The effect of viral infection on the Black Sea microalgae Tetraselmis viridis: the role of nutrients and copper ions
Liudmila V. Stelmakh
A * , Raisa R. Sagadatova A and Olga S. Alatartseva A
A
Abstract
The TvV-SM2 virus, isolated from the coastal waters of the Black Sea, causes lysis of its host, the algae Tetraselmis viridis (Chlorophyta). Under optimal conditions for nutrients, an increase in the initial abundance of algae cells by four times caused a 3-fold reduction in the latent period of viral infection. During the period of the most rapid cell lysis of T. viridis, nitrogen deficiency leads to a decrease in the average daily rate of death of cells affected by the virus by 3.2 times relative to the replete conditions, while in the case of phosphorus deficiency, this process slows down by up to 2.4 times. Under deplete conditions, the rate of cell death was only 34% lower than under replete conditions. The effect of copper ions (100 μg L−1) on the viral suspension for 6 h led to the complete suppression of its activity. In the presence of the host of this virus, its activity is only partially suppressed. As a result, cell lysis under the influence of a viral infection occurred in two stages. The first stage was noted only during the first 6 h of the experiment. The second main stage took place within 78–170 h. This study showed that in conditions of nutrient deficiency and in the presence of copper ions in seawater, the impact of viruses on microalgae will be weaker.
Keywords: algal viruses, Black Sea, copper ions, microalgae Tetraselmis viridis, nutrients, PAM fluorometry, the scanning electron and light microscopy, viral titer.
References
Arsenieff L, Simon N, Rigaut-Jalabert F, Le Gall F, Chaffron S, Corre E, Com E, Bigeard E, Baudoux A-C (2019) First viruses infecting the marine diatom Guinardia delicatula. Frontiers in Microbiology 9, 3235.
| Crossref | Google Scholar | PubMed |
Baudoux AC, Noordeloos AAM, Veldhuis MJW, Brussaard CPD (2006) Virally induced mortality of Phaeocystis globosa during two spring blooms in temperate coastal waters. Aquatic Microbial Ecology 44, 207-217.
| Crossref | Google Scholar |
Beckett SJ, Weitz JS (2018) The effect of strain level diversity on robust inference of virus-induced mortality of phytoplankton. Frontiers in Microbiology 9, 1850.
| Crossref | Google Scholar | PubMed |
Bettarel Y, Kan J, Wang K, Williamson KE, Cooney S, Ribblett S, Chen F, Wommack KE, Coats DW (2005) Isolation and preliminary characterisation of a small nuclear inclusion virus infecting the diatom Chaetoceros cf. gracilis. Aquatic Microbial Ecology 40, 103-114.
| Crossref | Google Scholar |
Bidle KD, Haramaty L, Barcelos e Ramos J, Falkowski P (2007) Viral activation and recruitment of metacaspases in the unicellular coccolithophore Emiliania huxleyi. Proceedings of the National Academy of Sciences 104, 6049.
| Crossref | Google Scholar | PubMed |
Bratbak G (1993) Microscope methods for measuring bacterial biovolume: epifluorescence microscopy, scanning electron microscopy, and transmission electron microscopy. In ‘Handbook of methods in aquatic microbial ecology’. (Eds PF Kemp, BF Sherr, EB Sherr, JJ Cole) pp. 309–316. (CRC Press: Boca Raton, FL, USA)
Bratbak G, Egge JK, Heldal M (1993) Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Marine Ecology Progress Series 93, 39-48.
| Crossref | Google Scholar |
Clasen JL, Elser JJ (1995) The effect of host Chlorella NC64A carbon: phosphorus ratio on the production of Paramecium bursaria Chlorella Virus-1. Freshwater Biology 52, 112-122.
| Crossref | Google Scholar |
Clasen JL, Brigden SM, Payet JP, Suttle CA (2008) Evidence that viral abundance across oceans and lakes is driven by different biological factors. Freshwater Biology 53, 1090-1100.
| Crossref | Google Scholar |
Clerissi C, Grimsley N, Subirana L, Maria E, Oriol L, Ogata H, Moreau H, Desdevises Y (2014) Prasinovirus distribution in the Northwest Mediterranean Sea is affected by the environment and particularly by phosphate availability. Virology 466–467, 146-157.
| Crossref | Google Scholar | PubMed |
Cottrell MT, Suttle CA (1995) Dynamics of lytic virus infecting the photosynthetic marine picoflagellate Micromonas pusilla. Limnology and Oceanography 40, 730-739.
| Crossref | Google Scholar |
Evans C, Brussaard CPD (2012) Regional variation in lytic and lysogenic viral infection in the Southern Ocean and its contribution to biogeochemical cycling. Applied and Environmental Microbiology 78, 6741-6748.
| Crossref | Google Scholar | PubMed |
Evans C, Archer SD, Jacquet S, Wilson WH (2003) Direct estimates of the contribution of viral lysis and microzooplankton grazing to the decline of a Micromonas spp. population. Aquatic Microbial Ecology 30, 207-219.
| Crossref | Google Scholar |
Finenko ZZ, Stelmakh LV, Galatonova OA, Babich II, Harchuk IA (2008) Cultivation of algae in the laboratory. In ‘The Black Sea microalgae: problems of biodiversity preservation and biotechnological usage’. (Eds YuN Tokarev, ZZ Finenko, NV Shadrin) pp. 186–200. (ECOSI-Gidrofizika: Sevastopol, Russia). [In Russian]
Garza DR, Suttle CA (1998) The effect of cyanophages on the mortality of Synechococcus spp. and selection for UV resistant viral communities. Microbial Ecology 36, 281-292.
| Crossref | Google Scholar | PubMed |
Häder D-P, Gao K (2015) Interactions of anthropogenic stress factors on marine phytoplankton. Frontiers in Environmental Science 3, 14.
| Crossref | Google Scholar |
Jacquet S, Heldal M, Iglesias-Rodriguez D, Larsen A, Wilson W, Bratbak G (2002) Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection. Aquatic Microbial Ecology 27, 111-124.
| Crossref | Google Scholar |
Jacquet S, Miki T, Noble R, Peduzzi P, Wilhelm S (2010) Viruses in aquatic ecosystems: important advancements of the last 20 years and prospects for the future in the field of microbial oceanography and limnology. Advances in Oceanography and Limnology 1, 97-141.
| Crossref | Google Scholar |
Jarvis B, Wilrich C, Wilrich P-T (2010) Reconsideration of the derivation of Most Probable Numbers, their standard deviations, confidence bounds and rarity values. Journal of Applied Microbiology 109, 1660-1667.
| Crossref | Google Scholar | PubMed |
Jover LF, Effler TC, Buchan A, Wilhelm SW, Weitz JS (2014) The elemental composition of virus particles: implications for marine biogeochemical cycles. Nature Reviews Microbiology 12, 519-528.
| Crossref | Google Scholar | PubMed |
Kimura K, Tomaru Y (2015) Discovery of two novel viruses expands the diversity of single-stranded DNA and single-stranded RNA viruses infecting a cosmopolitan marine diatom. Applied and Environmental Microbiology 81, 1120-1131.
| Crossref | Google Scholar | PubMed |
Korablina IV, Barabashin TO, Gevorkyan JV, Evseeva AI (2001) The dynamics of heavy metals distribution in the water column of the northeastern part of the Black Sea after 2000. Proceedings of VNIRO 183, 96-112 [In Russian].
| Google Scholar |
Lawrence JE, Brussaard CPD, Suttle CA (2006) Virus-specific responses of Heterosigma akashiwo to infection. Applied and Environmental Microbiology 72, 7829-7834.
| Crossref | Google Scholar | PubMed |
Levy JL, Angel BM, Stauber JL, Poon WL, Simpson SL, Cheng SH, Jolley DF (2008) Uptake and internalisation of copper by three marine microalgae: comparison of copper-sensitive and copper-tolerant species. Aquatic Toxicology 89, 82-93.
| Crossref | Google Scholar | PubMed |
Maat DS, Brussaard CPD (2016) Both phosphorus- and nitrogen limitation constrain viral proliferation in marine phytoplankton. Aquatic Microbial Ecology 77, 87-97.
| Crossref | Google Scholar |
Maat DS, Crawfurd KJ, Timmermans KR, Brussaard CPD (2014) Elevated CO2 and phosphate limitation favor Micromonas pusilla through stimulated growth and reduced viral impact. Applied and Environmental Microbiology 80, 3119-3127.
| Crossref | Google Scholar | PubMed |
Malapascua JRF, Jerez CG, Sergejevová M, Figueroa FL, Masojídek J (2014) Photosynthesis monitoring to optimize growth of microalgal mass cultures: application of chlorophyll fluorescence techniques. Aquatic Biology 22, 123-140.
| Crossref | Google Scholar |
Mikaelyan AS, Kubryakov AA, Silkin VA, Pautova LA, Chasovnikov VK (2018) Regional climate and patterns of phytoplankton annual succession in the open waters of the Black Sea. Deep Sea Research Part I: Oceanographic Research Papers 142, 44-57.
| Crossref | Google Scholar |
Mojica KDA, Brussaard CPD (2014) Factors affecting virus dynamics and microbial host-virus interactions in marine environments. FEMS Microbiology Ecology 89, 495-515.
| Crossref | Google Scholar | PubMed |
Mojica KDA, Huisman J, Wilhelm SW, Brussaard CPD (2016) Latitudinal variation in virus-induced mortality of phytoplankton across the North Atlantic Ocean. The ISME Journal 10, 500-513.
| Crossref | Google Scholar | PubMed |
Muradov SV (2014) The heavy metals impact on macrophytes algae of the Avacha Bay. Fundamental research 9, 1998-2002 [In Russian].
| Google Scholar |
Nagasaki K, Yamaguchi M (1998) Effect of temperature on the algicidal activity and the stability of HaV (Heterosigma akashiwo virus). Aquatic Microbial Ecology 15, 211-216.
| Crossref | Google Scholar |
Nagasaki K, Tomaru Y, Tarutani K, Katanozaka N, Yamanaka S, Tanabe H, Yamaguchi M (2003) Growth characteristics and intraspecies host specificity of a large virus infecting the dinoflagellate Heterocapsa circularisquama. Applied and Environmental Microbiology 69, 2580-2586.
| Crossref | Google Scholar | PubMed |
Nagasaki K, Tomaru Y, Katanozaka N, Shirai Y, Nishida K, Itakura S, Yamaguchi M (2004) Isolation and characterization of a novel single-stranded RNA virus infecting the bloom-forming diatom Rhizosolenia setigera. Applied and Environmental Microbiology 70, 704-711.
| Crossref | Google Scholar | PubMed |
Oguz T, Gilbert D (2007) Abrupt transitions of the top-down controlled Black Sea pelagic ecosystem during 1960-2000: evidence for regime-shifts under strong fishery exploitation and nutrient enrichment modulated by climate-induced variations. Deep Sea Research Part I: Oceanographic Research Papers 54, 220-242.
| Crossref | Google Scholar |
Orekhova NA, Varenik AV (2018) Current hydrochemical regime of the Sevastopol Bay. Physical Oceanography 25, 124-135.
| Crossref | Google Scholar |
Pagarete A, Grébert T, Stepanova O, Sandaa R-A, Bratbak G (2015) Tsv-N1: a novel DNA algal virus that infects Tetraselmis striata. Viruses 7, 3937-3953.
| Crossref | Google Scholar | PubMed |
Pasulka AL, Samo TJ, Landry ML (2015) Grazer and viral impacts on microbial growth and mortality in the southern California Current Ecosystem. Journal of Plankton Research 37, 320-336.
| Crossref | Google Scholar |
Pemmada R, Zhu X, Dash M, Zhou Y, Ramakrishna S, Peng X, Thomas V, Jain S, Nanda HS (2020) Science-based strategies of antiviral coatings with viricidal properties for the COVID-19 like pandemics. Materials 13, 4041.
| Crossref | Google Scholar | PubMed |
Poggio C, Colombo M, Arciola CR, Greggi T, Scribante A, Dagna AJM (2020) Copper-alloy surfaces and cleaning regimens against the spread of SARS-CoV-2 in dentistry and orthopedics. From fomites to anti-infective nanocoatings. Materials 13, 3244.
| Crossref | Google Scholar | PubMed |
Proctor LM, Okubo A, Fuhrman JA (1993) Calibrating estimates of phage-induced mortality in marine bacteria: ultrastructural studies of marine bacteriophage development from one-step growth experiments. Microbial Ecology 25, 161-182.
| Crossref | Google Scholar | PubMed |
Rowe JM, Saxton MA, Cottrell MT, DeBruyn JM, Berg GM, Kirchman DL, Hutchins DA, Wilhelm SW (2008) Constraints on viral production in the Sargasso Sea and North Atlantic. Aquatic Microbial Ecology 52, 233-244.
| Crossref | Google Scholar |
Schmoker C, Hernández-León S, Calbet A (2013) Microzooplankton grazing in the oceans: impacts, data variability, knowledge gaps and future directions. Journal of Plankton Research 35, 691-706.
| Crossref | Google Scholar |
Slagter HA, Gerringa LJA, Brussaard CPD (2016) Phytoplankton virus production negatively affected by iron limitation. Frontiers in Environmental Science 3, 156.
| Crossref | Google Scholar |
Stelmakh LV, Stepanova OA (2020) Effect of viral infection on the functioning and lysis of Black Sea microalgae Tetraselmis viridis (Chlorophyta) and Phaeodactylum tricornutum (Bacillariophyta). Inland Water Biology 13, 417-424.
| Crossref | Google Scholar |
Suttle CA (2007) Marine viruses: major players in the global ecosystem. Nature Reviews Microbiology 5, 801-812.
| Crossref | Google Scholar | PubMed |
Thurman RB, Gerba CP, Bitton G (1989) The molecular mechanisms of copper and silver ion disinfection of bacteria and viruses. Critical Reviews in Environmental Control 18, 295-315.
| Crossref | Google Scholar |
Tomaru Y, Tarutani K, Yamaguchi M, Nagasaki K (2004) Quantitative and qualitative impacts of viral infection on a Heterosigma akashiwo (Raphidophyceae) bloom in Hiroshima Bay, Japan. Aquatic Microbial Ecology 34, 227-238.
| Crossref | Google Scholar |
Waters RE, Chan AT (1982) Micromonas pusilla virus: the virus growth cycle and associated physiological events within the host cells; host range mutation. Journal of General Virology 63, 199-206.
| Crossref | Google Scholar |
Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiology Reviews 28, 127-181.
| Crossref | Google Scholar | PubMed |
Wilhelm SW, Matteson AR (2008) Freshwater and marine virioplankton: a brief overview of commonalities and differences. Freshwater Biology 53, 1076-1089.
| Crossref | Google Scholar |
Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiology and Molecular Biology Reviews 64, 69-114.
| Crossref | Google Scholar | PubMed |
Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiology 117, 129-139.
| Crossref | Google Scholar | PubMed |
Yunev O, Carstensen J, Stelmakh L, Belokopytov V, Suslin V (2022) Temporal changes of phytoplankton biomass in the western Black Sea shelf waters: evaluation by satellite data (1998–2018). Estuarine, Coastal and Shelf Science 271, 107865.
| Crossref | Google Scholar |
