AIMS Microbiology, 2018, 4(2): 304-318. doi: 10.3934/microbiol.2018.2.304.

Research article

Export file:


  • RIS(for EndNote,Reference Manager,ProCite)
  • BibTex
  • Text


  • Citation Only
  • Citation and Abstract

Low temperatures can promote cyanobacterial bloom formation by providing refuge from microbial antagonists

Norwegian University of Life Sciences, Faculty for Environmental Sciences and Natural Resource Management, Postbox 5003, NO-1432 Ås, Norway

Freshwater cyanobacteria are prone to a wide range of highly potent microbial antagonists. Most of these exploit their prey in a frequency-dependent manner and are therefore particularly well suited to prevent any accumulation of cyanobacteria. Mass developments of cyanobacteria, the so-called blooms, should therefore be rare events, which is in striking contrast to what we actually see in nature. Laboratory experiments of the present study showed that the temperature range 5.8–10 °C forms a thermal refuge, inside which the cyanobacterium Planktothrix can grow without being exploited by two otherwise highly potent microbial antagonists. In nature, access of Planktothrix to this refuge was associated with positive net growth and a high probability of bloom formation, confirming that refuge temperatures indeed allow Planktothrix to grow with a minimum of biomass loss caused by microbial antagonists. Contact to higher temperatures, in contrast, was associated with decreases in net growth rate and in probability of bloom formation, with population collapses and with the occurrence of parasite infection. This is in agreement with the finding of laboratory experiments that above 10 °C exploitation of Planktothrix by multiple microbes increases in a temperature-dependent manner. Taken together, above findings suggest that temperature modulates the microbial control of natural Planktothrix populations. Low temperatures form a thermal refuge that may promote Planktothrix bloom formation by shielding the cyanobacterium from otherwise highly potent microbial antagonists.
  Article Metrics

Keywords cyanobacteria; bloom formation; thermal refuge; Rhizophydium; Nassula

Citation: Thomas Rohrlack. Low temperatures can promote cyanobacterial bloom formation by providing refuge from microbial antagonists. AIMS Microbiology, 2018, 4(2): 304-318. doi: 10.3934/microbiol.2018.2.304


  • 1. Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microbial Ecol 65: 995–1010.    
  • 2. Ibelings BW, Fastner J, Bormans M, et al. (2016) Cyanobacterial blooms. Ecology, prevention, mitigation and control: Editorial to a CYANOCOST Special Issue. Aquat Ecol 50: 327–331.
  • 3. Van Wichelen J, Vanormelingen P, Codd GA, et al. (2016) The common bloom-forming cyanobacterium Microcystis is prone to a wide array of microbial antagonists. Harmful Algae 55: 97–111.    
  • 4. Gerphagnon M, Macarthur DJ, Latour D, et al. (2015) Microbial players involved in the decline of filamentous and colonial cyanobacterial blooms with a focus on fungal parasitism. Environ Microbiol 17: 2573–2587.    
  • 5. Thingstad TF, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13: 19–27.    
  • 6. Kuno S, Yoshida T, Kaneko T, et al. (2012) Intricate Interactions between the bloom-forming cyanobacterium Microcystis aeruginosa and foreign genetic elements, revealed by diversified clustered regularly interspaced short palindromic repeat (CRISPR) signatures. Appl Environ Microbiol 78: 5353–5360.    
  • 7. Rohrlack T, Christiansen G, Kurmayer R (2013) Putative antiparasite defensive system involving ribosomal and nonribosomal oligopeptides in cyanobacteria of the Genus Planktothrix. Appl Environ Microbiol 79: 2642–2647.    
  • 8. Pajdak-Stos A, Fialkowska E, Fyda J (2001) Phormidium autumnale (Cyanobacteria) defense against three ciliate grazer species. Aquat Microb Ecol 23: 237–244.    
  • 9. Agha R, Lezcano MA, Labrador MDM, et al. (2014) Seasonal dynamics and sedimentation patterns of Microcystis oligopeptide-based chemotypes reveal subpopulations with different ecological traits. Limnol Oceanogr 59: 861–871.    
  • 10. Sønstebø JH, Rohrlack T (2011) Possible implications of chytrid parasitism for population subdivision in freshwater cyanobacteria of the genus Planktothrix. Appl Environ Microbiol 77: 1344–1351.    
  • 11. Jenkins CA, Hayes PK (2006) Diversity of cyanophages infecting the heterocystous filamentous cyanobacterium Nodularia isolated from the brackish Baltic Sea. J Mar Biol Assoc UK 86: 529–536.    
  • 12. Kimura S, Sako Y, Yoshida T (2013) Rapid Microcystis cyanophage gene diversification revealed by long- and short-term genetic analyses of the tail sheath gene in a natural pond. Appl Environ Microbiol 79: 2789–2795.    
  • 13. Brockhurst MA, Chapman T, King KC, et al. (2014) Running with the Red Queen: the role of biotic conflicts in evolution. P Roy Soc B-Biol Sci 281: 9.
  • 14. Scholthof KBG (2007) The disease triangle: pathogens, the environment and society. Nat Rev Microbiol 5: 152–156.    
  • 15. Chiaramonte LV, Ray RA, Corum RA, et al. (2016) Klamath River thermal refuge provides juvenile salmon reduced exposure to the parasite Ceratonova shasta. T Am Fish Soc 145: 810–820.    
  • 16. Tobler M, Schlupp I, de Leon FJG, et al. (2007) Extreme habitats as refuge from parasite infections? Evidence from an extremophile fish. Acta Oecol 31: 270–275.
  • 17. Strom SL, Harvey EL, Fredrickson KA, et al. (2013) Broad salinity tolerance as a refuge from predation in the harmful raphidophyte alga Heterosigma akashiwo (Raphidophyceae). J Phycol 49: 20–31.    
  • 18. Bruning K (1991) Infection of the diatom Asterionella by a chytrid. II. Effects of light on survival and epidemic development of the parasite. J Plankton Res 13: 119–129.
  • 19. Bruning K (1991) Effect of phosphorus limitation on the epidemiology of a chytrid phytoplankton parasite. Freshwater Biol 25: 409–417.    
  • 20. Gsell AS, Domis LND, van Donk E, et al. (2013) Temperature alters host genotype-specific susceptibility to chytrid infection. PLoS One 8: 10.
  • 21. Bruning K (1991) Effects of temperature and light on the population-dynamics of the Asterionella-Rhizophydium association. J Plankton Res 13: 707–719.    
  • 22. Ibelings BW, Gsell AS, Mooij WM, et al. (2011) Chytrid infections and diatom spring blooms: paradoxical effects of climate warming on fungal epidemics in lakes. Freshwater Biol 56: 754–766.    
  • 23. Mankiewicz-Boczek J, Jaskulska A, Paweczyk J, et al. (2016) Cyanophages infection of Microcystis bloom in lowland dam reservoir of Sulejw, Poland. Microbial Ecol 71: 315–325.    
  • 24. Gerphagnon M, Colombet J, Latour D, et al. (2017) Spatial and temporal changes of parasitic chytrids of cyanobacteria. Sci Rep UK 7.
  • 25. Gleason FH, Lilje O (2009) Structure and function of fungal zoospores: ecological implications. Fungal Ecol 2: 53–59.    
  • 26. Lindstedt KJ (1971) Chemical control of feeding behavior. Comp Biochem Phys A 39: 553–581.    
  • 27. Berge DM, Løvik JE, Brettum P (1985) Tyrifjordenundersøkelsen 1978–1981, Datarapport. NIVA Rep 1777: 249.
  • 28. Halstvedt CB, Rohrlack T, Andersen T, et al. (2007) Seasonal dynamics and depth distribution of Planktothrix spp. in Lake Steinsfjorden (Norway) related to environmental factors. J Plankton Res 29: 471–482.
  • 29. Beard SJ, Davis PA, Iglesias-Rodriguez D, et al. (2000) Gas Vesicle genes in Planktothrix spp. from Nordic lakes: strains with weak gas vesicles possess a longer variant of gvpC. Microbiology 146: 2009–2018.
  • 30. Perga ME, Domaizon I, Guillard J, et al. (2013) Are cyanobacterial blooms trophic dead ends? Oecologia 172: 551–562.    
  • 31. Kurmayer R, Juttner F (1999) Strategies for the co-existence of zooplankton with the toxic cyanobacterium Planktothrix rubescens in Lake Zurich. J Plankton Res 21: 659–683.    
  • 32. Gliwicz ZM (1990) Why do cladocerans fail to control algal blooms? Hydrobiologia 200: 83–97.
  • 33. Kyle M (2015) Learning from the past; using lake sediments as chemical and biological archives. Norwegian University of Life Sciences.
  • 34. Canter HM, Heaney SI, Lund JWG (1990) The ecological significance of grazing on plnaktonic populations od cyanobacteria by the ciliate Nassula. New Phytol 114: 247–263.    
  • 35. Davis PA, Dent M, Parker J, et al. (2003) The annual cycle of growth rate and biomass change in Planktothrix spp. in Blelham Tarn, English Lake District. Freshwater Biol 48: 852–867.
  • 36. Brabrand A, Faafeng BA, Kallqvist T, et al. (1983) Biological control of undesirable cyanobacteria in culturally eutrohpic lakes. Oecologia 60: 1–5.    
  • 37. Hausmann K, Ruskens A (1984) Studies on the digestion in the ciliate Nassula aurea Ehrenberg. Arch Protistenkd 128: 77–87.    
  • 38. Rohrlack T, Edvardsen B, Skulberg R, et al. (2008) Oligopeptide chemotypes of the toxic freshwater cyanobacterium Planktothrix can form subpopulations with dissimilar ecological traits. Limnol Oceanogr 53: 1279–1293.    
  • 39. Rounge TB, Rohrlack T, Decenciere B, et al. (2010) Subpopulation differentiation associated with nonribosomal peptide synthese gene cluster dynamics in the cyanobacterium Planktothrix spp. J Phycol 46: 645–652.    
  • 40. Rounge TB, Rohrlack T, Nederbragt AJ, et al. (2009) A genome-wide analysis of nonribosomal peptide synthetase gene clusters and their peptides in a Planktothrix rubescens strain. BMC Genomics 10: 396.    
  • 41. Tooming-Klunderud A, Sogge H, Rounge TB, et al. (2013) From green to red: Horizontal gene transfer of the phycoerythrin gene cluster between Planktothrix strains. Appl Environ Microbiol 79: 6803–6812.    
  • 42. Gerphagnon M, Latour D, Colombet J, et al. (2013) Fungal parasitism: life cycle, dynamics and impact on cyanobacterial blooms. PLoS One 8: 10.
  • 43. Edvardsen B (2002) Overvåking av toksinproduserende cyanobakterier i Steinsfjorden 2001. Sammenfattende resultater fra 1997–2001. NIVA Rep 4509: 40.
  • 44. Su JF, Ma M, Wei L, et al. (2016) Algicidal and denitrification characterization of Acinetobacter sp J25 against Microcystis aeruginosa and microbial community in eutrophic landscape water. Mar Pollut Bull 107: 233–239.    
  • 45. Liu YM, Wang MH, Jia RB, et al. (2012) Removal of cyanobacteria by an Aeromonas sp. Desalin Water Treat 47: 205–210.    
  • 46. Kim BR, Nakano S, Kim BH, et al. (2006) Grazing and growth of the heterotrophic flagellate Diphylleia rotans on the cyanobacterium Microcystis aeruginosa. Aquat Microb Ecol 45: 163–170.    
  • 47. Zhang L, Gu L, Wei Q, et al. (2017) High temperature favors elimination of toxin-producing Microcystis and degradation of microcystins by mixotrophic Ochromonas. Chemosphere 172: 96–102.    
  • 48. Chu TC, Murray SR, Hsu SF, et al. (2011) Temperature-induced activation of freshwater Cyanophage AS-1 prophage. Acta Histochem 113: 294–299.    
  • 49. Bruning K (1991) Infection of the diatom Asterionella by a chytrid. I. Effects of light on reproduction and infectivity of the parasite. J Plankton Res 13: 103–117.
  • 50. Visser PM, Verspagen JMH, Sandrini G, et al. (2016) How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae 54: 145–159.    
  • 51. Rohrlack T, Haande S, Molversmyr A, et al. (2015) Environmental conditions determine the course and outcome of phytoplankton chytridiomycosis. PLoS One 10: 17.


This article has been cited by

  • 1. M.Á. Lezcano, R. Agha, S. Cirés, A. Quesada, Spatial-temporal survey of Microcystis oligopeptide chemotypes in reservoirs with dissimilar waterbody features and their relation to genetic variation, Harmful Algae, 2019, 81, 77, 10.1016/j.hal.2018.11.009

Reader Comments

your name: *   your email: *  

© 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (

Download full text in PDF

Export Citation

Copyright © AIMS Press All Rights Reserved