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EVOLUTIONARY HISTORY OF PHAGES WITH dsDNA GENOMES Arcady Mushegian Stowers Institute, Kansas City, USA Image: A. Merkov © 2007,

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Presentation on theme: "EVOLUTIONARY HISTORY OF PHAGES WITH dsDNA GENOMES Arcady Mushegian Stowers Institute, Kansas City, USA Image: A. Merkov © 2007,"— Presentation transcript:

1 EVOLUTIONARY HISTORY OF PHAGES WITH dsDNA GENOMES Arcady Mushegian Stowers Institute, Kansas City, USA Image: A. Merkov © 2007, http://wsbs-msu.ru/foto Image: A. Merkov © 2007, http://wsbs-msu.ru/foto

2 Galina Glazko University of Rochester, USA Vladimir Makarenkov Université du Québec à Montreal, Canada Jing Liu U of Kansas - Utah Law

3 SiphoviridaeMyoviridaePodoviridaeTectiviridaeLipothrixviridae Fuselloviridae ICTV CLASSIFICATION: VIRION SHAPE PLUS A FEW MOLECULAR CHARACTERS RudiviridaeCorticoviridaePlasmaviridae lambdaT4P60SIFV SIRV2SSV1 Bam35c & PRD1 L2PM2

4 EVOLUTIONARY HISTORY OF PHAGES : A GENOME-BASED APPROACH ? EVOLUTIONARY HISTORY OF PHAGES : A GENOME-BASED APPROACH ? WHY ICTV APPROACH IS NOT ENOUGH : WHY ICTV APPROACH IS NOT ENOUGH : - LOW RESOLUTION OF STRUCTURAL TRAITS - LOW RESOLUTION OF STRUCTURAL TRAITS - STRUCTURE CONVERGENCE ? - STRUCTURE CONVERGENCE ? - NO WAY TO ACCOUNT FOR HGT - NO WAY TO ACCOUNT FOR HGT CAN WE DO BETTER WITH GENOMES ? CAN WE DO BETTER WITH GENOMES ? - ARE THERE ENOUGH MOLECULAR TRAITS ? - ARE THERE ENOUGH MOLECULAR TRAITS ? - WILL HGT SWAMP EVERYTHING ? - WILL HGT SWAMP EVERYTHING ?

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6 RECOMBINATION DOES NOT HAVE TO BE HOMOLOGOUS Modified from J.G.Lawrence et al., J.Bacteriol. 2002

7 PHYLOGENY BASED ON GENE CONTENT PHYLOGENY BASED ON GENE CONTENT THE CLOSER TWO GENOMES ARE, THE MORE GENES THEY HAVE IN COMMON - ALL CLASSES OF METHODS CAN BE APPLIED - ALL CLASSES OF METHODS CAN BE APPLIED - NO NEED FOR OMNIPRESENT GENES - NO NEED FOR OMNIPRESENT GENES - HOW TO MEASURE AND NORMALIZE ? - HOW TO MEASURE AND NORMALIZE ? USED WITH BACTERIA (Koonin, Bork ) AND PHAGES (Rohwer and Edwards, J. Bacteriol. 2002) USED WITH BACTERIA (Koonin, Bork ) AND PHAGES (Rohwer and Edwards, J. Bacteriol. 2002) - HGT WAS STILL UNACCOUNTED FOR - HGT WAS STILL UNACCOUNTED FOR

8 Bacteriophages dsDNAssDNAdsRNA domains tailedfilamentousicosahedral … divisions modus Imodus IImodus IIImodus IV modi … RETICULATE EVOLUTION PROPOSAL FOR PHAGE TAXONOMY (Lawrence et al., 2002) kingdom Phage SfV might belong to the domain of dsDNA viruses, the division of tailed bacteriophages, but to at least 3 modi : (i)Phages with HK97-like head proteins and maturation processes, (ii)Phages with Mu-like contractile tails, and (iii) Integrase-mediated temperate phages.

9 BUT …. … HOW WE DERIVE THE MODI ? … WHAT IS THE EVOLUTIONARY SCENARIO ? ( esp. given the claim of a new view of viral evolution, classification, and taxonomy ?? ) ON THE BRIGHT SIDE : ON THE BRIGHT SIDE : THE IMPORTANCE OF HGT THE IMPORTANCE OF HGT

10 A POST-MODERN DISTRACTION: A TREE ( OF LIFE ) OR NOT A TREE? THE GOAL OF EVOLUTIONARY RECONSTRUCTION IS NOT TO BUILD A TREE, BUT TO LEARN WHAT HAPPENED OR ? W.F.Doolittle, Science 1999 © AAAS

11 PHAGE ORTHOLOGOUS GROUPS ( POGs ) - FOLLOWING THE NCBI COG FRAMEWORK Tatusov et al., Science 1997; NCBI 1997-2007

12 VECTORS OF GENE CONTENT IN PHAGES

13 THE MAIN OBSERVATIONS - FAT-TAILED DISTRIBUTION, MANY ZEROS - HIGH POG CONTENT IN GENOMES - av. 52 % (mostly 30 - 70 %) - av. 42 % even for the unclassified phages - PHAGENESS QUOTIENT where, i.e., is this POG more likely to be drawn from a phage or from a cellular organism?

14 WHY HIGH PQ IS IMPORTANT PQ max = (phage-specific POGs) 82% OF POGs HAVE PQ = + 8% - HIGH PQ, FORM A CLADE - MOST OF THE POGS TAKE NO PART IN HOST-VIRUS GENE TRANSFER - WE CAN RESTATE THE TASK AS DETECTION OF PHAGE-PHAGE HGT

15 TREES FROM GENE CONTENT, NO HGT YET - PRETEND THAT DESPITE HGT, EVOLUTION OF PHAGES IS TREE-LIKE - BUILT CONVENTIONAL TREE, VERIFY THAT THE SIGNAL IS TRUE, THEN INFER HGT - DISTANCE METHODS REQUIRE PROPER DISTANCE MEASURE ( SEPARATE STORY …)

16 NJMrBayes Siphoviridae Podoviridae Myoviridae Fuselloviridae Tectiviridae Unclassified TREES FROM GENE CONTENT

17 Siphoviridae Podoviridae Myoviridae Fuselloviridae Tectiviridae Unclassified

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19 TREES FROM GENE CONTENT - CONCLUSIONS - VERTICAL SIGNAL IS CONSIDERABLE - RESAMPLING, SIMULATIONS, COMPATIBILITY - 18 WELL-SUPPORTED GROUPS - 71 % OF ALL PHAGES - SOME GROUPS INCLUDE PHAGES WITH DIFFERENT MORPHOLOGY - THE LARGEST 3 ICTV MORPHOTYPES DO NOT RESOLVE AS MONOPHYLETIC

20 GROUPS WITH SIMILAR MORPHOLOGY group 2 staphylococci phages group 3 Sfi21-like siphoviruses group 7 fuselloviruses group 11 -like siphoviruses group 14 T4-like myoviruses group 18 P2-like myoviruses and groups 4, 5, 6, 8, 10 Siphoviridae Myoviridae Fuselloviridae Unclassified

21 group 9 PZA-like podoviruses group 13 mycobacteriophages group 15 T7-like podoviruses group 16 and groups 1, 12, 17 Siphoviridae Podoviridae Myoviridae Tectiviridae Unclassified GROUPS WITH DISSIMILAR MORPHOLOGY

22 HOW TO INFER RETICULATIONS ? IN PRACTICE : T-REX (MAKARENKOV, 1999-2007) - SPR OF T GC, MINIMIZE DISTANCE TO T SF, WHILE MAINTAINING SUB-TREE TOPOLOGIES

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24 HGT EVENTS IN NUMBERS 294 HGT EVENTS 90 % within groups 114 (of 158) PHAGES ARE INVOLVED GENES FROM 229 POGs HAVE BEEN TRANSFERRED REMOVE THESE POGs : GROUPS STAY TOGETHER, SOME LOSE 1-2 MEMBERS

25 FREQUENCY DISTRIBUTIONS OF ALL HGT EVENTS ARE FAT-TAILED MOST PHAGES RARELY EXCHANGE GENES MOST POGs ARE NEVER TRANSFERRED THE HGT DEBATE ( NOT ONLY IN PHAGES ) IS ABOUT THE OPPOSITE TAILS OF THE SAME DISTRIBUTION

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27 WHAT NEXT - MORE PHAGES ( ~500 ) -MORE TRAITS, EVEN FOR CURRENT COLLECTION -HIGHER DENSITY OF TAXON SPACE - TRAITS OTHER THAN ORFs -COS, PAC SITES? - BETTER METHODS -ARE ICTV FAMILIES MONOPHYLETIC ? -RELATIONSHIP WITH HERPESVIRUSES ? -ON TO BACTERIAL EVOLUTION ?

28 http://www.stowers-institute.org/ScientistsSought/TrainingPrograms.asp

29 52% of the analyzed phage proteins are clustered into 981 Phage Orthologous Groups (POGs) ICTV family Number ofNumber of Number of proteins POG genomes proteins in POGs coverage Myoviridae 28 3538 1526 43% Siphoviridae 80 5815 3431 59% Podoviridae 31 1520 879 58% Tectiviridae 2 55 10 18% Cortiviridae 1 22 3 14% Plasmaviridae 1 14 2 14% Fuselloviridae 4 134 79 59% Lipothrixviridae 1 72 5 7% Unclassified 16 1052 443 42% Total number164 12222 6378 52%

30 POGs shared by phage genomes are suitable characters in evolutionary reconstruction

31 461 POGs belong to 14 functional categories L, replication, recombination, and repair K, transcription F, nucleotide transport and metabolism X, virion assembly S, unknown function X,Y,Z,W,V,U,A – phage specific categories

32 Phages vary significantly in genome size and content 381 8

33 How to normalize shared gene count I. Correlation between gene-content trees and 16S rRNA-based tree JC: Jaccard coefficient distance MB: Maryland bridge distance WA: Weighted average distanceCORR: Standard correlation distance

34 How to normalize shared gene count II. The effect of differences in genome sizes Number of shared genes (k) = 100 Number of shared genes (k) = 500 Size of Genome 1: N1 = 1000, size of Genome 2: N2 JC: Jaccard coefficient distance MB: Maryland bridge distance WA: Weighted average distanceCORR: Standard correlation distance

35 Possible evolutionary links between viruses from different host domains Hendrix 1999 Curr. Biol. Shared colors indicate proposed evolutionary connections between relevant viruses

36 Many dsDNA phage prohead proteases are herpesvirus assemblin-like serine proteases Liu & Mushegian, 2004 J. Bacteriol.


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