Novel marine diatom ssRNA virus NitRevRNAV infecting Nitzschia reversa
Cover of volume 152, number 2 of Plant Ecology and Evolution
PDF

Keywords

marine virus
algal virus
new species
Nitzschia
Bacillariophyta
diatom

How to Cite

Toyoda, K., Kimura, K., Osada, K., Williams, D., Adachi, T., Yamada, K. and Tomaru, Y. (2019) “Novel marine diatom ssRNA virus NitRevRNAV infecting Nitzschia reversa”, Plant Ecology and Evolution, 152(2), pp. 178-187. doi: 10.5091/plecevo.2019.1615.

Abstract

Background and aims – Diatoms are one of the most species rich groups of organisms on Earth. They are fundamental in supporting the biomass of the natural environment. The presence of marine viruses can greatly influence diatom diversity in their natural environment and has attracted interest from multi-disciplinary research teams after a diatom infected virus was reported for the first time in the 21st century. As initial research in this field demonstrated, for the acquisition of a new virus it is important to learn about their infect hosts. Therefore, we have been searching for new viruses that infect diatoms.

Methods – A clonal host species Nitzschia reversa was isolated from natural sea water. Aliquots of the filtrates obtained from this sea water were inoculated to yield the exponentially-growing isolated host species. The resultant lysate was used as a clonal lysate and treated as a clonal virus suspension. The suspension was then used for further analysis of various biochemical studies.

Key results – We discovered and isolated a new virus that infected the pennate diatom Nitzschia reversa. Since this newly discovered virus was a single strand RNA virus, it has capsid proteins with 30 nm size icosahedron without an envelope. The species epithet is NitRevRNAV.

Conclusions – In this study, we described the morphology, genome type and partial sequences, as well as lytic activities, of the new species NitRevRNAV. Of note, the virus harbours a positive-sense single-stranded RNA genome. These features were highly similar to those of previously known diatom RNA viruses therefore NitRevRNAV is a new member of the genus Bacillarnavirus in the Order Picornavirales.

https://doi.org/10.5091/plecevo.2019.1615
PDF

References

Allen L.S., McCrow J.P., Ininbergs K., Dupont C.L., Badger J.H., Hoffman J.M., Ekman M., Allen A.E., Bergman B., Venter J.C. (2017) The Baltic Sea Virome: Diversity and Transcriptional Activity of DNA and RNA Viruses. mSystems 2: e00125-16. https://doi.org/10.1128/mSystems.00125-16

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. https://doi.org/10.3389/fmicb.2018.03235

Bergh Ø., Børsheim K.Y., Bratbak G., Heldal M. (1989) High abundance of viruses found in aquatic environments. Nature 340: 467–468. https://doi.org/10.1038/340467a0

Brum J.R., Sullivan M.B. (2015) Rising to the challenge: Accelerated pace of discovery transforms marine virology. Nature Reviews Microbiology, 13: 147–159. https://doi.org/10.1038/nrmicro3404

Carpenter S., Brock W., Hanson P. (1999) Ecological and social dynamics in simple models of ecosystem management. Conservation Ecology 3: 4. https://doi.org/10.5751/ES-00122-030204

Culley A.I., Lang A.S., Suttle C.A. (2003) High diversity of unknown picorna-like viruses in the sea. Nature 424: 1054–1057. https://doi.org/10.1038/nature01886

Guillard R.R.L. (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith W.L., Chanley M.H (eds) Culture of marine invertebrate animals: 26–60. New York, USA, Plenum Press.

Guillard R.R.L., Ryther J.H. (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Canadian Journal of Microbiology 8: 229–239. https://doi.org/10.1139/m62-029

Imai I., Itakura S., Matsuyama Y., Yamaguchi M. (1996) Selenium requirement for growth of a novel red tide flagellate Chattonella verruculosa (Raphidophyceae) in culture. Fisheries Science 62: 834–835. https://doi.org/10.2331/fishsci.62.834

John D.M., Maggs C.M. (1997) Species problem in eukaryotic algae: a modern perspective. In: Claridge M.F., Dawah H.A., Wilson,M.R. (eds) Species, the units of diversity: 83–107. London, Chapman & Hall.

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. https://doi.org/10.1128/AEM.02380-14

Kumar, S., Stecher, G., Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874. https://doi.org/10.1093/molbev/msw054

Kooistra W.H.C.F., Gersonde R., Medlin L.K., Mann D.G. (2007) The origin and evolution of the diatoms: their adaptation to a planktonic existence. In: Falkowski P.G., Knoll A.H. (eds) Evolution of primary producers in the sea: 207–249. Burlington, Elsevier Academic Press.

Mann D.G (1999) The species concept in diatoms. Phycologia 38: 437–495. https://doi.org/10.2216/i0031-8884-38-6-437.1

Mackinder L.C.M., Worthy C.A., Biggi G., Hall M., Ryan K.P., Varsani A., Harper G.M., Wilson W.H., Brownlee C., Schroeder D.C. (2009) A unicellular algal virus , Emiliania huxleyi virus 86, exploits an animal-like infection strategy. Journal of General Virology 90: 2306–2316. https://doi.org/10.1099/vir.0.011635-0

Matsuda Y., Hopkinson B.M., Nakajima K., Dupont C.L., Tsuji Y. (2017) Mechanisms of carbon dioxide acquisition and CO2 sensing in marine diatoms: a gateway to carbon metabolism. Philosophical Transactions of the Royal Society 372: 20160403. https://doi.org/10.1098/rstb.2016.0403

Moniruzzaman M., Wurch L.L., Alexander H., Dyhrman S.T., Gobler C.J., Wilhelm S.W. (2017) Virus-host relationships of marine single-celled eukaryotes resolved from metatranscriptomics. Nature Communications 8: 1–10. https://doi.org/10.1038/ncomms16054

Nagasaki K., Bratbak G. (2010) Isolation of viruses infecting photosynthetic and nonphotosynthetic protists. In: Wilhelm S.W., Weinbauer M.G., Suttle C.A. (eds) Manual of aquatic viral ecology: 92–101. Waco, American Society of Limnology and Oceanography.

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: 704–11. https://doi.org/10.1128/AEM.70.2.704-711.2004

Nagasaki K., Shirai Y., Tomaru Y., Nishida K., Pietrokovski S. (2005) Algal viruses with distinct intraspecies host specificities include identical intein elements. Genetics and Molecular Biology 71: 3599–3607. https://doi.org/10.1128/AEM.71.7.3599-3607.2005

Nelson D.M., Treguer P., Brzezinski M.A., Leynaert A., Queguiner B. (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochemistry Cycle 9: 359–372. https://doi.org/10.1029/95GB01070

Norton T.A., Melkonian M., Andersen R.A., (1996) Algal biodiversity. Phycologia 35: 308–326. https://doi.org/10.2216/i0031-8884-35-4-308.1

Provasoil L., Shiraishi K., Lance J.R. (1959) Nutritional idiosyncrasies of Artemia and Tigriopus in monoxenic culture. Annals of the New York Academy of Sciences 77: 250–261. https://doi.org/10.1111/j.1749-6632.1959.tb36905.x

Shirai Y., Tomaru Y., Takao Y., Suzuki H., Nagumo T., Nagasaki K. (2008) Isolation and characterization of a single-stranded RNA virus infecting the marine planktonic diatom Chaetoceros tenuissimus Meunier. Applied and Environmental Microbiology 74: 4022–4027. https://doi.org/10.1128/AEM.00509-08

Sarthoua G., Timmermansb K.R., Blaina S., Tréguer P. (2005) Growth physiology and fate of diatoms in the ocean: a review. Journal of Sea Research 53: 25–42. https://doi.org/10.1016/j.seares.2004.01.007

Suttle C.A. (1993) Enumeration and isolation of viruses. In: Kemp P.F., Sherr E.A., Cole J.J. (eds) Handbook of methods in aquatic microbial ecology: 121–137. Boca Raton, Lewis Publishers.

Suttle C.A. (2007) Marine viruses – major players in the global ecosystem. Nature Review Microbiology 5: 801–812. https://doi.org/10.1038/nrmicro1750

Thompson J.D., Higgins D.G., Gibson T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680. https://doi.org/10.1007/978-1-4020-6754-9_3188

Tomaru Y., Tarutani K., Yamaguchi M., Nagasaki K. (2004) Quantitative and qualitative impacts of viral infection on Heterosigma akashiwo (Raphidophyceae) population during a bloom in Hiroshima Bay, Japan. Aquatic Microbial Ecology 34: 227–238. https://doi.org/10.3354/ame035227

Tomaru Y., Hata N., Masuda T., Tsuji M., Igata K., Masuda Y., Yamatogi T., Sakaguchi M., Nagasaki K. (2007) Ecological dynamics of the bibalve-killing dinoflagellate Heterocapsa circularisquama and its infectious viruses in different locations of western Japan. Environment Microbiology 9: 1376–1383. https://doi.org/10.1111/j.1462-2920.2007.01252.x

Tomaru Y., Takao Y., Suzuki H., Nagumo T., Nagasaki K. (2009) Isolation and characterization of a single-stranded RNA virus infecting the bloom forming diatom Chaetoceros socialis. Applied and Environmental Microbiology 75: 2375–2381. https://doi.org/10.1128/AEM.02580-08

Tomaru Y., Fujii N., Oda S., Toyoda K., Nagasaki K. (2011) Dynamics of diatom viruses on the western coast of Japan. Aquatic Microbial Ecology 63: 223–230. https://doi.org/10.3354/ame01496

Tomaru Y., Nagasaki K. (2011) Diatom viruses. In: Seckbach J., Kociolek J.P. (eds) The diatom world. Cellular origin, life in extreme habitats and astrobiology book 19: 211–225. London, Springer.

Tomaru Y., Toyoda K., Kimura K., Hata N., Yoshida M., Nagasaki K. (2012) First evidence for the existence of pennate diatom viruses. ISME Journal 6: 1445–1448. https://doi.org/10.1038/ismej.2011.207

Tomaru Y., Toyoda K., Kimura K., Takao Y., Sakurada K., Nakayama N., Nagasaki K. (2013) Isolation and characterization of a single-stranded RNA virus that infects the marine planktonic diatom Chaetoceros sp. (SS08-C03). Phycological Research 61: 27–36. https://doi.org/10.1111/j.1440-1835.2012.00670.x

Tomaru Y., Toyoda K., Kimura K. (2015) Marine diatom viruses and their hosts: Resistance mechanisms and population dynamics. Perspectives in Phycology 2: 69–81. https://doi.org/10.1127/pip/2015/0023

Toyoda K., Kimura K., Hata N., Nakayama N., Nagasaki K., Tomaru Y. (2012) Isolation and characterization of a single-stranded DNA virus infecting the marine planktonic diatom Chaetoceros sp. (strain TG07-C28). Plankton & Benthos Research 7: 20–28. https://doi.org/10.3800/pbr.7.20

Tréguer P., Bowler C., Moriceau B., Dutkiewicz S., Gehlen M., Aumont O., Bittner L., Dugdale R., Finkel Z., Iudicone D., Jahn O., Guidi L., Lasbleiz M., Leblanc K., Levy M., Pondaven P. (2017) Influence of diatom diversity on the ocean biological carbon pump. Nature Geoscience 11: 27–37. https://doi.org/10.1038/s41561-017-0028-x

Urayama S., Takaki Y., Nishi S., Yoshida‐Takashima Y., Deguchi S., Takai K., Nunoura T. (2018) Unveiling the RNA virosphere associated with marine microorganisms. Molecular Ecology Resources 18: 1444–1455. https://doi.org/10.1111/1755-0998.12936

Yau S., Lauro F.M., DeMaere M.Z., Brown M.V., Thomas T., Raftery M.J., Andrews-Pfannkoch C., Lewis M., Hoffman J.M., Gibson J.A., Cavicchioli R. (2011) Virophage control of antarctic algal host-virus dynamics. Proceedings of the National Academy of Sciences of the United States of America 108: 6163–6168. https://doi.org/10.1073/pnas.1018221108

Yolken R.H., Jones-Brando L., Dunigan D.D., Kannan G., Dickerson F., Severance E., Sabunciyan S., Talbot Jr. C.C., Prandovszky E., Gurnon J.R., Agarkova I.V., Leister F., Gressitt K.L., Chen O., Deuber B., Ma F., Pletnikov M.V., Van Etten J.L. (2014) Chlorovirus ATCV-1 is part of the human oropharyngeal virome and is associated with changes in cognitive functions in humans and mice. Proceedings of the National Academy of Sciences of the United States of America 111: 16106–16111. https://doi.org/10.1073/pnas.1418895111

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.