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Evolution of bacterial regulatory systems

Evolution of bacterial regulatory systems. Mikhail Gelfand Institute for Information Transmission Problems, RAS BGRS-2004, Novosibirsk. Early analyses (BGRS’98, 00, 02). “Making good predictions with bad rules” Basic assumption : regulons are conserved =>

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Evolution of bacterial regulatory systems

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  1. Evolution of bacterial regulatory systems Mikhail Gelfand Institute for Information Transmission Problems, RAS BGRS-2004, Novosibirsk

  2. Early analyses (BGRS’98, 00, 02) “Making good predictions with bad rules” Basic assumption: regulons are conserved => Consistency check: sites upstream of orthologous genes are correct; false positives are scattered at random • Validation of individual sites • Validation of signals: candidate signals for orthologous factors are correct if similar

  3. Multiple genomes: taxon-specific regulation; multiple interacting systems; evolution of regulation • Evolution of orthologous regulatory sites • Co-evolution of transcription factors and their binding signals • Evolution of regulons (sets of co-regulated genes) • Evolution of regulatory systems

  4. Это – ряд наблюдений. В углу – тепло. Взгляд оставляет на вещи след. Вода представляет собой стекло. Человек страшней, чем его скелет.Иосиф Бродский A list of some observations. In a corner, it’s warm. A glance leaves an imprint on anything it’s dwelt on. Water is glass’s most public form. Man is more frightening than its skeleton. Joseph Brodsky

  5. Conservation of non-consensus positions in orthologous sites regulatory site LexAlexAconsensus nucleotides are in caps wrong consensus?

  6. PurRpurL PurRpurM

  7. Non-consensus positions are more conserved than synonymous codon positions

  8. Non-consensus positions may be more conserved than consensus positions

  9. Regulators and their signals • Subtle changes at close evolutionary distances • Changes in spacing / geometry of dimers • Correlation between contacting nucleotides and amino acid residues • Cases of conservation at surprisingly large distances

  10. nZUR- nZUR- Zinc repressors GAAATGTTATANTATAACATTTC GATATGTTATAACATATC GTAATGTAATAACATTAC TTAACYRGTTAA pZUR AdcR TAAATCGTAATNATTACGATTTA

  11. Alignment ofnZUR binding signals GTAATGTAA TAACATTAC (alpha – most genera) GATATGTTA TAACATATC (alpha – Rhodobacter) GAAATGTTATANTATAACATTTC (gamma) GaaATGTtA-----TAACATttC (consensus of consensi)

  12. CRP/FNR family of regulators

  13. Correlation between contacting nucleotides and amino acid residues Contacting residues: REnnnR TG: 1st arginine GA: glutamate and 2nd arginine • CooA in Desulfovibrio spp. • CRP in Gamma-proteobacteria • HcpR in Desulfovibrio spp. • FNR in Gamma-proteobacteria DD COOA ALTTEQLSLHMGATRQTVSTLLNNLVR DV COOA ELTMEQLAGLVGTTRQTASTLLNDMIR EC CRP KITRQEIGQIVGCSRETVGRILKMLED YP CRP KXTRQEIGQIVGCSRETVGRILKMLED VC CRP KITRQEIGQIVGCSRETVGRILKMLEE DD HCPR DVSKSLLAGVLGTARETLSRALAKLVE DV HCPR DVTKGLLAGLLGTARETLSRCLSRMVE EC FNR TMTRGDIGNYLGLTVETISRLLGRFQK YP FNR TMTRGDIGNYLGLTVETISRLLGRFQK VC FNR TMTRGDIGNYLGLTVETISRLLGRFQK TGTCGGCnnGCCGACA TTGTGAnnnnnnTCACAA TTGTgAnnnnnnTcACAA TTGATnnnnATCAA

  14. The correlation holds for other factors in the family

  15. The LacI family of transcrip-tional regulators (eachbranch represents a subfamily)

  16. … and their signals

  17. BirA: regulator of biotin biosynthesis and transport in eubacteria and archaea Profile 1:Gram-positive bacteria, Archaea Profile 2:Gram-negative bacteria

  18. Evolution of regulons and regulatory systems • conserved cores • taxon-specific marginal members • migration of genes between interacting regulatory systems • taxon-specific cross-regulation • genome-specific operons and genomic loci • complete change of regulatory mechanisms

  19. Genome loci for hyaluronate utilization in invasive Streptococcus spp. S. pyogenes, S. agalactiae S. equi S. pneumoniae TIGR4 S. pneumoniae R6 S. suis

  20. Respiration in gamma-proteobacteria1. Three regulators, different regulatory cascades Escherichia coli(experimental data) Haemophilus influenzae,Pasteurella multocida, A. actinomycetemcomitans Haemophilus ducreyi, Vibrio spp.

  21. Respiration in gamma-proteobacteria2. New genome/taxon-specific regulon members Escherichia coli(known) New, non-homologous regulon member Yersinia pestisFnr ArcA — Yersinia entercoliticaFnr — — Pasteurella multocidaFnr ArcA NarP Actinobacillus actinomycetemcomitans— ArcA NarP Haemophilus influenzae Fnr ArcA — Haemophilus ducreyiFnr ArcA NarP Vibrio vulnificus— ArcA — Vibrio parahaemolyticus— ArcA — Vibrio cholerae Fnr ArcA — Vibrio fischeri— ArcA —

  22. Respiration in gamma-proteobacteria3. New genome/taxon-specific regulon members, cont’d Synthesis of molybdate cofactor Yersinia pestisFnr — — Yersinia entercoliticaFnr ArcA — Pasteurella multocidaFnr ArcA — Actinobacillus actinomycetemcomitans Fnr—NarP Haemophilus influenzae Fnr—NarP Haemophilus ducreyiFnr ArcA NarP Vibrio vulnificus——NarP Vibrio parahaemolyticus——NarP Vibrio cholerae ——NarP Vibrio fischeri— ArcA NarP

  23. nZUR- nZUR- Zinc repressors - recapitulation GAAATGTTATANTATAACATTTC GATATGTTATAACATATC GTAATGTAATAACATTAC TTAACYRGTTAA pZUR AdcR TAAATCGTAATNATTACGATTTA

  24. Five regulatory systems for methionine biosynthesis • SAM-dependent RNA riboswitch • Met-tRNA-dependent T-box (RNA) C,D,E. repressors of transcription

  25. Three methionine regulatory systems in Gram-positive bacteria: loss of S-box regulons ZOO • S-boxes (riboswitch) • Bacillales • Clostridiales • the Zoo: • Petrotoga • actinobacteria (Streptomyces, Thermobifida) • Chlorobium, Chloroflexus, Cytophaga • Fusobacterium • Deinococcus • proteobacteria (Xanthomonas, Geobacter) • Met-T-boxes (Met-tRNA-dependent attenuator) • Lactobacillales • MET-boxes(candidate transcription signal) • Streptococcales Lact. Strep. Bac. Clostr.

  26. Catabolism of gluconate in proteobacteria

  27. Three regulatory systemsone global (FruR), two taxon-specific (GntR, PtxS) β γ1 Pseudomonas spp.

  28. Andrei A. Mironov (BGRS’98,00,02,04) Anna Gerasimova (BGRS’02,04) Olga Kalinina (BGRS’02,04) Alexei Kazakov (BGRS’02,04) Ekaterina Kotelnikova (BGRS’02,04) Galina Kovaleva (BGRS’04) Pavel Novichkov (BGRS’00,02,04) Olga Laikova (BGRS’02,04) Ekaterina Panina (BGRS’00)(now at UCLA, USA) Elizabeth Permina (BGRS’02,04) Dmitry Ravcheev (BGRS’02,04) Alexandra B. Rakhmaninova (BGRS’00) Dmitry Rodionov (BGRS’00) Alexey Vitreschak (BGRS’00,04)(visiting LORIA, France) Howard Hughes Medical Institute Ludwig Institute of Cancer Research Russian Fund of Basic Research Programs “Origin and Evolution of the Biosphere” and “Molecular and Cellular Biology”, Russian Academy of Sciences Instead of conclusions…

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