Sandaa, Ruth-Anne, Clokie, Martha R. J. and Mann, Nicholas H.. (2008) Photosynthetic genes in viral populations with a large genomic size range from Norwegian coastal waters. FEMS Microbiology Ecology, Vol.63 (No.1). pp. 2-11. ISSN 0168-6496

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Abstract

This study reports the diversity of uncultured environmental viruses harbouring photosynthetic genes (psbA and psbD) in samples from cold seawater (latitude above 60 degrees). The viral community in coastal Norwegian waters was separated according to genome size using pulse field gel electrophoresis. Viral populations within a wide genome size range (31-380 kb) were investigated for the presence of the psbA and psbD genes using PCR, combined with cloning and sequencing. The results show the presence of photosynthetic genes in viral populations from all size ranges. Thus, valuable information could be obtained about the size class to which viral particles that encode photosynthesis genes belong. The wide genomic size range detected implies that a different cyanophage profile has been observed than has been reported previously. Thus, the method of phage gene detection applied here may represent a truer picture of phage diversity in general or that there is a larger range of size profile for viruses with psbA and psbD in higher latitudes than for the better-studied lower latitudes. Alternatively, a picture of diversity based on a different set of biases than that from either isolation-based research or from conventional metagenomic approaches may be observed.

Item Type:	Journal Article
Subjects:	Q Science > QP Physiology Q Science > QR Microbiology
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH):	Cyanobacteria -- Norway, Gene mapping, Photosynthesis -- Genetic aspects, Viral genomes, Pulsed-field gel electrophoresis
Journal or Publication Title:	FEMS Microbiology Ecology
Publisher:	Wiley-Blackwell Publishing Ltd.
ISSN:	0168-6496
Date:	January 2008
Volume:	Vol.63
Number:	No.1
Number of Pages:	10
Page Range:	pp. 2-11
Identification Number:	DOI:10.1111/j.1574-6941.2007.00400.x
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
Funder:	Norges forskningsråd [Research Council of Norway], European Union (EU)
Grant number:	EVK3-CT-2002-00078 (EU)
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Larsen A, Castberg T, Sandaa RA, Brussaard CPD, Egge J, Heldal M, Paulino A, Thyrhaug R, van Hannen EJ & Bratbak G (2001) Population dynamics and diversity of phytoplankton, bacteria and viruses in a seawater enclosure. Mar Ecol Prog Ser 221: 47–57. Larsen A, Flaten GAF, Sandaa RA, Castberg T, Thyrhaug R, Erga SR, Jacquet S & Bratbak G (2004) Spring phytoplankton bloom dynamics in Norwegian coastal waters: microbial community succession and diversity. Limnol Oceanogr 49: 180–190. Li WKW (1995) Composition of ultraphytoplankton in the central North-Atlantic. Mar Ecol Prog Ser 122: 1–8. Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F & Chisholm SW (2004) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad SciUSA 101: 11013–11018. Lindell D, Jaffe JD, Johnson ZI, Church GM & Chisholm SW (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438: 86. Liu HB, Nolla HA & Campbell L (1997) Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Microb Ecol 12: 39–47. Mann NH (2003) Phages of the marine cyanobacterial picophytoplankton. FEMS Microbiol Rev 27: 17–34. Mann NH, Clokie MRJ, Millard A, Cook A, Wilson WH, Wheatley PJ, Letarov A & Krisch HM (2005) The genome of S-PM2, a ‘photosynthetic’ T4-type bacteriophage that infects marine Synechococcus strains. J Bacteriol 187: 3188–3200. Millard A, Clokie MRJ, Shub DA & Mann NH (2004) Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci USA 101: 11007–11012. Olson RJ, Chisholm SW, Zettler ER, Altabet MA & Dusenberry JA (1990) Spatial and temporal distributions of prochlorophyte picoplankton in the North Atlantic Ocean. Deep-Sea Res Part A-Oceanogr Res Papers 37: 1033. Ovreas L, Bourne D, Sandaa RA, Casamayor EO, Benlloch S, Goddard V, Smerdon G, Heldal M & Thingstad TF (2003) Response of bacterial and viral communities to nutrient manipulations in seawater mesocosms. Aquat Microb Ecol 31: 109–121. Partensky F, Hess WR & Vaulot D (1999) Prochlorococcus a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106–127. Proctor LM & Fuhrman JA (1990) Viral mortality of marinebacteria and cyanobacteria. Nature 343: 60–62. Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, La Scola B, Suzan M & Claverie J (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306: 1344–1350. Rapp´e M & Giovannoni S (2003) The uncultured microbial majority. Annu Rev Microbiol 57: 369–394. Riemann L & Middelboe M (2002) Stability of bacterial and viral community compositions in Danish coastal waters as depicted by DNA fingerprinting techniques. Aquat Microb Ecol 27: 219–232. Sandaa RA & Larsen A (2006) Seasonal variations in viral-host populations in Norwegian coastal waters: focusing on the Ackermann H-W & DuBow MS (1987) Viruses of Prokaryotes. CRC Press Inc, Boca Raton, FL. Altschul S, Gish W, Miller W, Myers E & Lipman D (1990) Basic local alignment search tool. J Mol Biol 215: 403–410. Angly FE, Felts B, BreitbartMet al. (2006) The marine viromes of four oceanic regions. PLoS Biol 4: e368. Aro E-M, Virgin I & Andersson B (1993) Photoinhibition of photosystem-2-inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134. Blanco L, Bernad A, L´azaro JM, Mart´ın G, Garmendia C & Salas M (1989) Highly efficient DNA synthesis by the phage phi 29 DNA polymerase. Symmetrical mode of DNA replication. J Biol Chem 264: 8935–8940. Cann A (2005) Principles of Molecular Virology. Elsevier Academic Press, Burlington, MA. Castberg T, Larsen A, Sandaa RA, Brussaard CPD, Egge JK, Heldal M, Thyrhaug R, van Hannen EJ & Bratbak G (2001) Microbial population dynamics and diversity during a bloom of the marine coccolithophorid Emiliania huxleyi (Haptophyta). Mar Ecol Progr Ser 221: 39–46. Castberg T, Thyrhaug R, Larsen A, Sandaa RA, Heldal M, Van Etten JL & Bratbak G (2002) Isolation and characterization of a virus that infects Emiliania huxleyi (Haptophyta). J Phycol 38: 767–774. Chen F & Lu J (2002) Genomic sequence and evolution of marine cyanophage P60: a new insight on lytic and lysogenic phages. Appl Environ Microbiol 68: 2589–2594. Clokie MRJ, Shan J, Bailey S, Jia Y, Krisch HM, West S & Mann NH (2006a) Transcription of a ‘photosynthetic’ T4-type phage that infects marine cyanobacteria. Environ Microbiol 8: 827–835. Clokie MRJ, Millard AD, Mehta JY & Mann NH (2006b) Virus isolation studies suggest short-term variations in abundance in natural cyanophage populations of the Indian Ocean. J Mar Biol Ass UK 86: 499–505. Dean FB, Hosono S, Fang L et al. (2002) Comprehensive human genome amplification using multiple displacement amplification. Proc Natl Acad Sci USA 99: 5261–5266. Detter JC, Jett JM, Lucas SM et al. (2002) Isothermal stranddisplacement amplification applications for high-throughput genomics. Genomics 80: 691–698. Fuller NJ, Wilson WH, Joint IR & Mann NH (1998) Occurrence of a sequence in marine cyanophages similar to that of T4 g20 and its application to PCR-based detection and quantification techniques. Appl Environ Microbiol 64: 2051–2060. Jiang S, FuW, Chu W & Fuhrman JA (2003) The vertical distribution and diversity of marine bacteriophage at a station off Southern California. Microb Ecol 45: 399–410. Jiang Z, Zhang X, Deka R & Jin L (2005) Genome amplification of single sperm using multiple displacement amplification. Nucleic Acids Res 33: e91. Larsen A, Castberg T, Sandaa RA, Brussaard CPD, Egge J, Heldal M, Paulino A, Thyrhaug R, van Hannen EJ & Bratbak G (2001) Population dynamics and diversity of phytoplankton, bacteria and viruses in a seawater enclosure. Mar Ecol Prog Ser 221: 47–57. Larsen A, Flaten GAF, Sandaa RA, Castberg T, Thyrhaug R, Erga SR, Jacquet S & Bratbak G (2004) Spring phytoplankton bloom dynamics in Norwegian coastal waters: microbial community succession and diversity. Limnol Oceanogr 49: 180–190. Li WKW (1995) Composition of ultraphytoplankton in the central North-Atlantic. Mar Ecol Prog Ser 122: 1–8. Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F & Chisholm SW (2004) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad SciUSA 101: 11013–11018. Lindell D, Jaffe JD, Johnson ZI, Church GM & Chisholm SW (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438: 86. Liu HB, Nolla HA & Campbell L (1997) Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Microb Ecol 12: 39–47. Mann NH (2003) Phages of the marine cyanobacterial picophytoplankton. FEMS Microbiol Rev 27: 17–34. Mann NH, Clokie MRJ, Millard A, Cook A, Wilson WH, Wheatley PJ, Letarov A & Krisch HM (2005) The genome of S-PM2, a ‘photosynthetic’ T4-type bacteriophage that infects marine Synechococcus strains. J Bacteriol 187: 3188–3200. Millard A, Clokie MRJ, Shub DA & Mann NH (2004) Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci USA 101: 11007–11012. Olson RJ, Chisholm SW, Zettler ER, Altabet MA & Dusenberry JA (1990) Spatial and temporal distributions of prochlorophyte picoplankton in the North Atlantic Ocean. Deep-Sea Res Part A-Oceanogr Res Papers 37: 1033. Ovreas L, Bourne D, Sandaa RA, Casamayor EO, Benlloch S, Goddard V, Smerdon G, Heldal M & Thingstad TF (2003) Response of bacterial and viral communities to nutrient manipulations in seawater mesocosms. Aquat Microb Ecol 31: 109–121. Partensky F, Hess WR & Vaulot D (1999) Prochlorococcus a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106–127. Proctor LM & Fuhrman JA (1990) Viral mortality of marinebacteria and cyanobacteria. Nature 343: 60–62. Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, La Scola B, Suzan M & Claverie J (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306: 1344–1350. Rapp´e M & Giovannoni S (2003) The uncultured microbial majority. Annu Rev Microbiol 57: 369–394. Riemann L & Middelboe M (2002) Stability of bacterial and viral community compositions in Danish coastal waters as depicted by DNA fingerprinting techniques. Aquat Microb Ecol 27: 219–232. Sandaa RA & Larsen A (2006) Seasonal variations in viral-host populations in Norwegian coastal waters: focusing on the
URI:	http://wrap.warwick.ac.uk/id/eprint/30897

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