto PH (2013) Extremophiles and extreme environments. Life Open Access J 3:482–485. https://doi.org/10.3390/life3030482
Rashidan KK, Bird DF (2001) Role of predatory bacteria in the termination of a cyanobacterial bloom. Microb Ecol 41:97–105. https://doi.org/10.1007/s002480000074
Ratkowsky DA, Olley J, McMeekin TA, Ball A (1982) Relationship between temperature and growth rate of bacterial cultures. J Bacteriol 149:1–5
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. https://doi.org/10.1007/s11274-009-0192-2
Schneider OD, Weinrich LA, Brezinski S (2015) Ultrasonic treatment of algae in a New Jersey reservoir. J Am Water Works Assoc 107:E533–E542. https://doi.org/10.5942/jawwa.2015.107.0149
Shao J, Jiang Y, Wang Z, Peng L, Luo S, Gu J, Li R (2014) Interactions between algicidal bacteria and the cyanobacterium Microcystis aeruginosa: lytic characteristics and physiological responses in the cyanobacteria. Int J Environ Sci Technol 11:469–476. https://doi.org/10.1007/s13762-013-0205-4
Shi L, Cai Y, Yang H, Xing P, Li P, Kong L, Kong F (2009) Phylogenetic diversity and specificity of bacteria associated with Microcystis aeruginosa and other cyanobacteria. J Environ Sci 21:1581–1590. https://doi.org/10.1016/S1001-0742(08)62459-6
Shi L, Cai Y, Kong F, Yu Y (2011) Changes in abundance and community structure of bacteria associated with buoyant Microcystis colonies during the decline of cyanobacterial bloom (autumn–winter transition). Ann Limnol Int J Limnol 47:355–362. https://doi.org/10.1051/limn/2011047
Shunyu S, Yongding L, Yinwu S, Genbao L, Dunhai L (2006) Lysis of Aphanizomenon flos-aquae (cyanobacterium) by a bacterium Bacillus cereus. Biol Control 39:345–351. https://doi.org/10.1016/j.biocontrol.2006.06.011
Sigee DC, Glenn R, Andrews MJ, Bellinger EG, Butler RD, Epton HAS, Hendry RD (1999) Biological control of cyanobacteria: principles and possibilities. Hyd 395(396):161–172. https://doi.org/10.1051/animres:19950569
Soini J, Falschlehner C, Mayer C, Böhm D, Weinel S, Panula J, Vasala A, Neubauer P (2005) Transient increase of ATP as a response to temperature up-shift in Escherichia coli. Microb Cell Factories 4:9. https://doi.org/10.1186/1475-2859-4-9
Stroom JM, Kardinaal WEA (2016) How to combat cyanobacterial blooms: strategy toward preventive lake restoration and reactive control measures. Aquat Ecol 50:541–576. https://doi.org/10.1007/s10452-016-9593-0
Su JF, Ma M, Wei L, Ma F, Lu JS, Shao SC (2016a) Algicidal and denitrification characterization of Acinetobacter sp. J25 against Microcystis aeruginosa and microbial community in eutrophic landscape water. Mar Pollut Bull 107:233–239. https://doi.org/10.1016/j.marpolbul.2016.03.066
Su JF, Shao SC, Ma F, Lu JS, Zhang K (2016b) Bacteriological control by Raoultella sp. R11 on growth and toxins production of Microcystis aeruginosa. Chem Eng J 293:139–150. https://doi.org/10.1016/j.cej.2016.02.044
Tian B, Yang J, Zhang KQ (2007) Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiol Ecol 61:197–213. https://doi.org/10.1111/j.1574-6941.2007.00349.x
Tian C, Liu X, Tan J, Lin S, Li D, Yang H (2012) Isolation, identification and characterization of an algicidal bacterium from Lake Taihu and preliminary studies on its algicidal compounds. J Environ Sci 24:1823–1831. https://doi.org/10.1016/S1001-0742(11)60983-2
Touloupakis E, Cicchi B, Benavides AMS, Torzillo G (2016) Effect of high pH on growth of Synechocystis sp. PCC 6803 cultures and their contamination by golden algae (Poterioochromonas sp.). Appl Microbiol Biotechnol 100:1333–1341. https://doi.org/10.1007/s00253-015-7024-0
Vadstein O, Olsen LM, Busch A, Andersen T, Reinertsen HR (2003) Is phosphorus limitation of planktonic heterotrophic bacteria and accumulation of degradable DOC a normal phenomenon in phosphorus-limited systems? A microcosm study. FEMS Microbiol Ecol 46:307–316
Van Wichelen J, Vanormelingen P, Codd GA, Vyverman W (2016) The common bloom-forming cyanobacterium Microcystis is prone to a wide array of microbial antagonists. Harmful Algae 55:97–111. https://doi.org/10.1016/j.hal.2016.02.009
Verschuere L, Rombaut G, Sorgeloos P, Verstraete W (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 64:655–671.
Wang K, Wommack KE, Chen F (2011) Abundance and distribution of Synechococcus spp. and cyanophages in the Chesapeake Bay. Appl Environ Microbiol 77:7459–7468. https://doi.org/10.1128/AEM.00267-11
Welker M, Steinberg C, Jones GJ (2001) Release and persistence of microcystins in natural waters. Cyanotoxins Occur Causes, Consequences 85–103
West M, Louda JW (2011) Effect of external pH on cyanobacterial pigment expression. Florida Sci 74:181–186
White PA, Kalff J, Rasmussen JB, Gasol JM (1991) The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats. Microb Ecol 21:99–118. https://doi.org/10.1007/BF02539147
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. https://doi.org/10.1007/s10750-005-0008-9
Yang L, Maeda H, Yoshikawa T, Zhou G (2012) Algicidal effect of bacterial isolates of Pedobacter sp. against cyanobacterium Microcystis aeruginosa. Water Sci Eng 5:375–382. https://doi.org/10.3882/j.issn.1674-2370.2012.04.002
Yang F, Zhou Y, Yin L, Zhu G, Liang G, Pu Y (2014) Microcystin-degrading activity of an indigenous bacterial strain Stenotrophomonas acidaminiphila MC-LTH2 isolated from Lake Taihu. PLoS One 9:1–7. https://doi.org/10.1371/journal.pone.0086216
Zhang X, Hu H-Y, Hong Y, Yang J (2008) Isolation of a Poterioochromonas capable of feeding on Microcystis aeruginosa and degrading microcystin-LR. FEMS Microbiol Lett 288:241–246. https://doi.org/10.1111/j.1574-6968.2008.01355.x
Zhang H, Yu Z, Huang Q, Xiao X, Wang X, Zhang F, Wang X, Liu Y, Hu C (2011) Isolation, identification and characterization of phytoplankton-lytic bacterium CH-22 against Microcystis aeruginosa. Limnologica 41:70–77. https://doi.org/10.1016/j.limno.2010.08.001
Zhang B-H, Ding Z-G, Li H-Q, Mou X-Z, Zhang Y-Q, Yang J-Y, Zhou E-M, Li W-J (2016) Algicidal activity of Streptomyces eurocidicus JXJ-0089 metabolites and their effects on Microcystis physiology. Appl Environ Microbiol 82:5132–5143. https://doi.org/10.1128/AEM.01198-16
Zhou Q, Chen W, Zhang H, Peng L, Liu L, Han Z, Wan N, Li L, Song L (2012) A flow cytometer based protocol for quantitative analysis of bloom-forming cyanobacteria (Microcystis) in lake sediments. J Environ Sci (China) 24:1709–1716. https://doi.org/10.1016/S1001-0742(11)60993-5
Zhou S, Yin H, Tang S, Peng H, Yin D, Yang Y, Liu Z, Dang Z (2016) Physiological responses of Microcystis aeruginosa against the algicidal bacterium Pseudomonas aeruginosa. Ecotoxicol Environ Saf 127:214–221. https://doi.org/10.1016/j.ecoenv.2016.02.001
Zhu L, Wu Y, Song L, Gan N (2014) Ecological dynamics of toxic Microcystis spp. and microcystin-degrading bacteria in Dianchi Lake, China. Appl Environ Microbiol 80:1874–1881. https://doi.org/10.1128/AEM.02972-13
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical statement
This article does not contain any studies with animals performed by any of the authors.
Rights and permissions
About this article
Cite this article
Ndlela, L.L., Oberholster, P.J., Van Wyk, J.H. et al. Bacteria as biological control agents of freshwater cyanobacteria: is it feasible beyond the laboratory?. Appl Microbiol Biotechnol 102, 9911–9923 (2018). https://doi.org/10.1007/s00253-018-9391-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-018-9391-9