Cite this paper:
LI Chuanbiao, DING Jun, ZHOU Lizhen, ZHANG Zhao, LI Shengkang, LIU Wenhua, WEN Xiaobo. Survey of cyanomyovirus abundance in Shantou coastal waters by g20[J]. Journal of Oceanology and Limnology, 2015, 33(3): 604-615

Survey of cyanomyovirus abundance in Shantou coastal waters by g20

LI Chuanbiao1,2, DING Jun1,2, ZHOU Lizhen1,2, ZHANG Zhao1,2, LI Shengkang1,2, LIU Wenhua1,2, WEN Xiaobo1,2
1 Guangdong Provincial Key Laboratory of Marine Biology, Shantou University, Shantou 515063, China;
2 Marine Biology Institute, Shantou University, Shantou 515063, China
Abstract:
To understand the genetic diversity and population changes in cyanophages in the coastal waters of Shantou, northeast South China Sea, we used the capsid assembly protein gene g20 as a marker of the abundance and phylogeny of natural cyanomyovirus communities. The abundance of total viruses, heterotrophic bacteria, and picophytoplankton in the coastal waters was monitored with flow cytometry. Hydrological parameters (NO3-, NO2-, NH3, soluble reactive phosphorus, total dissolved nitrogen, total dissolved phosphorus, dissolved oxygen, chemical oxygen demand, temperature, salinity, and chlorophyll a concentration) and microbial abundance (total viruses, total bacteria, Prochlorococcus, Synechococcus, and eukaryotes) were measured in the upper and lower layers at four sampling sites in the research area. In the direct viral counts, cyanomyoviruses accounted for 1.92% to >10% of the total viral community. A phylogenetic analysis showed that the g20 sequences in the Shantou coastal waters were very diverse, distributed in eight distinct operational taxonomic units, including the newly formed Cluster W. The g20 gene copies inferred from real time PCR assay indicated that cyanomyoviruses were correlated significantly with the heterotrophic bacteria numbers and the nitrate and chlorophyll a concentrations. These results suggest that cyanomyoviruses are ubiquitous and are an abundant component of the virioplankton in Shantou coastal waters.
Key words:    cyanomyovirus|g20|Shantou|coastal water   
Received: 2014-07-14   Revised: 2014-10-14
Tools
PDF (369 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by LI Chuanbiao
Articles by DING Jun
Articles by ZHOU Lizhen
Articles by ZHANG Zhao
Articles by LI Shengkang
Articles by LIU Wenhua
Articles by WEN Xiaobo
References:
Bergh Ø, BØrsheim K Y, Bratbak G, Heldal M. 1989. High abundance of viruses found in aquatic environments.Nature, 340 (6233): 467-468.
Brussaard C P D, Wilhelm S W, Thingstad F, Weinbauer M G,Bratbak G, Heldal M, Kimmance S A, Middelboe M,Nagasaki K, Paul J H, Schroeder D C, Suttle C A, Vaqué D, Wommack K E. 2008. Global-scale processes with a nanoscale drive: the role of marine viruses. ISME. J., 2 : 575-578.
Brussaard C P D. 2006. Optimization of procedures for counting viruses by flow cytometry. Appl. Environ.Microbiol., 70 (3): 1 506-1 513.
Bidle K D, Haramaty L, Barcelos E R J, Falkowski P. 2007.Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc.Natl. Acad. Sci. USA, 104 (14): 6 049-6 054.Chen F, Lu J R, Binder B J, Liu Y C, Hodson R E. 2001.
Application of digital image analysis and flow cytometry to enumerate marine viruses stained with SYBR gold.Appl. Environ. Microbiol., 67 (2): 539-545.
Chen F, Suttle C A, Short S M. 1996. Genetic diversity in marine algal virus communities as revealed by sequence analysis of DNA polymerase genes. Appl. Environ.Microbiol., 62 (8) : 2 869-2 874.
Choi D H, Hawang C Y, Cho B C. 2003. Comparison of virusand bacterivory-induced bacterial mortality in the eutrophic Masan Bay, Korea. Aquat. Microb. Ecol., 30 : 117-125.
Danovaro R, Corinaldesi C, Dell'anno A, Fuhrman J A,Middelburg J J, Noble R T, Suttle C A. 2011. Marine viruses and global climate change. FEMS Microbiol. Rev., 35 (6): 993-1 034.
Dinsdale E A, Edwards R A, Hall D, Angly F, Breitbart M,Brulc J M, Furlan M, Desnues C, Haynes M, Li L L,McDaniel L, Moran M A, Nelson K E, Nilsson C, Olson
R, Paul J, Brito B R, Ruan Y J, Swan B K, Stevens R,Valentine D L, Thurber R V, Wegley L, White B A,Rohwer F. 2008. Functional metagenomic profiling of nine biomes. Nature, 452 (7187): 629-632.
Dorigo U, Jacquet S, Humbert J F. 2004. Cyanophage diversity, inferred from g20 gene analyses, in the largest natural lake in France, Lake Bourget. Appl. Environ. Microbiol., 70 (2): 1 017-1 022.
Filee J, Tetart F, Suttle C A, Krisch H M. 2005. Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc. Natl. Acad. Sci. USA, 102 (35): 12 471-12 476.
Fuller N J, Wilson W H, Joint I R, Mann N H. 1998. Occurrence of a sequence in marine cyanophages similar to that of T4 g 20 and its application to PCR-based detection and quantification techniques. Appl. Environ. Microbiol., 64 (6): 2 051-2 060.
Jeffrey S W, Humphrey G F. 1975. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem.Physiol. Pflanz., 167 : 191-194.
Jiao N Z, Yang Y H. 2002. Ecological studies on Prochlorococcus in China seas. Chin. Sci. Bull., 47 (15): 1 243-1 250.
Kim J D, Lee C G. 2006. Diversity of heterocystous filamentous cyanobacteria (blue-green algae) from rice paddy fields and their differential susceptibility to ten fungicides used in Korea. J. Microbiol. Biotech., 16(2) : 240-246.
Larsen A, Flaten G A F, Sandaa R A, Castberg T, Thyrhaug R,Erga S R, Jacquet S, Bratbak G. 2004. Spring phytoplankton bloom dynamics in Norwegian coastal waters: microbial community succession and diversity.Limnol. Oceano., 49 (1): 180-190.
Lee S, Fuhrman J A. 1987. Relationships between biovolume and biomass of naturally derived marine bacterioplankton.Appl. Environ. Microbiol., 53(6): 1 298-1 303.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔCT method. Methods, 25 (4): 402-408.
Lu J R, Chen F, Hodson R E. 2001. Distribution, isolation, host specificity, and diversity of cyanophages infecting marine Synechococcus spp. in river estuaries. Appl. Environ.Microbiol., 67 (7): 3 285-3 290.
Mann N H. 2005. The third age of phage. Plos Biol., 3 (5): e182.
Marie D, Partensky F, Jacquet S, Vaulot D. 1997. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl. Environ. Microbiol., 63 (1): 186-193.
Marie D, Brussaard C P D, Thyrhaug R, Bratbak G, Vaulot D. 1999. Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl. Environ.Microbiol., 65 (1): 45-52.
Marston M F, Sallee J L. 2003. Genetic diversity and temporal variation in the cyanophage community infecting marine Synechococcus species in Rhode Island's coastal waters.Appl. Environ. Microbiol., 69 (8): 4 639-4 647.
Matteson A R, Loar S N, Bourbonniere R A, Wilhelm S W. 2011. Molecular enumeration of an ecologically important cyanophage in a Laurentian Great Lake. Appl. Environ.Microbiol., 77 (19): 6 772-6 779.
Matteson A R, Rowe J M, Ponsero A J, Pimentel T M, Boyd P W, Wilhelm S W. 2013. High abundances of cyanomyoviruses in marine ecosystems demonstrate ecological relevance. FEMS Microbiol. Ecol., 84 (2): 223-234.
Murray A G, Jackson G A. 1992. Viral dynamics: a model of the effects of size shape, motion and abundance of singlecelled planktonic organisms and other particles. Mar.Ecol. Prog. Ser., 89 : 103-116. Øvreas L, Bourne D, Sandaa R A, Casamayor E O, Benlloch S,Goddard V, Smerdon G, Heldal M, Thingstad T F. 2003.
Response of bacterial and viral communities to nutrient manipulations in seawater mesocosms. Aquat. Microb.Ecol., 31 : 109-121.
Palenik B. 1994. Cyanobacterial community structure as seen from RNA polymerase gene sequence analysis. Appl.Environ. Microbiol., 60 (9): 3 212-3 219.
Partensky F, Hess W R, Vaulot D. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance.Microbiol. Mol. Biol. Rev., 63 : 106-127.
Rohwer F, Thurber R V. 2009.Viruses manipulate the marine environment. Nature, 459 (7244): 207-212.Safferman R S, Cannon R E, Desjardins P R, Gromov B V,Haselkorn R, Sherman L A, Shilo M. 1983. Classification and nomenclature of viruses of cyanobacteria.Intervirology, 19(2): 61-66.
Sandaa R A, Larsen A. 2006. Seasonal variations in virus-host populations in Norwegian coastal waters: Focusing on the cyanophage community infecting marine Synechococcus spp. Appl. Environ. Microbiol., 72 (7): 4 610-4 618.
Sandaa R A, Clokie M, Mann N H. 2008. Photosynthetic genes in viral populations with a large genomic size range from Norwegian coastal waters. FEMS Microbiol. Ecol., 63 (1): 2-11.
Short C M, Suttle C A. 2005. Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl. Environ.Microbiol., 71(1) : 480-486.
Sullivan M B, Waterbury J B, Chisholm S W. 2003.Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature, 424 (6952): 1 047-1 051.
State Bureau of Quality and Technical Supervision. 2007. The Specification for Oceanographic Survey-Observations of Chemical Parameters in Sea Water. China Standard Press,Beijing, China. (in Chinese)Suttle C A. 2005. Viruses in the sea. Nature, 437 (7057): 356-361.
Suttle C A. 2007. Marine viruses-major players in the global ecosystem. Nat. Rev. Microbiol., 5 (10): 801-812.
Suttle C A, Chan A M, Cottrell M T. 1990. Infection of phytoplankton by viruses and reduction of primary productivity. Nature, 347 (6292): 467-469.
Thingstad T F, Heldal M, Bratbak G, Dundas I. 1993. Are viruses important partners in pelagic feed webs?. Trends Ecol. Evol., 8 (6): 209-213.
Thingstad T F, Lignell R. 1997. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol., 13 : 19-27.
Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acid. Res., 25 (24): 4 876-4 882.
Venter J C, Remington K, Heidelberg J F, Halpern A L, Rusch D, Eisen J A, Wu D Y, Paulsen I, Nelson K E, Nelson W,Fouts D E, Levy S, Knap A H, Lomas M W, Nealson K,White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers Y H, Smith H O. 2004.
Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304 (5667): 66-74.
Waldor M K, Mekalanos J J. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science, 272 (5270): 1 910-1 914.
Wang G H, Asakawa S, Kimura M. 2011. Spatial and temporal changes of cyanophage communities in paddy field soils as revealed by the capsid assembly protein gene g20.FEMS Microbiol. Ecol., 76 (2): 352-359.
Wang K, Chen F. 2004. Genetic diversity and population dynamics of cyanophage communities in the Chesapeake Bay. Aquat. Microb. Ecol., 34 (2) : 105-116.
Wang M, Liang Y T, Bai X G, Jiang X J, Wang F, Qiao Q. 2010. Distribution of microbial populations and their relationship with environmental parameters in the coastal waters of Qingdao, China. Environ. Microbiol., 12 (7): 1 926-1 939.
Waterbury J B, Watson S W, Valois F W, Franks D G. 1986.Biological and ecological characterization of the marine unicellular cyanobacterium Synechococcus. Can. Bull.Fish. Aquat. Sci., 214: 71-120.
Weinbauer M G, Rassoulzadegan F. 2004. Are viruses driving microbial diversification and diversity? Environ.Microbiol., 6 (1): 1-11.
Wichels A, Biel S S, Gelderblom H R, Brinkhoff T, Muyzer G,Schütt C. 1998. Bacteriophage diversity in the North Sea.Appl. Environ. Microbiol., 64 (11): 4 128-4 133.
Wilhelm S W, Carberry M J, Eldridge M L, Poorvin L, Saxton M A, Doblin M A. 2006. Marine and freshwater cyanophages in a Laurentian Great Lake: evidence from infectivity assays and molecular analyses of g20 genes.Appl. Environ. Microbiol., 72(7) : 4 957-4 963.
Wilhelm S W, Jeffrey W H, Dean A L, Meador J, Pakulski J D,Mitchell D L. 2003. UV radiation induced DNA damage in marine viruses along a latitudinal gradient in the southeastern Pacific Ocean. Aquat. Microb. Ecol., 31(4) : 1-8.
Wilhelm S W, Suttle C A. 1999. Viruses and nutrient cycles in the sea-viruses play critical roles in the structure and function of aquatic food webs. Bioscience, 49(10): 781-788.
Wilhelm S W, Weinbauer M G, Suttle C A, Jeffrey W H. 1998.The role of sunlight in the removal and repair of viruses in the sea. Limnol. Oceanogr., 43 (1): 586-592.
Wommack K E, Colwell R R. 2000. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev., 64 (1): 69-114.
Yan Q, Wang M, Bai X, Sun J, Liang Y, Wang F. 2010. New phylogenetically distinct cyanophages found in the coastal Yellow Sea by Qingdao. Acta. Virologica., 54 (4): 255-260.
Zhong Y, Chen F, Wilhelm S W, Poorvin L, Hodson R E. 2002.Phylogenetic diversity of marine cyanophage isolates and natural virus communities as revealed by sequences of viral capsid assembly protein gene g20. Appl. Environ.Microbiol., 68 (4): 1 576-1 584.
Zwirglmaier K, Heywood J L, Chamberlain K, Woodward E M, Zubkov M V, Scanlan D J. 2007. Basin-scale distribution patterns of picocyanobacterial lineages in the Atlantic Ocean. Environ. Microbiol., 9 (5): 1 278-1 290.
Copyright © Haiyang Xuebao