Absence of evidence for viral infection in colony-embedded cyanobacterial isolates from the Curonian Lagoon

• Autorzy: Sulcius S. , Staniulis J. , Paskauskas R. , Olenina I. , Salyte A. , Ivanauskaite A. , Griniene E.

Identyfikatory

DOI

10.5697/oc.56-3.651

• Języki publikacji: EN

Abstrakty

EN

The aim of the present study was to assess the frequency of viral infections in colony-embedded cells of the cyanobacteria Aphanizomenon flos-aquae and Microcystis aeruginosa collected from the brackish Curonian Lagoon. Natural and mitomycin C-treated A. flos-aquae and M. aeruginosa samples were examined for the presence of viruses and lysis by a combination of light-, epifluorescence and transmission electron microscopy techniques. Here we report a lack of evidence for virus infection, progeny formation and cell lysis in colony-embedded cells of A. flos-aquae and M. aeruginosa. These results indicated that viruses contribute little to the mortality of these cyanobacteria when the latter occur in colonies. Consequently, the results supported the hypothesis that colony formation can, at least temporarily, provide an efficient strategy for protection against virus-induced mortality. Finally, assuming that grazing has a negligible effect on colony-embedded cells in the Curonian Lagoon, we propose that most of the cyanobacterial biomass produced is lost from the pelagic food web by sedimentation.

Słowa kluczowe

EN

aphanizomenon flos-aquae; bloom dynamics; colony formation; defence strategy; lysis; lysogeny; Microcystis aeruginosa; virus infection; virus-host interactions; virus production

• Wydawca: Polish Academy of Sciences, Institute of Oceanology ; Elsevier
• Czasopismo: Oceanologia
• Rocznik: 2014
• Tom: No. 56 (3)
• Strony: 651--660
• Opis fizyczny: Bibliogr. 45 poz., wykr.

Twórcy

autor

Sulcius S.

• Klaipeda University, Marine Science and Technology Centre, H. Manto 84, LT-92294 Klaipeda, Lithuania
• Klaipeda University, Faculty of Natural Sciences and Mathematics, Biology Department, H. Manto 84, LT-92294 Klaipeda, Lithuania

autor

Staniulis J.

• Nature Research Centre, Institute of Botany, Žaliuju ežeru 49, LT-2021 Vilnius, Lithuania

autor

Paskauskas R.

• Klaipeda University, Marine Science and Technology Centre, H. Manto 84, LT-92294 Klaipeda, Lithuania
• Nature Research Centre, Institute of Botany, Žaliuju ežeru 49, LT-2021 Vilnius, Lithuania

autor

Olenina I.

• Klaipeda University, Marine Science and Technology Centre, H. Manto 84, LT-92294 Klaipeda, Lithuania
• Environmental Protection Agency, Marine Research Department, Taikos 26, LT-91149 Klaipeda, Lithuania

autor

Salyte A.

• Klaipeda University, Faculty of Natural Sciences and Mathematics, Biology Department, H. Manto 84, LT-92294 Klaipeda, Lithuania

autor

Ivanauskaite A.

• Klaipeda University, Faculty of Natural Sciences and Mathematics, Biology Department, H. Manto 84, LT-92294 Klaipeda, Lithuania

autor

Griniene E.

• Klaipeda University, Marine Science and Technology Centre, H. Manto 84, LT-92294 Klaipeda, Lithuania

Bibliografia

• [1]. Baudoux A. C., Brussaard C. P. D., 2005, Characterization of different viruses infecting the marine harmful algal bloom species Phaeocystis globosa, Virology, 341 (1), 80-90, http://dx.doi.org/10.1016/j.virol.2005.07.002
• [2]. Baudoux A. C., Noordeloos A. A. M., Veldhuis M. J. W., Brussaard C. P. D., 2006, Virally induced mortality of Phaeocystis globosa during two spring blooms in temperate coastal waters, Aquat. Microb. Ecol., 44 (3), 207-217, http://dx.doi.org/10.3354/ame044207
• [3]. Brussaard C. P. D., Bratbak G., Baudoux A. C., Ruardij P., 2007, Phaeocystis and its interaction with viruses, Biogeochemistry, 83 (1-3), 201-215, http://dx.doi.org/10.1007/s10533-007-9096-0
• [4]. Brussaard C. P. D., Kuipers B., Veldhuis M. J. W., 2005, A mesocosm study of Phaeocystis globosa population dynamics I. Regulatory role of viruses in bloom control, Harmful Algae, 4 (5), 859-874, http://dx.doi.org/10.1016/j.hal.2004.12.015
• [5]. Callieri C., 2010, Single cells and microcolonies of freshwater picocyanobacteria?: a common ecology, J. Limnol., 69 (2), 257-277, http://dx.doi.org/10.4081/jlimnol.2010.257
• [6]. Cao H., Shimura Y., Masanobu K., Yin Y., 2014, Draft genome sequence of the toxic bloom-forming cyanobacterium Aphanizomenon flos-aquae NIES-81, Genome Announcements, 2 (1), e00044-14, http://dx.doi.org/10.1128/genomeA.00044-14
• [7]. Cochran P.K., Paul J.H., 1998, Seasonal abundance of lysogenic bacteria in a subtropical estuary, Appl. Environ. Microb., 64 (6), 2308-2312.
• [8]. Coulombe A.M., Robinson G.G.C., 1981, Collapsing Aphanizomenon flosaquae blooms: possible contributions of photo-oxidation, O2 toxicity, and cyanophages, Can. J. Bot., 59 (7), 1277-1284.
• [9]. Deng L., Hayes P. K., 2008, Evidence for cyanophages active against bloomforming freshwater cyanobacteria, Freshwater Biol., 53 (6), 1240-1252, http://dx.doi.org/10.1111/j.1365-2427.2007.01947.x
• [10]. Dillon A., Parry J.D., 2008, Characterization of temperate cyanophages active against freshwater phycocyanin-rich Synechococcus species, Freshwater Biol., 53 (6), 1253-1261.
• [11]. Gasiūnaitė Z.R., Cardoso A.C., Heiskanen A. S., Henriksen P., Kauppila P., Olenina I., Pilkaitytė R., Purina I., Razinkovas A., Sagert S., Schubert H., Wasmund N., 2005, Seasonality of coastal phytoplankton in the Baltic Sea: Influence of salinity and eutrophication, Estuar. Coast. Shelf Sci., 65 (1-2), 239-252, http://dx.doi.org/10.1016/j.ecss.2005.05.018
• [12]. Gasiūnaitė Z.R., Olenina I., 1998, Zooplankton-phytoplankton interactions: a possible explanation of the seasonal succession in the Kuršiu Marios Lagoon, Hydrobiologia, 363 (1-3), 333-339.
• [13]. Granhall U., 1972, Aphanizomenon flos-aquae: Infection by cyanophages, Physiol. Plantarum, 26 (3), 332-337.
• [14]. Glauert A.M., Lewis P.R., 1998, Biological specimen preparation for transmission electron microscopy, [in:] Practical methods in electron microscopy, A.M. Glauert (ed.), Princeton Univ., Princeton, 175-223.
• [15]. Hamm C. E., Simson D.A., Merkel R., Smetacek V., 1999, Colonies of Phaeocystis globosa are protected by a thin but tough skin, Mar. Ecol.-Prog. Ser., 187, 101-111, http://dx.doi.org/10.3354/meps187101
• [16]. Hewson I., Govil S. R., Capone D.G., Carpenter E. J., Fuhrman J.A., 2004, Evidence of Trichodesmium viral lysis and potential significance for biogeochemical cycling in the oligotrophic ocean, Aquat. Microb. Ecol., 36 (1), 1-8, http://dx.doi.org/10.3354/ame036001
• [17]. Hughes K.A., Sutherland I.W., Jones M.V., 1998, Biofilm susceptibility to bacteriophage attack: the role of phage-borne polysaccharide depolymerase, Microbiology, 144 (11), 3039-3047.
• [18]. Jacobsen A., Bratbak G., Heldal M., 1996, Isolation and characterization of a virus infecting Phaeocystis pouchetii (Prymnesiophyceae), J. Phycol., 32 (6), 923-927.
• [19]. Jacobsen A., Larsen A., Martínez-Martínez J., Verity P.G., Frischer Mė., 2007, Susceptibility of colonies and colonial cells of Phaeocystis pouchetii (Haptophyta) to viral infection, Aquat. Microb. Ecol., 48 (2), 105-112, http://dx.doi.org/10.3354/ame048105
• [20]. Jassim S.A.A., Limoges R.G., 2013, Impact of external forces on cyanophage-host interactions in aquatic ecosystems, World J. Microb. Biot., 29 (10), 1751-1762, http://dx.doi.org/10.1007/s11274-013-1358-5
• [21]. Jüurgens K., Güude H., 1994, The potential importance of grazing-resistant bacteria in planktonic systems, Mar. Ecol.-Prog. Ser., 112 (1), 169-188.
• [22]. 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. Microb., 78 (16), 5805-5811, http://dx.doi.org/10.1128/AEM.00571-12
• [23]. Luft J.H., 1961, Improvements in epoxy resin embedding methods, J. Bioph. Biochem. Cytol., 9 (2), 409-414.
• [24]. Lüurling M., Van Donk E., 2000, Grazer-induced colony formation in Scenedesmus: are there costs to being colonial?, Oikos, 88 (1), 111-118.
• [25]. Łotocka M., 2001, Toxic effect of cyanobacterial blooms on the grazing activity of Daphnia magna Straus, Oceanologia, 43 (4), 441-453.
• [26]. Martínez J. L., Rojo F., 2011, Metabolic regulation of antibiotic resistance, FEMS Microbiol. Rev., 35 (5), 768-789, http://dx.doi.org/10.1111/j.1574-6976.2011.00282.x
• [27]. McDaniel L., Houchin L.A., Williamson S. J., Paul J.H., 2002, Lysogeny in marine Synechococcus, Nature, 415 (6871), 496, http://dx.doi.org/10.1038/415496a
• [28]. Patel A., Noble R.T., Steele J.A., Schwalbach M. S., Hewson I., Fuhrman J.A., 2007, Virus and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I, Nat. Protocols, 2 (2), 269-276, http://dx.doi.org/10.1038/nprot.2007.6
• [29]. Paul J.H., Weinbauer M.G., 2010, Detection of lysogeny in marine environments, 30-33, [in:] Manual of aquatic viral ecology, S.W. Wilhelm, M. G. Weinbauer, & C.A. Suttle (eds.), ASLO.
• [30]. Pilkaitytė R., Razinkovas A., 2006, Factors controlling phytoplankton blooms in a temperate estuary: Nutrient limitation and physical forcing, Hydrobiologia, 555 (1), 41-48, http://dx.doi.org/10.1007/s10750-005-1104-6
• [31]. Pollard P.C., Young L.M., 2010, Lake viruses lyse cyanobacteria, Cylindrospermopsis raciborskii, enhances filamentous-host dispersal in Australia, Acta Oecol., 36 (1), 114-119, http://dx.doi.org/10.1016/j.actao.2009.10.007
• [32]. Ruardij P., Veldhuis M. J., Brussaard C.P., 2005, Modeling the bloom dynamics of the polymorphic phytoplankter Phaeocystis globosa: impact of grazers and viruses, Harmful Algae, 4 (5), 941-963.
• [33]. Sato T., 1968, A modified method for lead staining of thin sections, J. Electron Microsc., 17 (2), 158-159.
• [34]. Sellner K.G., Olson M.M., Kononen K., 1994, Copepod grazing in a summer cyanobacteria bloom in the Gulf of Finland, Hydrobiologia, 292/293 (1), 249-254, http://dx.doi.org/10.1007/BF00229948
• [35]. Sulcius S., Staniulis J., Paüukauskas R., 2011, Morphology and distribution of phage-like particles in a eutrophic boreal lagoon, Oceanologia, 53 (2), 587-603, http://dx.doi.org/10.5697/oc.53-2.587
• [36]. Šimek K., Weinbauer M.G., Hornk K., Jezbera J., Nedoma J., Dolan J. R., 2007, Grazer and virus-induced mortality of bacterioplankton accelerates development of Flectobacillus populations in a freshwater community, Environ. Microbiol., 9 (3), 789-800, http://dx.doi.org/10.1111/j.1462-2920.2006.01201.x
• [37]. Tang K. W., 2001, Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal, J. Plankton Res., 25 (7), 831-842.
• [38]. Waterbury J. B., Valois F. W., 1993, Resistance to co-occurring phages enables marine Synechococcus communities to coexist with cyanophages abundant in seawater, Appl. Environ. Microb., 59 (10), 3393-3399.
• [39]. Weinbauer M. G., Suttle C. A., 1999, Lysogeny and prophage induction in coastal and offshore bacterial communities, Aquat. Microb. Ecol., 18 (3), 217-225.
• [40]. Yamamoto Y., Shiah F. K., Chen Y. L., 2011, Importance of large colony formation in bloom-forming cyanobacteria to dominate in eutrophic ponds, Int. J. Limnol., 47 (2), 167-173, http://dx.doi.org/10.1051/limn/2011013
• [41]. Yang Z., Kong F., 2012, Formation of large colonies: a defense mechanism of Microcystis aeruginosa under continuous grazing pressure by flagellate Ochromonas sp., J. Limnol., 71 (1), 61-66.
• [42]. Yoshida T., Nagasaki K., Takashima Y., Shirai Y., Tomaru Y., Takao Y., Sakamoto S., Hiroishi S., Ogata H., 2008a, Ma-LMM01 infecting toxic Microcystis aeruginosa illuminates diverse cyanophage genome strategies, J. Bacteriol., 190 (5), 1762-1772, http://dx.doi.org/10.1128/JB.01534-07
• [43]. Yoshida T., Takashima Y., Tomaru Y., Takao Y., Hiroishi S., Shirai Y., Nagasaki K., 2006, Isolation and characterization of a cyanophage infecting the toxic cyanobacterium Microcystis aeruginosa, Appl. Environ. Microb., 72 (2), 1239-1247.
• [44]. Yoshida M., Yoshida T., Kashima A., Takashima Y., Hosoda N., Nagasaki K., Hiroishi S., 2008b, Ecological dynamics of the toxic bloom-forming cyanobacterium Microcystis aeruginosa and its cyanophages in freshwater, Appl. Environ. Microb., 74 (10), 3269-73, http://dx.doi.org/10.1128/AEM.02240-07
• [45]. Zilius M., Bartoli M., Daunys D., Pilkaityte R., Razinkovas A., 2012, Patterns of benthic oxygen uptake in a hypertrophic lagoon: spatial variability and controlling factors, Hydrobiologia, 699 (1), 85-98, http://dx.doi.org/10.1007/s10750-012-1155-4