Symbiosis

, Volume 70, Issue 1–3, pp 69–78 | Cite as

Characterization of PAS domains in Frankia and selected Actinobacteria and their possible interaction with other co-domains for environmental adaptation

  • Indrani Sarkar
  • Philippe Normand
  • Louis S. Tisa
  • Maher Gtari
  • Asim Bothra
  • Arnab Sen
Article

Abstract

Functional domains are semi-autonomous parts of proteins. The Per-Arnt-Sim (PAS) domain functions as signal-sensor in two-component systems of several bacteria. This domain exhibits large sequence diversity and is linked to other co-domains to modulate their function. In the present study, we analyzed the PAS domains found in the proteomes of several actinobacteria representing a variety of niches. PAS-domain containing proteins were identified with the HMMER program and characterized via an in silico approach. In general, the PAS proteins were found to be in the COG T (signal transduction) category implying their role was indeed in signal transduction. Most of the PAS proteins were found to be structurally conserved and moderately expressed. However, they showed a strong bias towards the lagging strand which may be a result of their involvement in adaptive evolution. A structure based phylogenetic analysis showed that PAS domains with similar interacting co-domains grouped together in a cluster irrespective of the bacterial genus from which they were identified. Thus, we may say that the association of PAS with its co-domains is based upon the PAS domain structure and not on the sequence.

Keywords

Signal transduction Co-domain Structure-based phylogeny Domain-domain interaction Biological network 

Abbreviations

PAS proteins

PAS domain containing proteins

PAS genes

Gene sequence of PAS domain containing proteins

ENc

Effective number of codons

COA

Correspondence analysis

CAI

Codon adaptation index

Supplementary material

13199_2016_413_MOESM1_ESM.xls (28 kb)
ESM 1(XLS 27 kb)
13199_2016_413_MOESM2_ESM.pdf (680 kb)
ESM 2(PDF 680 kb)
13199_2016_413_MOESM3_ESM.xls (28 kb)
ESM 3(XLS 27 kb)
13199_2016_413_MOESM4_ESM.pdf (298 kb)
ESM 4(PDF 297 kb)
13199_2016_413_Fig4_ESM.gif (238 kb)
ESM 5

(TIF 266 kb)

13199_2016_413_MOESM5_ESM.tif (266 kb)
High resolution image (TIF 266 kb)
13199_2016_413_MOESM6_ESM.xls (24 kb)
ESM 6(XLS 23 kb)
13199_2016_413_MOESM7_ESM.xls (100 kb)
ESM 7(XLS 100 kb)
13199_2016_413_Fig5_ESM.gif (248 kb)
ESM 8

(TIF 1.03 mb)

13199_2016_413_MOESM8_ESM.tif (1 mb)
High resolution image (TIF 1114 kb)
13199_2016_413_MOESM9_ESM.doc (48 kb)
ESM 9(DOC 47 kb)
13199_2016_413_MOESM10_ESM.xlsx (11 kb)
ESM 10(XLSX 11 kb)

References

  1. Alloisio N et al. (2010) The Frankia alni symbiotic transcriptome. Mol Plant Microbe In 23.5: 593-607Google Scholar
  2. Aravind L, Ponting CP (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22:458–459CrossRefPubMedGoogle Scholar
  3. Badejo AC, Badejo AO, Shin KH, Chai YG (2013) A gene expression study of the activities of aromatic ring-cleavage dioxygenases in Mycobacterium gilvum PYR-GCK to changes in salinity and pH during pyrene degradation. PLoS One 8, e58066CrossRefPubMedPubMedCentralGoogle Scholar
  4. Banerjee T, Basak S, Gupta SK, Ghosh TC (2004) Evolutionary forces in shaping the codon and amino acid usages in Blochmannia floridanus. J Biomol Struct Dyn 22:13–23CrossRefPubMedGoogle Scholar
  5. Barabote RD et al (2009) Complete genome of the cellulolytic thermophile Acidothermus cellulolyticus 11B provides insights into its ecophysiological and evolutionary adaptations. Genome Res 19:1033–1043CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bentley SD et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147CrossRefPubMedGoogle Scholar
  7. Bibikov SI, Barnes LA, Gitin Y, Parkinson JS (2000) Domain organization and flavin adenine dinucleotide-binding determinants in the aerotaxis signal transducer Aer of Escherichia coli. Proc Natl Acad Sci U S A 97:5830–5835CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bignell DR, Seipke RF, Huguet-Tapia JC, Chambers AH, Parry RJ, Loria R (2010) Streptomyces scabies 87–22 contains a coronafacic acid-like biosynthetic cluster that contributes to plant-microbe interactions. Mol Plant Microbe Interact 23:161–175CrossRefPubMedGoogle Scholar
  9. Chouaia B et al (2012) Genome sequence of Blastococcus saxobsidens DD2, a stone-inhabiting bacterium. J Bacteriol 194:2752–2753CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cui T, Zhang L, Wang X, He ZG (2009) Uncovering new signaling proteins and potential drug targets through the interactome analysis of Mycobacterium tuberculosis. BMC Genomics 10:118CrossRefPubMedPubMedCentralGoogle Scholar
  11. David M et al (1988) Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 54:671–683CrossRefPubMedGoogle Scholar
  12. Dunham CM, Dioum EM, Tuckerman JR, Gonzalez G, Scott WG, Gilles-Gonzalez MA (2003) A distal arginine in oxygen-sensing heme-PAS domains is essential to ligand binding, signal transduction, and structure. Biochemistry 42:7701–7708CrossRefPubMedGoogle Scholar
  13. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763CrossRefPubMedGoogle Scholar
  14. Eswar N, Eramian D, Webb B, Shen M-Y, Sali A (2008) Protein structure modeling with MODELLER. In: Structural proteomics, vol 426. Springer, p 145–159Google Scholar
  15. Fijalkowska IJ, Jonczyk P, Tkaczyk MM, Bialoskorska M, Schaaper RM (1998) Unequal fidelity of leading strand and lagging strand DNA replication on the Escherichia coli chromosome. Proc Natl Acad Sci USA 95(17): PMC21454Google Scholar
  16. Gao B, Gupta RS (2012) Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiol Mol Biol Rev 76:66–112CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gao S, Romdhane SB, Beullens S, Kaever V, Lambrichts I, Fauvart M, Michiels J (2014) Genomic analysis of cyclic-di-GMP-related genes in rhizobial type strains and functional analysis in Rhizobium etli. Appl Microbiol Biotechnol 98:4589–4602CrossRefPubMedGoogle Scholar
  18. Gilles-Gonzalez MA, Gonzalez G (2004) Signal transduction by heme-containing PAS-domain proteins. J Appl Physiol 96:774–783CrossRefPubMedGoogle Scholar
  19. Gtari M et al (2012) Contrasted resistance of stone-dwelling Geodermatophilaceae species to stresses known to give rise to reactive oxygen species. FEMS Microbiol Ecol 80:566–577CrossRefPubMedGoogle Scholar
  20. Hefti MH, Franaoijs KJ, De Vries SC, Dixon R, Vervoort J (2004) The PAS fold European. J Biochem 271:1198–1208Google Scholar
  21. Huang ZJ, Edery I, Rosbash M (1993) PAS is a dimerization domain common to Drosophila period and several transcription factors. Nature 364:259–262CrossRefPubMedGoogle Scholar
  22. Ikeda H et al (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526–531CrossRefPubMedGoogle Scholar
  23. Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34PubMedGoogle Scholar
  24. Iwamoto T, Sonobe T, Hayashi K (2003) Loop-mediated isothermal amplification for direct detection of Mycobacterium tuberculosis complex, M. avium, and M. intracellulare in sputum samples. J Clin Microbiol 41:2616–2622CrossRefPubMedPubMedCentralGoogle Scholar
  25. Jaiswal RK, Manjeera G, Gopal B (2010) Role of a PAS sensor domain in the Mycobacterium tuberculosis transcription regulator Rv1364c. Biochem Biophys Res Commun 398:342–349CrossRefPubMedPubMedCentralGoogle Scholar
  26. Jonathan T, Crosson S (2011) Ligand binding PAS domains in a genomic, cellular, and structural context. Annu Rev Microbiol 65:261–286. doi:10.1146/annurev-micro-121809-151631 CrossRefGoogle Scholar
  27. Kaplan W, Littlejohn TG (2001) Swiss-PDB viewer (deep view). Brief Bioinform 2:195–197CrossRefPubMedGoogle Scholar
  28. Kataoka M, Li H, Arakawa S, Kuramitsu H (1997) Characterization of a methyl-accepting chemotaxis protein gene, dmcA, from the oral spirochete Treponema denticola. Infect Immun 65:4011–4016PubMedPubMedCentralGoogle Scholar
  29. Kay SA (1997) PAS, present, and future: clues to the origins of circadian clocks. Science 276:753–754CrossRefPubMedGoogle Scholar
  30. Kirby R et al (2012) Draft genome sequence of the human pathogen Streptomyces somaliensis, a significant cause of actinomycetoma. J Bacteriol 194:3544–3545CrossRefPubMedPubMedCentralGoogle Scholar
  31. Konagurthu AS et al (2010) MUSTANG-MR structural sieving server: applications in protein structural analysis and crystallography. PLoS One 5, e10048CrossRefPubMedPubMedCentralGoogle Scholar
  32. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291CrossRefGoogle Scholar
  33. Marchler-Bauer A et al (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225–D229CrossRefPubMedGoogle Scholar
  34. McWilliam et al (2013) Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 41(W1):W597–W600CrossRefPubMedPubMedCentralGoogle Scholar
  35. Monot M et al (2009) Comparative genomic and phylogeographic analysis of Mycobacterium leprae. Nat Genet 41:1282–1289CrossRefPubMedGoogle Scholar
  36. Narikawa R, Okamoto S, Ikeuchi M, Ohmori M (2004) Molecular evolution of PAS domain-containing proteins of filamentous cyanobacteria through domain shuffling and domain duplication. DNA Res 11:69–81CrossRefPubMedGoogle Scholar
  37. Normand P (2006) Geodermatophilaceae fam. nov., a formal description. Int J Syst Evol Microbiol 56:2277–2278CrossRefPubMedGoogle Scholar
  38. Normand P et al (1996) Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int J Syst Bacteriol 46:1–9CrossRefPubMedGoogle Scholar
  39. Normand P et al (2012) Genome sequence of radiation-resistant Modestobacter marinus strain BC501, a representative actinobacterium that thrives on calcareous stone surfaces. J Bacteriol 194:4773–4774CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ohnishi Y et al (2008) Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J Bacteriol 190:4050–4060CrossRefPubMedPubMedCentralGoogle Scholar
  41. Paul S, Million-Weaver S, Chattopadhyay S, Sokurenko E, Merrikh H (2013) Accelerated gene evolution through replication-transcription conflicts. Nature 495:512–515CrossRefPubMedGoogle Scholar
  42. Ponting CP, Aravind L (1997) PAS: a multifunctional domain family comes to light. Curr Biol 7:R674–R677CrossRefPubMedGoogle Scholar
  43. Prasanna AN, Mehra S (2013) Comparative phylogenomics of pathogenic and non-pathogenic mycobacterium. PLoS One 8(8), e71248CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rickman L, Saldanha JW, Hunt DM, Hoar DN, Colston MJ, Millar JB, Buxton RS (2004) A two-component signal transduction system with a PAS domain-containing sensor is required for virulence of Mycobacterium tuberculosis in mice. Biochem Biophys Res Commun 314:259–267CrossRefPubMedPubMedCentralGoogle Scholar
  45. Scheu PD, Kim OB, Griesinger C, Unden G (2010) Sensing by the membrane-bound sensor kinase DcuS: exogenous versus endogenous sensing of C(4)-dicarboxylates in bacteria. Future Microbiol 5:1383–1402CrossRefPubMedGoogle Scholar
  46. Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95:5857–5864CrossRefPubMedPubMedCentralGoogle Scholar
  47. Sen A, Sur S, Bothra AK, Benson DR, Normand P, Tisa LS (2008) The implication of life style on codon usage patterns and predicted highly expressed genes for three Frankia genomes. Antonie Van Leeuwenhoek 93:335–346CrossRefPubMedGoogle Scholar
  48. Sen A, Daubin V, Abrouk D, Gifford I, Berry AM, Normand P (2014) Phylogeny of the class Actinobacteria revisited in the light of complete genomes. The orders ‘Frankiales’ and Micrococcales should be split into coherent entities: proposal of Frankiales ord. nov., Geodermatophilales ord. nov., Acidothermales ord. nov. and Nakamurellales ord. nov. Int J Syst Evol Microbiol 64:3821–3832CrossRefPubMedGoogle Scholar
  49. Shah N, Gaupp R, Moriyama H, Eskridge KM, Moriyama EN, Somerville GA (2013) Reductive evolution and the loss of PDC/PAS domains from the genus Staphylococcus. BMC Genomics 14:524CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sharp PM, Li WH (1987) The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sievers et al. (2011) Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Mol Sys Biol 7(1)Google Scholar
  52. Simm R, Morr M, Kader A, Nimtz M, Romling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53:1123–1134CrossRefPubMedGoogle Scholar
  53. Stock AM, Mottonen JM, Stock JB, Schutt CE (1989) Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature 337:745–749CrossRefPubMedGoogle Scholar
  54. Tamura T, Hayakawa M, Hatano K (1998) A new genus of the order Actinomycetales, Cryptosporangium gen. nov., with descriptions of Cryptosporangium arvum sp. nov. and Cryptosporangium japonicum sp. nov. Int J Syst Bacteriol 48(Pt 3):995–1005CrossRefPubMedGoogle Scholar
  55. Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36CrossRefPubMedPubMedCentralGoogle Scholar
  56. Taylor BL, Zhulin IB (1998) In search of higher energy: metabolism-dependent behaviour in bacteria. Mol Microbiol 28:683–690CrossRefPubMedGoogle Scholar
  57. Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:479–506PubMedPubMedCentralGoogle Scholar
  58. Thakur S, Normand P, Daubin V, Tisa LS, Sen A (2013) Contrasted evolutionary constraints on secreted and non-secreted proteomes of selected Actinobacteria. BMC Genomics 14:474CrossRefPubMedPubMedCentralGoogle Scholar
  59. Tian H, McKnight SL, Russell DW (1997) Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev 11:72–82CrossRefPubMedGoogle Scholar
  60. Tice H et al (2010) Complete genome sequence of Nakamurella multipartita type strain (Y-104) Stand. Gsenomic Sci 2:168–175Google Scholar
  61. Tsirigos A, Rigoutsos I (2005) A new computational method for the detection of horizontal gene transfer events. Nucleic Acids Res 33:922–933CrossRefPubMedPubMedCentralGoogle Scholar
  62. Wang XJ et al (2010) Genome sequence of the milbemycin-producing bacterium Streptomyces bingchenggensis. J Bacteriol 192:4526–4527CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wright F (1990) The effective number of codons used in a gene. Gene 87:23–29CrossRefPubMedGoogle Scholar
  64. Wu G, Culley DE, Zhang W (2005) Predicted highly expressed genes in the genomes of Streptomyces coelicolor and Streptomyces avermitilis and the implications for their metabolism. Microbiology 151:2175–2187CrossRefPubMedGoogle Scholar
  65. Yu CS, Lin CJ, Hwang JK (2004) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 13:1402–1406CrossRefPubMedPubMedCentralGoogle Scholar
  66. Zhang Y et al (2011) Complete genome sequences of Mycobacterium tuberculosis strains CCDC5079 and CCDC5080, which belong to the Beijing family. J Bacteriol 193:5591–5592CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Indrani Sarkar
    • 1
  • Philippe Normand
    • 2
  • Louis S. Tisa
    • 3
  • Maher Gtari
    • 4
  • Asim Bothra
    • 5
  • Arnab Sen
    • 1
  1. 1.NBU Bioinformatics Facility, Department of BotanyUniversity of North BengalSiliguriIndia
  2. 2.Université de Lyon; Université Lyon 1; CNRS, Ecologie Microbienne UMR5557; INRA, UMR1418, CedexVilleurbanneFrance
  3. 3.Department of Molecular, Cellular & Biomedical Sciences, University of New HampshireDurhamUSA
  4. 4.Laboratoire Microorganismes et Biomolécules Actives, Université de Tunis El Manar (FST) & Université de Carthage (INSAT)TunisTunisia
  5. 5.Bioinformatics Chemoinformatics Laboratory, Department of Chemistry, Raiganj University CollegeRaiganjIndia

Personalised recommendations