Skip to main content
SpringerLink
Log in

Comparative structural bioinformatics analysis of Bacillus amyloliquefaciens chemotaxis proteins within Bacillus subtilis group

  • Genomics, transcriptomics, proteomics
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Chemotaxis is a process in which bacteria sense their chemical environment and move towards more favorable conditions. Since plant colonization by bacteria is a multifaceted process which requires a response to the complex chemical environment, a finely tuned and sensitive chemotaxis system is needed. Members of the Bacillus subtilis group including Bacillus amyloliquefaciens are industrially important, for example, as bio-pesticides. The group exhibits plant growth-promoting characteristics, with different specificity towards certain host plants. Therefore, we hypothesize that while the principal molecular mechanisms of bacterial chemotaxis may be conserved, the bacterial chemotaxis system may need an evolutionary tweaking to adapt it to specific requirements, particularly in the process of evolution of free-living soil organisms, towards plant colonization behaviour. To date, almost nothing is known about what parts of the chemotaxis proteins are subjected to positive amino acid substitutions, involved in adjusting the chemotaxis system of bacteria during speciation. In this novel study, positively selected and purified sites of chemotaxis proteins were calculated, and these residues were mapped onto homology models that were built for the chemotaxis proteins, in an attempt to understand the spatial evolution of the chemotaxis proteins. Various positively selected amino acids were identified in semi-conserved regions of the proteins away from the known active sites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  Google Scholar 

  • Borriss R, Chen X, Rueckert C, Blom J, Becker A, Baumgarth B, Fan B, Pukall R, Schumann P, Spröer C, Junge H, Vater J, Pühler A, Klenk HP (2010) Relationship of Bacillus amyloliquefaciens clades associated with strains DSM7T and FZB42: a proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on their discriminating complete genome sequences. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.023267-0

  • Buchan A, Crombie B, Alexandre GM (2010) Temporal dynamics and genetic diversity of chemotactic-competent microbial populations in the rhizosphere. Environ Microbiol 12(12):3171–3184

    Article  CAS  Google Scholar 

  • Bunn MW, Ordal GW (2003) Transmembrane organization of the Bacillus subtilis chemoreceptor McpB deduced by cysteine disulfide crosslinking. J Mol Biol 331:941–949

    Article  CAS  Google Scholar 

  • Chao X, Muff TJ, Park S, Zhang S, Pollard AM, Ordal GW, Bilwes AM, Crane BR (2006) A receptor-modifying deamidase in complex with a signaling phosphatase reveals reciprocal regulation. Cell 124:561–571

    Article  CAS  Google Scholar 

  • Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O, Junge H, Voigt B, Jungblut PR, Vater J, Süssmuth R, Liesegang H, Strittmatter A, Gottschalk G, Borriss R (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotech 25:1007–1014

    Article  CAS  Google Scholar 

  • Chen XH, Koumoutsi A, Scholz R, Schneider K, Vater J, Süssmuth R, Piel J, Borriss R (2009) Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol 140:27–37

    Article  CAS  Google Scholar 

  • Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants—with special reference to induced. Microbiol Res 164(5):493–513

    Article  CAS  Google Scholar 

  • Chun J, Bae KS (2000) Phylogenetic analysis of Bacillus subtilis and related taxa based on partial gyrA gene sequences. Antonie van Leeuwenhoek 78:123–127

    Article  CAS  Google Scholar 

  • Djordjevic S, Stock AM (1997) Crystal structure of the chemotaxis receptor methyltransferase CheR suggests a conserved structural motif for binding S-adenosylmethionine. Structure 5:545–558

    Article  CAS  Google Scholar 

  • Djordjevic S, Goudreau PN, Xu Q, Stock AM, West AH (1998) Structural basis for methylesterase CheB regulation by a phosphorylation-activated domain. Proc Natl Acad Sci USA 95:1381–1386

    Article  CAS  Google Scholar 

  • Doron-Faigenboim A, Pupko T (2007) A combined empirical and mechanistic codon model. Mol Biol Evol 24:388–397

    Article  CAS  Google Scholar 

  • Doron-Faigenboim A, Stern A, Mayrose I, Bacharach E, Pupko T (2005) Selecton: a server for detecting evolutionary forces at a single amino-acid site. Bioinformatics 21:2101–2103

    Article  CAS  Google Scholar 

  • Edgar R (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113

    Article  Google Scholar 

  • Eisenberg D, Lüthy R, Bowie JU (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 277:396–404

    Article  CAS  Google Scholar 

  • Falke JJ, Hazelbauer GL (2001) Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26:257–265

    Article  CAS  Google Scholar 

  • Felsenstein J, Churchill GA (1996) A Hidden Markov Model approach to variation among sites in rate of evolution. Mol Biol Evol 13:93–104

    CAS  Google Scholar 

  • Fritze D (2004) Taxonomy of the genus Bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 94:1245–1248

    Article  Google Scholar 

  • Garrity LF, Ordal GW (1995) Chemotaxis in Bacillus subtilis: how bacteria monitor environmental signals. Pharmacol Ther 68:87–104

    Article  CAS  Google Scholar 

  • Garrity LF, Schiel SL, Merrill R, Reizer J, Saier MH Jr, Ordal GW (1998) Unique regulation of carbohydrate chemotaxis in Bacillus subtilis by the phosphoenolpyruvate-dependent phosphotransferase system and the methyl-accepting chemotaxis protein McpC. J Bacteriol 180:4475–4480

    CAS  Google Scholar 

  • Goldman DJ, Ordal GW (1984) In vitro methylation and demethylation of methyl-accepting chemotaxis proteins in Bacillus subtilis. Biochemistry 23:2600–2606

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hamer R, Chen P, Armitage J, Reinert G, Deane C (2010) Deciphering chemotaxis pathways using cross species comparisons. BMC Systems Biology 4:3

    Article  Google Scholar 

  • Hernández-Sánchez C, Mansilla A, de Pablo F, Zardoya R (2008) Evolution of the insulin receptor family and receptor isoform expression in vertebrates. Mol Biol Evol 25:1043–1053

    Article  Google Scholar 

  • Kirby JR, Niewold TB, Maloy S, Ordal GW (2000) CheB is required for behavioural responses to negative stimuli during chemotaxis in Bacillus subtilis. Mol Microbiol 35:44–57

    Article  CAS  Google Scholar 

  • Kirby JR, Kristich CJ, Saulmon M, Zimmer MA, Garrity L, Zhulin IB, Ordal G (2001) CheC is related to the family of flagellar switch proteins and acts independently from CheD to control chemotaxis in Bacillus subtilis. Mol Microbiol 42:573–585

    Article  CAS  Google Scholar 

  • Kristich CJ, Ordal GW (2002) Bacillus subtilis CheD is a chemoreceptor modification enzyme required for chemotaxis. J Biol Chem 277:25356–25362

    Article  CAS  Google Scholar 

  • Kristich CJ, Ordal GW (2004) Analysis of chimeric chemoreceptors in Bacillus subtilis reveals a role for CheD in the function of the McpC HAMP domain. J Bacteriol 186:5950–5955

    Article  CAS  Google Scholar 

  • Kristich CJ, Glekas GD, Ordal GW (2003) The conserved cytoplasmic module of the transmembrane chemoreceptor McpC mediates carbohydrate chemotaxis in Bacillus subtilis. Mol Microbiol 47:1353–1366

    Article  CAS  Google Scholar 

  • Lupas A, Stock J (1989) Phosphorylation of an N-terminal regulatory domain activates the CheB methylesterase in bacterial chemotaxis. J Biol Chem 264:17337–17342

    CAS  Google Scholar 

  • Lux R, Munasinghe VRN, Castellano F, Lengeler JW, Corrie JET, Khan S (1999) Elucidation of a PTS-carbohydrate chemotactic signal pathway in Escherichia coli using a time-resolved behavioral assay. Mol Biol Cell 10:1133–1146

    CAS  Google Scholar 

  • Manson MD, Armitage JP, Hoch JA, Macnab RM (1998) Bacterial locomotion and signal transduction. J Bacteriol 180:1009–1022

    CAS  Google Scholar 

  • Mowbray SL, Sandgren MOJ (1998) Chemotaxis receptors: a progress report on structure and function. J Struct Biol 124:257–275

    Article  CAS  Google Scholar 

  • Muff TJ, Ordal GW (2007) The CheC phosphatase regulates chemotactic adaptation through CheD. J Biol Chem 282:34120–34128

    Article  CAS  Google Scholar 

  • Park S, Chao X, Gonzalez-Bonet G, Beel BD, Bilwes AM, Crane BR (2004a) Structure and function of an unusual family of protein phosphatases: the bacterial chemotaxis proteins CheC and CheX. Mol Cell 16:563–574

    CAS  Google Scholar 

  • Park S, Beel BD, Simon MI, Bilwes AM, Crane BR (2004b) In different organisms, the mode of interaction between two signaling proteins is not necessarily conserved. Proc Natl Acad Sci USA 101:11646–11651

    Article  CAS  Google Scholar 

  • Park S, Borbat PP, Gonzalez-Bonet G, Bhatnagar J, Pollard AM, Freed JH, Bilwes AM, Crane BR (2006) Reconstruction of the chemotaxis receptor-kinase assembly. Nat Struct Mol Biol 13:400–407

    Article  CAS  Google Scholar 

  • Pawlowski M, Gajda M, Matlak R, Bujnicki J (2008) MetaMQAP: a meta-server for the quality assessment of protein models. BMC Bioinformatics 9:403

    Article  Google Scholar 

  • Pazy Y, Motaleb MA, Guarnieri MT, Charon NW, Zhao R, Silversmith RE (2010) Identical phosphatase mechanisms achieved through distinct modes of binding phosphoprotein substrate. Proc Natl Acad Sci USA 107:1924–1929

    Article  CAS  Google Scholar 

  • Pei J, Kim B, Grishin NV (2008) PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucl Acids Res 36:2295–2300

    Article  CAS  Google Scholar 

  • Rao CV, Kirby JR, Arkin AP (2004) Design and diversity in bacterial chemotaxis: a comparative study in Escherichia coli and Bacillus subtilis. PLoS Biol 2:e49

    Article  Google Scholar 

  • Rao CV, Glekas GD, Ordal GW (2008) The three adaptation systems of Bacillus subtilis chemotaxis. Trends Microbiol 16:480–487

    Article  CAS  Google Scholar 

  • Reva ON, Dixelius C, Meijer J, Priest FG (2004) Taxonomic characterization and plant colonizing abilities of some bacteria related to Bacillus amyloliquefaciens and Bacillus subtilis. FEMS Microbiol Ecol 48:249–259

    Article  CAS  Google Scholar 

  • Rosario MM, Fredrick KL, Ordal GW, Helmann JD (1994) Chemotaxis in Bacillus subtilis requires either of two functionally redundant CheW homologs. J Bacteriol 176:2736–2739

    CAS  Google Scholar 

  • Rosario MML, Kirby JR, Bochar DA, Ordal GW (1995) Chemotactic methylation and behavior in Bacillus subtilis: role of two unique proteins, CheC and CheD. Biochemistry 34:3823–3831

    Article  CAS  Google Scholar 

  • Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779–815

    Article  CAS  Google Scholar 

  • Saulmon MM, Karatan E, Ordal GW (2004) Effect of loss of CheC and other adaptational proteins on chemotactic behaviour in Bacillus subtilis. Microbiology 150:581–589

    Article  CAS  Google Scholar 

  • Shen M, Sali A (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci 15:2507–2524

    Article  CAS  Google Scholar 

  • Soding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucl Acids Res 33:W244–W248

    Article  Google Scholar 

  • Tastan Bishop O, Kroon M (2011) Study of protein complexes via homology modeling, applied to cysteine proteases and their protein inhibitors. J Mol Model. doi:10.1007/s00894-011-0990-y

  • Usher KC, De La Cruz AFA, Dahlquist FW, James Remington S, Swanson RV, Simon MI (1998) Crystal structures of CheY from Thermotoga maritima do not support conventional explanations for the structural basis of enhanced thermostability. Protein Sci 7:403–412

    Article  CAS  Google Scholar 

  • Van de Broek A, Lambrecht M, Vanderleyden J (1998) Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144:2599–2606

    Article  Google Scholar 

  • Wallner B, Elofsson A (2003) Can correct protein models be identified? Protein Sci 12:1073–1086

    Article  CAS  Google Scholar 

  • Yao J, Allen C (2006) Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum. J Bacteriol 188:3697–3708

    Article  CAS  Google Scholar 

  • Yao W, Shi L, Liang D (2007) Crystal structure of scaffolding protein CheW from Thermoanaerobacter tengcongensis. Biochem Biophys Res Commun 361:1027–1032

    Article  Google Scholar 

  • Zhang W, Phillips GN (2003) Structure of the oxygen sensor in Bacillus subtilis: signal transduction of chemotaxis by control of symmetry. Structure 11:1097–1110

    Article  CAS  Google Scholar 

  • Zimmer MA, Tiu J, Collins MA, Ordal GW (2000) Selective methylation changes on the Bacillus subtilis chemotaxis receptor McpB promote adaptation. J Biol Chem 275:24264–24272

    Article  CAS  Google Scholar 

  • Zimmer MA, Szurmant H, Saulmon MM, Collins MA, Bant JS, Ordal GW (2002) The role of heterologous receptors in McpB-mediated signalling in Bacillus subtilis chemotaxis. Mol Microbiol 45:555–568

    Article  CAS  Google Scholar 

Download references

Acknowledgements

AY thanks Rhodes University and National Research Foundation (NRF) of South Africa for financial support, OR's work was funded by the NRF grant 71261. We thank Prof. R. Borriss (Humboldt University, Berlin) for providing us with newly sequenced B. amyloliquefaciens genomes. We also thank Prof. N. Bishop and Dr. T. Bray for kindly proofreading the manuscript. AY and OTB started this work at the Bioinformatics and Computational Biology Unit, University of Pretoria; then continued at Rhodes University, Grahamstown.

Author information

Authors and Affiliations

  1. Department of Biochemistry, Microbiology and Biotechnology, Rhodes University Bioinformatics (RUBi), Rhodes University, Grahamstown, 6140, South Africa

    Anna Yssel & Ozlem Tastan Bishop

  2. Department of Biochemistry, Bioinformatics and Computational Biology Unit, University of Pretoria, Pretoria, 0002, South Africa

    Oleg Reva

Authors
  1. Anna Yssel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Oleg Reva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ozlem Tastan Bishop
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ozlem Tastan Bishop.

Electronic Supplementary Materials

Below is the link to the electronic supplementary material.

ESM 1

(PDF 175 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yssel, A., Reva, O. & Tastan Bishop, O. Comparative structural bioinformatics analysis of Bacillus amyloliquefaciens chemotaxis proteins within Bacillus subtilis group. Appl Microbiol Biotechnol 92, 997–1008 (2011). https://doi.org/10.1007/s00253-011-3582-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3582-y

Keywords

Search

Navigation