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Cyanophages Infection of Microcystis Bloom in Lowland Dam Reservoir of Sulejów, Poland

  • Microbiology of Aquatic Systems
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Abstract

An increased incidence of cyanobacterial blooms, which are largely composed of toxigenic cyanobacteria from the Microcystis genus, leads to a disruption of aquatic ecosystems worldwide. Therefore, a better understanding of the impact of environmental parameters on the development and collapse of blooms is important. The objectives of the present study were as follows: (1) to investigate the presence and identity of Microcystis-specific cyanophages capable of cyanobacterial cell lysis in a lowland dam reservoir in Central Europe; (2) to investigate Microcystis sensitivity to phage infections with regard to toxic genotypes; and (3) to identify key abiotic parameters influencing phage infections during the summer seasons between 2009 and 2013. Sequencing analysis of selected g91 gene amplification products confirmed that the identified cyanophages belonged to the family Myoviridae (95 % homology). Cyanophages and Microcystis hosts, including toxic genotypes, were positively correlated in 4 of the 5 years analyzed (r = 0.67–0.82). The average percentage of infected Microcystis cells varied between 0.1 and 32 %, and no particular sensitivity of the phages to toxigenic genotypes was recorded. The highest number of cyanophages (>104 gene copy number per microliter) was observed in the period preceded by the following: an increase of the water retention time, growth of the water temperature, optimum nutrient concentrations, and the predomination of Microcystis bloom.

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References

  1. Welker M, Brunke M, Preussel K, Lippert I, von Döhren H (2004) Diversity and distribution of Microcystis (cyanobacteria) oligopeptide chemotypes from natural communities studies by single-colony mass spectrometry. Microbiology 150:1785–1796. doi:10.1099/mic.0.26947-0

    Article  CAS  PubMed  Google Scholar 

  2. Šejnohová L, Maršálek B (2012) Microcystis. In: Whitton BA (ed) Ecology of cyanobacteria ii: their diversity in space and time. Springer Verlag GmbH, Heidelberg, pp 195–227

    Chapter  Google Scholar 

  3. Paerl HW, Paul VJ (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Res 46:1349–1363. doi:10.1016/j.watres.2011.08.002

    Article  CAS  PubMed  Google Scholar 

  4. Meissner S, Steinhauser D, Dittmann E (2015) Metabolomic analysis indicates a pivotal role of the hepatotoxin microcystin in high light adaptation of Microcystis. Environ Microbiol 17:1497–1509. doi:10.1111/1462-2920.12565

    Article  CAS  PubMed  Google Scholar 

  5. Merel S, Walker D, Chicana R, Snyder S, Baurès E, Thomas O (2013) State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int 59:303–327. doi:10.1016/j.envint.2013.06.013

    Article  CAS  PubMed  Google Scholar 

  6. Srivastava A, Ahn C, Asthana RK, Lee HG, Oh HM (2015) Status, alert system, and prediction of cyanobacterial bloom in South Korea. Biomed Res Int 2015:8. doi:10.1155/2015/584696

    Google Scholar 

  7. 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. doi:10.1023/A:1017097502124

    Article  Google Scholar 

  8. Wu L, Wu H, Chen L, Xie S, Zang H, Borriss R, Gao X (2014) Bacilysin from Bacillus amyloliquefaciens FZB42 has specific bactericidal activity against harmful algal bloom species. Environ Microbiol 80(24):7512–7520. doi:10.1128/AEM.02605-14

    Article  CAS  Google Scholar 

  9. Gerphagnon M, MacArthur DJ, Latour D, Gachon CM, Van Ogtrop F, Gleason FH, Sime-Ngando T (2015) Microbial players involved in the decline of filamentous and colonial cyanobacterial blooms with a focus on fungal parasitism. Environ Microbiol 17(8):2573–2587. doi:10.1111/1462-2920.12860

    Article  PubMed  Google Scholar 

  10. Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010. doi:10.1007/s00248-012-0159-y

    Article  CAS  PubMed  Google Scholar 

  11. Tucker S, Pollard P (2005) Identification of cyanophage Ma-LBP and infection of the cyanobacterium Microcystis aeruginosa from an Australian subtropical lake by the virus. Appl Environ Microbiol 71:629–635. doi:10.1128/AEM.71.2.629-635.2005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Yoshida M, Yoshida T, Kashima A, Takashima Y, Hosoda N, Nagasaki K, Hiroishi S, Prefectural F (2008) Ecological dynamics of the toxic bloom-forming Microcystis aeruginosa and its cyanophages in freshwater. Appl Environ Microbiol 74:3269–3273. doi:10.1128/AEM.02240-07

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Kimura S, Yoshida T, Hosoda N, Honda T, Kuno S, Kamiji R, Hashimoto R, Sako Y (2012) Diurnal infection patterns and impact of Microcystis cyanophages in a Japanese pond. Appl Environ Microbiol 78:5805–5811. doi:10.1128/AEM.00571-12

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Matteson AR, Loar SN, Bourbonniere RA, Wilhelm SW (2011) Molecular enumeration of an ecologically important cyanophage in a Laurentian Great Lake. Appl Environ Microbiol 77(19):6772–6779. doi:10.1128/AEM.05879-11

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Zhong X, Ram AS, Colombet J, Jacquet S (2014) Variations in abundance, genome size, morphology, and functional role of the virioplankton in lakes Annecy and Bourget over a 1-Year Period. Microb Ecol 67:66–82. doi:10.1007/s00248-013-0320-2

    Article  CAS  PubMed  Google Scholar 

  16. Jassim S, Limoges RG (2013) Impact of external forces on cyanophage-host interactions in aquatic ecosystems. World J Microbiol Biotechnol 29:1751–1762. doi:10.1007/s11274-013-1358-5

    Article  PubMed  Google Scholar 

  17. Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF (1999) Evolutionary relationship among bacteriophages and prophages: all the worlds a phage. Proc Natl Acad Sci U S A 95(5):2192–2197. doi:10.1073/pnas.96.5.2192

    Article  Google Scholar 

  18. Yoshida T, Nagasaki K, Takashima Y, Shirai Y, Tomaru Y, Takao Y, Sakamoto S, Hiroishi S, Ogata H (2008) Ma-LMM01 infecting toxic Microcystis aeruginosa illuminates diverse cyanophage genome strategies. J Bacteriol 190:1762–1772. doi:10.1128/JB.01534-07

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Yoshida M, Yoshida T, Yoshida-Takashima Y, Kashima A, Hiroishi S (2010) Real-time PCR detection of host-mediated cyanophage gene transcripts during infection of a natural Microcystis aeruginosa population. Microbes Environ 25:211–215. doi:10.1264/jsme2.ME10117

    Article  PubMed  Google Scholar 

  20. Xia H, Li T, Deng F, Hu Z (2013) Freshwater cyanophages. Virol Sin 28:253–259. doi:10.1007/s12250-013-3370-1

    Article  CAS  PubMed  Google Scholar 

  21. Moisa I, Sotropa E, Velehorschi V (1981) Investigations on the presence of cyanophages in fresh and sea waters of Romania. Virol 32:127–132

    CAS  Google Scholar 

  22. Suttle CA, Chan AM (1993) Marine cyanophages infecting oceanic and coastal strains of Synechococcus: abundance, morphology, cross-infectivity and growth characteristics. Mar Ecol Prog Ser 92:99–109. doi:10.3354/meps092099

    Article  Google Scholar 

  23. Wilson WH, Joint IR, Carr NG, Mann NH (1993) Isolation and molecular characterization of five marine cyanophages propagated on Synechococcus sp. strain WH7803. Appl Environ Microbiol 59:3736–43. doi: 0099-2240/93/113736-08$02.00/0

  24. Lu J, Chen F, Hodson RE (2001) Distribution, isolation, host specificity, and diversity of cyanophages infecting marine Synechococcus spp. in river estuaries. Appl Environ Microbiol 67(7):3285–3290. doi:10.1128/AEM.67.7.3285-3290.2001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Wang K, Chen F (2008) Prevalence of highly host-specific cyanophages in the estuarine environment. Environ Microbiol 10(2):300–312. doi:10.1111/j.1462-2920.2007.01452.x

    Article  CAS  PubMed  Google Scholar 

  26. Takashima Y, Yoshida T, Yoshida M, Shirai Y, Tomaru Y, Takao Y, Hiroishi S, Nagasaki K (2007) Development and application of quantitative detection of cyanophages phylogenetically related to cyanophage Ma-LMM01 infecting Microcystis aeruginosa in freshwater. Microbes Environ 22:207–213. doi:10.1264/jsme2.22.207

    Article  Google Scholar 

  27. Ou T, Li S, Liao X, Zhang Q (2013) Cultivation and characterization of the MaMV-DC cyanophage that infects bloom-forming cyanobacterium Microcystis aeruginosa. Virol Sin 28:266–271. doi:10.1007/s12250-013-3340-7

    Article  CAS  PubMed  Google Scholar 

  28. Li S, Ou T, Zhang Q (2013) Two virus-like particles that cause lytic infections in freshwater cyanobacteria. Virol Sin 28:303–305. doi:10.1007/s12250-013-3339-0

    Article  PubMed  Google Scholar 

  29. Watkins SC, Smith JR, Hayes PK, Watts JEM (2014) Characterisation of host growth after infection with a broad-range freshwater cyanopodophage. PLoS One 9:1–8. doi:10.1371/journal.pone.0087339

    Article  Google Scholar 

  30. Liu X, Shi M, Kong S, Gao Y, An C (2007) Cyanophage Pf-WMP4, a T7-like phage infecting the freshwater cyanobacterium Phormidium foveolarum: complete genome sequence and DNA translocation. Virology 366:28–39. doi:10.1016/j.virol.2007.04.019

    Article  CAS  PubMed  Google Scholar 

  31. Chenard C, Chan AM, Vincent WF, Suttle CA (2015) Polar freshwater cyanophage S-EIV1 represents a new widespread evolutionary lineage of phages. ISME J 9(9):2046–2058. doi:10.1038/ismej.2015.24

    Article  CAS  PubMed  Google Scholar 

  32. Sulcius S, Simoliunas E, Staniulis J, Koreiviene J, Baltrusis P, Meskys R, Paskauskas R (2015) Characterization of a lytic cyanophage that infects the bloom-forming cyanobacterium Aphanizomenon flos-aquae. FEMS Microbiol Ecol 91(2):1–7. doi:10.1093/femsec/fiu012

    PubMed  Google Scholar 

  33. 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. doi:10.1128/AEM.03751-12

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Nakamura G, Kimura S, Sako Y, Yoshida T (2014) Genetic diversity of Microcystis cyanophages in two different freshwater environments. Arch Microbiol 196:401–409. doi:10.1007/s00203-014-0980-4

    Article  CAS  PubMed  Google Scholar 

  35. Kimura-Sakai S, Sako Y, Yoshida T (2015) Development of a real-time PCR assay for the quantification of Ma-LMM01-type Microcystis cyanophages in a natural pond. Lett Appl Microbiol 60:400–408. doi:10.1111/lam.12387

    Article  CAS  PubMed  Google Scholar 

  36. Gągała I, Izydorczyk K, Jurczak T, Mankiewicz-Boczek J (2012) The key parameters and early warning methods to identify presence of toxigenic blooms dominated by Microcystis aeruginosa in the Jeziorsko reservoir (Central Poland). Fresenius Environ Bull 21:295–303

    Google Scholar 

  37. HACH (1991) Water analysis handbook. Method no. 10071 Hach Company, 1309

  38. Golterman H, Clymo R, Ohstand M (1978) Methods for physical and chemical analysis of freshwater. Blackwell Scientific Publication, Oxford, 213p

    Google Scholar 

  39. Mankiewicz-Boczek J, Izydorczyk K, Romanowska-Duda Z, Jurczak T, Stefaniak K, Kokociński M (2006) Detection and monitoring toxigenicity of cyanobacteria by application of molecular methods. Environ Toxicol 21:380–387. doi:10.1002/tox

    Article  CAS  PubMed  Google Scholar 

  40. Giovannoni SJ, DeLong EF, Schmidt TM, Pace NR (1990) Tangential flow filtration and preliminary phylogenetic analysis of marine picoplankton. Appl Environ Microbiol 56:2572–75. doi: 0099-2240/90/082572-04$02.00/0

  41. Ha JH, Hidaka T, Tsuno H (2009) Quantification of toxic Microcystis and evaluation of its dominance ratio in blooms using real-time PCR. Environ Sci Technol 43:812–818. doi:10.1021/es801265f

    Article  CAS  PubMed  Google Scholar 

  42. Neilan BA, Jacobs D, Del Dot T, Blackall LL, Hawkins PR, Cox PT, Goodman AE (1997) rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. Int J Syst Bacteriol 47:693–7. doi: 0020-7713/97/$04.00 + 0

  43. Gągała I, Izydorczyk K, Jurczak T, Pawełczyk J, Dziadek J, Wojtal-Frankiewicz A, Jóźwik A, Jaskulska A, Mankiewicz-Boczek J (2014) Role of environmental factors and toxic genotypes in the regulation of microcystins-producing cyanobacterial blooms. Microb Ecol 67(2):465–479. doi:10.1007/s00248-013-0303-3

    Article  PubMed  Google Scholar 

  44. Yoshida T, Takashima Y, Tomaru Y, Shirai Y, Takao Y, Hiroishi S, Nagasaki K (2006) Isolation and characterization of a cyanophage infecting the toxic cyanobacterium Microcystis aeruginosa. Appl Environ Microbiol 72:1239–1247. doi:10.1128/AEM.72.2.1239

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Boutte C, Mankiewicz-Boczek J, Komarkova J, Grubisic S, Izydorczyk K, Wautelet F, Jurczak T, Zalewski M, Wilmotte A (2008) Diversity of planktonic cyanobacteria and microcystin occurrence in Polish water bodies investigated using a polyphasic approach. Aquat Microb Ecol 51(3):223–236. doi:10.3354/ame01194

    Article  Google Scholar 

  46. Gągała I, Izydorczyk K, Skowron A, Kamecka-Plaskota D, Stefaniak K, Kokociński M, Mankiewicz-Boczek J (2010) Appearance of toxigenic cyanobacteria in two Polish lakes dominated by Microcystis aeruginosa and Planktothrix agardhii and environmental factors influence. Ecohydrol Hydrobiol 10(1):25–34. doi:10.2478/v10104-009-0045-5

    Article  Google Scholar 

  47. Zalewski M, Naiman RJ (1985) The regulation of riverine fish communities by a continuum of abiotic-biotic factors. Habitat Modif Freshw Fish. pp. 3–9. In: Alabaster JS (ed.), Habitat Modification and Freshwater Fisheries: Proceedings of a Symposium of the European Inland Fisheries Advisory Commission Butterworths, London

  48. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1-2):203–214. doi:10.1089/10665270050081478

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was funded by the National Science Centre (PL), project no. UMO-2013/11/N/NZ8/00607 “Ecological dynamics of cyanophages and their host in Polish water bodies” and partially by no. UMO-2012/07/N/NZ8/00599 “Assessment of the interaction between hepatotoxic cyanobacterium Microcystis aeruginosa and pathogenic bacteria of the genus Aeromonas.” The authors would like to acknowledge the European Cooperation in Science and Technology, COST Action ES 1105 “CYANOCOST - Cyanobacterial blooms and toxins in water resources: Occurrence, impacts and management” for adding value to this study through networking and knowledge sharing with European experts and researchers in the field”. The Sulejów Reservoir is a part of the Polish National Long-Term Ecosystem Research Network and the European LTER site.

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Correspondence to J. Mankiewicz-Boczek.

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Supplementary material 1

Detection of cyanobacteria from the genus Microcystis (fragment of 16S rRNA gene), its toxic genotypes (fragment of mcyA gene) and cyanophages specific for Microcystis (fragment of g91 gene) in samples taken from Sulejów Reservoir, station Tresta, in following seasons 2009-2013. M – DNA marker; C – negative control – MiliQ water

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Mankiewicz-Boczek, J., Jaskulska, A., Pawełczyk, J. et al. Cyanophages Infection of Microcystis Bloom in Lowland Dam Reservoir of Sulejów, Poland. Microb Ecol 71, 315–325 (2016). https://doi.org/10.1007/s00248-015-0677-5

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