Home LiteratureArticle Details
PMID: 15828858 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations.

PLoS biology ·Vol. 3 ·No. 5 ·2005-05-00 ·Pages e144

Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW

Abstract

The oceanic cyanobacteria Prochlorococcus are globally important, ecologically diverse primary producers. It is thought that their viruses (phages) mediate population sizes and affect the evolutionary trajectories of their hosts. Here we present an analysis of genomes from three Prochlorococcus phages: a podovirus and two myoviruses. The morphology, overall genome features, and gene content of these phages suggest that they are quite similar to T7-like (P-SSP7) and T4-like (P-SSM2 and P-SSM4) phages. Using the existing phage taxonomic framework as a guideline, we examined genome sequences to establish "core" genes for each phage group. We found the podovirus contained 15 of 26 core T7-like genes and the two myoviruses contained 43 and 42 of 75 core T4-like genes. In addition to these core genes, each genome contains a significant number of "cyanobacterial" genes, i.e., genes with significant best BLAST hits to genes found in cyanobacteria. Some of these, we speculate, represent "signature" cyanophage genes. For example, all three phage genomes contain photosynthetic genes (psbA, hliP) that are thought to help maintain host photosynthetic activity during infection, as well as an aldolase family gene (talC) that could facilitate alternative routes of carbon metabolism during infection. The podovirus genome also contains an integrase gene (int) and other features that suggest it is capable of integrating into its host. If indeed it is, this would be unprecedented among cultured T7-like phages or marine cyanophages and would have significant evolutionary and ecological implications for phage and host. Further, both myoviruses contain phosphate-inducible genes (phoH and pstS) that are likely to be important for phage and host responses to phosphate stress, a commonly limiting nutrient in marine systems. Thus, these marine cyanophages appear to be variations of two well-known phages-T7 and T4-but contain genes that, if functional, reflect adaptations for infection of photosynthetic hosts in low-nutrient oceanic environments.

MeSH Terms
Bacteriophage T7/classification,genetics Bacteriophages/classification,genetics DNA-Directed RNA Polymerases/genetics Ecosystem Genome, Bacterial Genome, Viral Molecular Sequence Data Prochlorococcus/genetics,virology
Chemicals
DNA-Directed RNA Polymerases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Sullivan Matthew B
Joint Program in Biological Oceanography, Woods Hole Oceanographic Institution and Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.
Coleman Maureen L
Weigele Peter
Rohwer Forest
Chisholm Sallie W
References (91)
91 references, click to expand
  1. Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage.
    Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2192-7 PMID: 10051617
  2. Prochlorococcus, a marine photosynthetic prokaryote of global significance.
    Microbiol Mol Biol Rev. 1999 Mar;63(1):106-27 PMID: 10066832
  3. Isolation and characterization of a split B-type DNA polymerase from the archaeon Methanobacterium thermoautotrophicum deltaH.
    J Biol Chem. 1999 Oct 1;274(40):28751-61 PMID: 10497247
  4. In vitro synthesis of the nucleotide loop of cobalamin by Salmonella typhimurium enzymes.
    Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):11798-803 PMID: 10518530
  5. The structure of bacteriophage T4 gene product 9: the trigger for tail contraction.
    Structure. 1999 Oct 15;7(10):1213-22 PMID: 10545330
  6. Conservation of the pyrrolnitrin biosynthetic gene cluster among six pyrrolnitrin-producing strains.
    FEMS Microbiol Lett. 1999 Nov 1;180(1):39-44 PMID: 10547442
  7. Phosphate depletion in the western North Atlantic Ocean.
    Science. 2000 Aug 4;289(5480):759-62 PMID: 10926534
  8. Structure of bacteriophage T4 gene product 11, the interface between the baseplate and short tail fibers.
    J Mol Biol. 2000 Aug 25;301(4):975-85 PMID: 10966799
  9. Phylogeny of the major head and tail genes of the wide-ranging T4-type bacteriophages.
    J Bacteriol. 2001 Jan;183(1):358-66 PMID: 11114936
  10. Fructose-6-phosphate aldolase is a novel class I aldolase from Escherichia coli and is related to a novel group of bacterial transaldolases.
    J Biol Chem. 2001 Apr 6;276(14):11055-61 PMID: 11120740
  11. Interaction of the PhiHSIC virus with its host: lysogeny or pseudolysogeny?
    Appl Environ Microbiol. 2001 Apr;67(4):1682-8 PMID: 11282621
  12. Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms.
    Plant Cell. 2001 Apr;13(4):965-78 PMID: 11283349
  13. No syringes please, ejection of phage T7 DNA from the virion is enzyme driven.
    Mol Microbiol. 2001 Apr;40(1):1-8 PMID: 11298271
  14. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions.
    Nucleic Acids Res. 2001 Jun 15;29(12):2607-18 PMID: 11410670
  15. Distribution, isolation, host specificity, and diversity of cyanophages infecting marine Synechococcus spp. in river estuaries.
    Appl Environ Microbiol. 2001 Jul;67(7):3285-90 PMID: 11425754
  16. Two recombination-dependent DNA replication pathways of bacteriophage T4, and their roles in mutagenesis and horizontal gene transfer.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8306-11 PMID: 11459968
  17. Identification and crystallisation of a heat- and protease-stable fragment of the bacteriophage T4 short tail fibre.
    Biol Chem. 2001 Jul;382(7):1049-55 PMID: 11530935
  18. Phycobiliprotein genes of the marine photosynthetic prokaryote Prochlorococcus: evidence for rapid evolution of genetic heterogeneity.
    Microbiology. 2001 Nov;147(Pt 11):3171-82 PMID: 11700369
  19. Phage genomics: small is beautiful.
    Cell. 2002 Jan 11;108(1):13-6 PMID: 11792317
  20. Lysogeny in marine Synechococcus.
    Nature. 2002 Jan 31;415(6871):496 PMID: 11823851
  21. Streptomyces spp. contain class Ia and class II ribonucleotide reductases: expression analysis of the genes in vegetative growth.
    Microbiology. 2002 Feb;148(Pt 2):391-404 PMID: 11832503
  22. Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies.
    Nucleic Acids Res. 2002 Feb 15;30(4):866-75 PMID: 11842097
  23. Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies.
    Trends Microbiol. 2002 Mar;10(3):134-42 PMID: 11864823
  24. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing.
    Bioinformatics. 2002 Mar;18(3):502-4 PMID: 11934758
  25. Genomic sequence and evolution of marine cyanophage P60: a new insight on lytic and lysogenic phages.
    Appl Environ Microbiol. 2002 May;68(5):2589-94 PMID: 11976141
  26. Lysogeny and lytic viral production during a bloom of the cyanobacterium Synechococcus spp.
    Microb Ecol. 2002 Mar;43(2):225-31 PMID: 12023729
  27. Crystal structure of decameric fructose-6-phosphate aldolase from Escherichia coli reveals inter-subunit helix swapping as a structural basis for assembly differences in the transaldolase family.
    J Mol Biol. 2002 May 24;319(1):161-71 PMID: 12051943
  28. MazG, a nucleoside triphosphate pyrophosphohydrolase, interacts with Era, an essential GTPase in Escherichia coli.
    J Bacteriol. 2002 Oct;184(19):5323-9 PMID: 12218018
  29. Genomic analysis of uncultured marine viral communities.
    Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14250-5 PMID: 12384570
  30. Isolation of the gene for the B12-dependent ribonucleotide reductase from Anabaena sp. strain PCC 7120 and expression in Escherichia coli.
    J Bacteriol. 2002 Dec;184(23):6544-50 PMID: 12426342
  31. Marine phage genomics.
    Comp Biochem Physiol B Biochem Mol Biol. 2002 Dec;133(4):463-76 PMID: 12470812
  32. Phycocyanobilin:ferredoxin oxidoreductase of Anabaena sp. PCC 7120. Biochemical and spectroscopic.
    J Biol Chem. 2003 Mar 14;278(11):9219-26 PMID: 12514179
  33. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440.
    Environ Microbiol. 2002 Dec;4(12):799-808 PMID: 12534463
  34. Bacteriophage T4 genome.
    Microbiol Mol Biol Rev. 2003 Mar;67(1):86-156, table of contents PMID: 12626685
  35. Thermotoga maritima MazG protein has both nucleoside triphosphate pyrophosphohydrolase and pyrophosphatase activities.
    J Biol Chem. 2003 Jun 13;278(24):21408-14 PMID: 12657645
  36. Phages of the marine cyanobacterial picophytoplankton.
    FEMS Microbiol Rev. 2003 Apr;27(1):17-34 PMID: 12697340
  37. Global phage diversity.
    Cell. 2003 Apr 18;113(2):141 PMID: 12705861
  38. Origins of highly mosaic mycobacteriophage genomes.
    Cell. 2003 Apr 18;113(2):171-82 PMID: 12705866
  39. Bioinformatics classification and functional analysis of PhoH homologs.
    In Silico Biol. 2003;3(1-2):3-15 PMID: 12762842
  40. The complete sequence of marine bacteriophage VpV262 infecting vibrio parahaemolyticus indicates that an ancestral component of a T7 viral supergroup is widespread in the marine environment.
    Virology. 2003 Jun 5;310(2):359-71 PMID: 12781722
  41. Prophage genomics.
    Microbiol Mol Biol Rev. 2003 Jun;67(2):238-76, table of contents PMID: 12794192
  42. The diversity and evolution of the T4-type bacteriophages.
    Res Microbiol. 2003 May;154(4):259-67 PMID: 12798230
  43. Prophages and bacterial genomics: what have we learned so far?
    Mol Microbiol. 2003 Jul;49(2):277-300 PMID: 12886937
  44. The genome of bacteriophage phiKMV, a T7-like virus infecting Pseudomonas aeruginosa.
    Virology. 2003 Jul 20;312(1):49-59 PMID: 12890620
  45. Genetic diversity and temporal variation in the cyanophage community infecting marine Synechococcus species in Rhode Island's coastal waters.
    Appl Environ Microbiol. 2003 Aug;69(8):4639-47 PMID: 12902252
  46. Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome.
    Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):10020-5 PMID: 12917486
  47. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation.
    Nature. 2003 Aug 28;424(6952):1042-7 PMID: 12917642
  48. Marine ecosystems: bacterial photosynthesis genes in a virus.
    Nature. 2003 Aug 14;424(6950):741 PMID: 12917674
  49. Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage.
    J Bacteriol. 2003 Sep;185(17):5220-33 PMID: 12923095
  50. Three-dimensional structure of bacteriophage T4 baseplate.
    Nat Struct Biol. 2003 Sep;10(9):688-93 PMID: 12923574
  51. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus.
    Nature. 2003 Aug 28;424(6952):1047-51 PMID: 12944965
  52. A role for bacteriophage T4 rI gene function in the control of phage development during pseudolysogeny and in slowly growing host cells.
    Res Microbiol. 2003 Oct;154(8):547-52 PMID: 14527655
  53. Lateral gene transfer: when will adolescence end?
    Mol Microbiol. 2003 Nov;50(3):739-49 PMID: 14617137
  54. Phage integrases: biology and applications.
    J Mol Biol. 2004 Jan 16;335(3):667-78 PMID: 14687564
  55. Genomic analysis of bacteriophages SP6 and K1-5, an estranged subgroup of the T7 supergroup.
    J Mol Biol. 2004 Jan 30;335(5):1151-71 PMID: 14729334
  56. Transfer of photosynthesis genes to and from Prochlorococcus viruses.
    Proc Natl Acad Sci U S A. 2004 Jul 27;101(30):11013-8 PMID: 15256601
  57. Genetic organization of the psbAD region in phages infecting marine Synechococcus strains.
    Proc Natl Acad Sci U S A. 2004 Jul 27;101(30):11007-12 PMID: 15263091
  58. DNA sequences of the tail fiber genes of bacteriophage P2: evidence for horizontal transfer of tail fiber genes among unrelated bacteriophages.
    J Bacteriol. 1992 Mar;174(5):1462-77 PMID: 1531648
  59. The genome of S-PM2, a "photosynthetic" T4-type bacteriophage that infects marine Synechococcus strains.
    J Bacteriol. 2005 May;187(9):3188-200 PMID: 15838046
  60. The photosynthetic apparatus of Prochlorococcus: Insights through comparative genomics.
    Photosynth Res. 2001;70(1):53-71 PMID: 16228362
  61. Resistance to co-occurring phages enables marine synechococcus communities to coexist with cyanophages abundant in seawater.
    Appl Environ Microbiol. 1993 Oct;59(10):3393-9 PMID: 16349072
  62. Dynamics and Distribution of Cyanophages and Their Effect on Marine Synechococcus spp.
    Appl Environ Microbiol. 1994 Sep;60(9):3167-74 PMID: 16349372
  63. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  64. PRESENCE OF PHYCOERYTHRIN IN TWO STRAINS OF PROCHLOROCOCCUS (CYANOBACTERIA) ISOLATED FROM THE SUBTROPICAL NORTH PACIFIC OCEAN .
    J Phycol. 2000 Aug 26;36(4):723-729 PMID: 29542150
  65. Length and shape variants of the bacteriophage T4 head: mutations in the scaffolding core genes 68 and 22.
    J Virol. 1988 Aug;62(8):2960-9 PMID: 3292792
  66. Isolation and characterization of a virus infecting a blue-green alga of the genus Synechococcus.
    Virology. 1973 Jul;54(1):230-6 PMID: 4197413
  67. Assembly of the tail of bacteriophage T4.
    J Mol Biol. 1968 Mar 14;32(2):231-62 PMID: 4868421
  68. Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements.
    J Mol Biol. 1983 Jun 5;166(4):477-535 PMID: 6864790
  69. Gene 67, a new, essential bacteriophage T4 head gene codes for a prehead core component, PIP. I. Genetic mapping and DNA sequence.
    J Mol Biol. 1982 Nov 15;161(4):479-89 PMID: 7154087
  70. Gene 67, a new, essential bacteriophage T4 head gene codes for a prehead core component, PIP. II. The construction in vitro of unconditionally lethal mutants and their maintenance.
    J Mol Biol. 1982 Nov 15;161(4):491-504 PMID: 7154088
  71. The cobalamin (coenzyme B12) biosynthetic genes of Escherichia coli.
    J Bacteriol. 1995 Nov;177(22):6371-80 PMID: 7592411
  72. Tail sheath and tail tube genes of the temperate coliphage 186.
    Virology. 1995 Sep 10;212(1):218-21 PMID: 7676633
  73. Infection of Synechococcus cedrorum by the cyanophage AS-1M. III. Cellular metabolism and phage development.
    Virology. 1976 May;71(1):199-206 PMID: 818807
  74. Isolation and characterization of a cyanophage infecting the unicellular blue-green algae A. nidulans and S. cedrorum.
    Virology. 1976 Jul 15;72(2):540-4 PMID: 821247
  75. Molecular analysis of the phoH gene, belonging to the phosphate regulon in Escherichia coli.
    J Bacteriol. 1993 Mar;175(5):1316-24 PMID: 8444794
  76. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis.
    Gene. 1995 Dec 29;167(1-2):GC1-10 PMID: 8566757
  77. Genetics of pentose-phosphate pathway enzymes of Escherichia coli K-12.
    Arch Microbiol. 1995 Nov;164(5):324-30 PMID: 8572885
  78. Stoichiometry and domainal organization of the long tail-fiber of bacteriophage T4: a hinged viral adhesin.
    J Mol Biol. 1996 Aug 2;260(5):767-80 PMID: 8709154
  79. Evolution of T4-related phages.
    Virus Genes. 1995;11(2-3):285-97 PMID: 8828153
  80. The effects of spermine and spermidine on the structure of photosystem II proteins in relation to inhibition of electron transport.
    FEBS Lett. 1997 Jan 27;402(1):41-4 PMID: 9013855
  81. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence.
    Nucleic Acids Res. 1997 Mar 1;25(5):955-64 PMID: 9023104
  82. Four genes from Pseudomonas fluorescens that encode the biosynthesis of pyrrolnitrin.
    Appl Environ Microbiol. 1997 Jun;63(6):2147-54 PMID: 9172332
  83. An immunological approach to detect phosphate stress in populations and single cells of photosynthetic picoplankton.
    Appl Environ Microbiol. 1997 Jun;63(6):2411-20 PMID: 9172363
  84. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  85. Similarities and differences among 105 members of the Int family of site-specific recombinases.
    Nucleic Acids Res. 1998 Jan 15;26(2):391-406 PMID: 9421491
  86. Functions encoded by pyrrolnitrin biosynthetic genes from Pseudomonas fluorescens.
    J Bacteriol. 1998 Apr;180(7):1939-43 PMID: 9537395
  87. Bacteriophage collagen.
    Science. 1998 Mar 20;279(5358):1834 PMID: 9537896
  88. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes.
    Nature. 1998 Jun 4;393(6684):464-7 PMID: 9624000
  89. A catalogue of T4-type bacteriophages.
    Arch Virol. 1997;142(12):2329-45 PMID: 9672598
  90. Genome plasticity in the distal tail fiber locus of the T-even bacteriophage: recombination between conserved motifs swaps adhesin specificity.
    J Mol Biol. 1998 Sep 25;282(3):543-56 PMID: 9737921
  91. Recombination and recombination-dependent DNA replication in bacteriophage T4.
    Annu Rev Genet. 1998;32:379-413 PMID: 9928485
Article Info
Journal
PLoS biology
Abbr.
PLoS Biol
ISSN
1545-7885
Published
2005-05-00
Epub
2005-00-19
Pages
e144
Language
English
Region
United States
NLM ID
101183755
PMCID
PMC1079782
Subset
IM
Databases
GENBANK
AY939843, AY939844, AY940168, BX548174
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com