Skip to main content
SpringerLink
Log in

Tandem mass tag-based quantitative proteomics analyses reveal the response of Bacillus licheniformis to high growth temperatures

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

As the optimal growth temperature of Bacillus licheniformis is relatively higher than many other industrial bacteria, its use for industrial production can reduce contamination and minimize cooling and product recovery costs during fermentation processes. However, little is known about the thermotolerance of this important bacterial species. To investigate the underlying mechanism, strains B. licheniformis ATCC 14580 and B186 were cultivated at their own optimal growth temperature (42 °C and 50 °C) and higher temperature (60 °C), respectively, and tandem mass tags (TMT)-based quantitative proteome analysis and bioinformatics tools were employed to identify differentially expressed proteins. A total of 21 differential proteins were identified and shown to participate in a wide range of biological processes, including protein refolding, amino acid and fatty acid metabolism, etc. Hence, the ability of B. licheniformis to exhibit optimal growth at high temperatures may depend on invoking its intrinsic “heat-against” proteomic mechanism for long-term viability. Our results may assist the genetic improvement of industrial strains of this important Bacillus specie.

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. 2a,b
Fig. 3a,b
Fig. 4a–c

Similar content being viewed by others

References

  • Arentson BW, Sanyal N, Becker DF (2012) Substrate channeling in proline metabolism. Front Biosci (Landmark Ed) 17:375–388

    Article  CAS  Google Scholar 

  • Baldin C, Valiante V, Krüger T, Schafferer L, Haas H, Kniemeyer O, Brakhage AA (2015) Comparative proteomics of a tor inducible Aspergillus fumigatus mutant reveals involvement of the tor kinase in iron regulation. Proteomics 15:2230–2243

    Article  CAS  PubMed  Google Scholar 

  • Battesti A, Bouveret E (2006) Acyl carrier protein/SpoT interaction, the switch linking SpoT-dependent stress response to fatty acid metabolism. Mol Microbiol 62:1048–1063

    Article  CAS  PubMed  Google Scholar 

  • Blaby IK, Lyons BJ, Wroclawska-Hughes E, Phillips GC, Pyle TP, Chamberlin SG, Benner SA, Lyons TJ, de Crécy-Lagard V, de Crécy E (2012) Experimental evolution of a facultative thermophile from a mesophilic ancestor. Appl Environ Microbiol 78:144–155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Byers DM, Gong H (2007) Acyl carrier protein: structure-function relationships in a conserved multifunctional protein family. Biochem Cell Biol 85:649–662

    Article  CAS  PubMed  Google Scholar 

  • Carroll TM, Setlow P (2005) Site-directed mutagenesis and structural studies suggest that the germination protease, GPR, in spores of Bacillus species is an atypical aspartic acid protease. J Bacteriol 187:7119–7125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan DI, Vogel HJ (2010) Current understanding of fatty acid biosynthesis and the acyl carrier protein. Biochem J 430:1–19

    Article  CAS  PubMed  Google Scholar 

  • De Lay NR, Cronan JE (2007) In vivo functional analyses of the type II acyl carrier proteins of fatty acid biosynthesis. J Biol Chem 282:20319–20328

    Article  CAS  PubMed  Google Scholar 

  • Foley S, Stolarczyk E, Mouni F, Brassart C, Vidal O, Aissi E, Bouquelet S, Krzewinski F (2008) Characterisation of glutamine fructose-6-phosphate amidotransferase (EC 2.6.1.16) and N-acetylglucosamine metabolism in Bifidobacterium. Arch Microbiol 189:157–167

    Article  CAS  PubMed  Google Scholar 

  • Gomes DF, da Silva Batista JS, Schiavon AL, Andrade DS, Hungria M (2012) Proteomic profiling of Rhizobium tropici PRF 81: identification of conserved and specific responses to heat stress. BMC Microbiol 12:84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerzoni ME, Lanciotti R, Cocconcelli PS (2001) Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiology 147:2255–2264

    Article  CAS  PubMed  Google Scholar 

  • Heidrich C, Templin MF, Ursinus A, Merdanovic M, Berger J, Schwarz H, de Pedro MA, Holtje JV (2001) Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol Microbiol 41:167–178

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann T, Bremer E (2011) Protection of Bacillus subtilis against cold stress via compatible-solute acquisition. J Bacteriol 193:1552–1562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horwich AL, Fenton WA, Chapman E, Farr GW (2007) Two families of chaperonin: physiology and mechanism. Annu Rev Cell Dev Biol 23:115–145

    Article  CAS  PubMed  Google Scholar 

  • Kawai Y, Ogasawara N (2006) Bacillus subtilis EzrA and FtsL synergistically regulate FtsZ ring dynamics during cell division. Microbiology 152:1129–1141

    Article  CAS  PubMed  Google Scholar 

  • Kerff F, Petrella S, Mercier F, Sauvage E, Herman R, Pennartz A, Zervosen A, Luxen A, Frere JM, Joris B, Charlier P (2010) Specific structural features of the N-acetylmuramoyl-l-alanine amidase AmiD from Escherichia coli and mechanistic implications for enzymes of this family. J Mol Biol 397:249–259

    Article  CAS  PubMed  Google Scholar 

  • Knap I, Lund B, Kehlet AB, Hofacre C, Mathis G (2010) Bacillus licheniformis prevents necrotic enteritis in broiler chickens. Avian Dis 54:931–935

    Article  CAS  PubMed  Google Scholar 

  • LaRossa R, Dyk T (1991) Physiological roles of the DnaK and GroE stress proteins: catalysts of protein folding or macromolecular sponges? Mol Microbiol 5:529–534

    Article  CAS  PubMed  Google Scholar 

  • Levin PA, Kurtser IG, Grossman AD (1999) Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. Proc Natl Acad Sci USA 96:9642–9647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Buchner J (2013) Structure, function and regulation of the hsp90 machinery. Biomed J 36:106–117

    Article  PubMed  Google Scholar 

  • Lo HF, Chen BE, Lin MG, Chi MC, Wang TF, Lin LL (2016) Gene expression and molecular characterization of a chaperone protein HtpG from Bacillus licheniformis. Int J Biol Macromol 85:179–191

    Article  CAS  PubMed  Google Scholar 

  • Majerus PW, Vagelos PR (1967) Fatty acid biosynthesis and the role of the acyl carrier protein. Adv Lipid Res 5:1–33

    Article  CAS  PubMed  Google Scholar 

  • Nielsen AK, Breüner A, Krzystanek M, Andersen JT, Poulsen TA, Olsen PB, Mijakovic I, Rasmussen MD (2010) Global transcriptional analysis of Bacillus licheniformis reveals an overlap between heat shock and iron limitation stimulon. J Mol Microbiol Biotechnol 18:162–173

    Article  CAS  PubMed  Google Scholar 

  • Niu D, Zuo Z, Shi GY, Wang ZX (2009) High yield recombinant thermostable α-amylase production using an improved Bacillus licheniformis system. Microb Cell Factories 8:611–631

    Article  Google Scholar 

  • Page R, Nelson MS, von Delft F, Elsliger MA, Canaves JM, Brinen LS, Dai X, Deacon AM, Floyd R, Godzik A, Grittini C, Grzechnik SK, Jaroszewski L, Klock HE, Koesema E, Kovarik JS, Kreusch A, Kuhn P, Lesley SA, McMullan D, McPhillips TM, Miller MD, Morse A, Moy K, Ouyang J, Robb A, Rodrigues K, Schwarzenbacher R, Spraggon G, Stevens RC, van den Bedem H, Velasquez J, Vincent J, Wang X, West B, Wolf G, Hodgson KO, Wooley J, Wilson IA (2004) Crystal structure of gamma-glutamyl phosphate reductase (TM0293) from Thermotoga maritima at 2.0 a resolution. Proteins 54:157–161

    Article  CAS  PubMed  Google Scholar 

  • Pagel O, Loroch S, Sickmann A, Zahedi RP (2015) Current strategies and findings in clinically relevant post-translational modification-specific proteomics. Expert Rev Proteomics 12:235–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papsdorf K, Richter K (2014) Protein folding, misfolding and quality control: the role of molecular chaperones. Essays Biochem 56:53–68

    Article  PubMed  Google Scholar 

  • Rey MW, Ramaiya P, Nelson BA, Brody-Karpin SD, Zaretsky EJ, Tang M, de Leon AL, Xiang H, Gusti V, Clausen IG (2004) Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillus species. Genome Biol 5:1

    Article  Google Scholar 

  • Schallmey M, Singh A, Ward OP (2004) Developments in the use of Bacillus species for industrial production. Can J Microbiol 50:1–17

    Article  CAS  PubMed  Google Scholar 

  • Schneider R, Lockatell CV, Johnson D, Belas R (2002) Detection and mutation of a luxS-encoded autoinducer in Proteus mirabilis. Microbiology (Reading, England) 148:773–782

    Article  CAS  Google Scholar 

  • Schroeter R, Voigt B, Jürgen B, Methling K, Pöther DC, Schäfer H, Albrecht D, Mostertz J, Mäder U, Evers S (2011) The peroxide stress response of Bacillus licheniformis. Proteomics 11:2851–2866

    Article  CAS  PubMed  Google Scholar 

  • Schroeter R, Hoffmann T, Voigt B, Meyer H, Bleisteiner M, Muntel J, Jürgen B, Albrecht D, Becher D, Lalk M (2013) Stress responses of the industrial workhorse Bacillus licheniformis to osmotic challenges. PLoS One 8:e80956

    Article  PubMed  PubMed Central  Google Scholar 

  • Sola-Penna M, Meyer-Fernandes JR (1998) Stabilization against thermal inactivation promoted by sugars on enzyme structure and function: why is trehalose more effective than other sugars? Arch Biochem Biophys 360:10–14

    Article  CAS  PubMed  Google Scholar 

  • Stankowska D, Czerwonka G, Rozalska S, Grosicka M, Dziadek J, Kaca W (2012) Influence of quorum sensing signal molecules on biofilm formation in Proteus mirabilis O18. Folia Microbiol 57:53–60

    Article  CAS  Google Scholar 

  • Storey KB, Storey JM (2011) Heat shock proteins and hypometabolism: adaptive strategy for proteome preservation. Res Rep Biol 2:57–68

    Article  CAS  Google Scholar 

  • Theodoraki MA, Caplan AJ (2012) Quality control and fate determination of Hsp90 client proteins. Biochim Biophys Acta 1823:683–688

    Article  CAS  PubMed  Google Scholar 

  • Veith B, Herzberg C, Steckel S, Feesche J, Maurer KH, Ehrenreich P, Bäumer S, Henne A, Liesegang H, Merkl R (2004) The complete genome sequence of Bacillus licheniformis DSM13, an organism with great industrial potential. J Mol Microbiol Biotechnol 7:204–211

    Article  CAS  PubMed  Google Scholar 

  • Voigt B, Schroeter R, Jürgen B, Albrecht D, Evers S, Bongaerts J, Maurer KH, Schweder T, Hecker M (2013) The response of Bacillus licheniformis to heat and ethanol stress and the role of the SigB regulon. Proteomics 13:2140–2161

    Article  CAS  PubMed  Google Scholar 

  • Voigt B, Schroeter R, Schweder T, Jurgen B, Albrecht D, van Dijl JM, Maurer KH, Hecker M (2014) A proteomic view of cell physiology of the industrial workhorse Bacillus licheniformis. J Biotechnol 191:139–149

    Article  CAS  PubMed  Google Scholar 

  • Xiao Y, Francke C, Abee T, Wells-Bennik MHJ (2011) Clostridial spore germination versus bacilli: genome mining and current insights. Food Microbiol 28:266–274

    Article  PubMed  Google Scholar 

  • Ye Y, Zhang L, Hao F, Zhang J, Wang Y, Tang H (2012) Global metabolomic responses of Escherichia coli to heat stress. J Proteome Res 11:2559–2566

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This project was financially supported by the National Natural Science Foundation of China (Grant No. 31370076), the International Collaborative Project Supported by National Natural Science Foundation of China (NSFC) and National Research Foundation of South Africa (NFC) (Grant No. 31461143026), and the Youth Innovation Fund from Tianjin University of Science & Technology (Grant No. 2016LG15).

Author information

Authors and Affiliations

  1. College of Chemical Engineering and Materials Science, Tianjin University of Science and Technology, No. 29, 13th Avenue, Tianjin Economic-technological Development Area, Tianjin, 300457, China

    Zixing Dong, Kangming Tian, Peng Jin, Xiaoguang Liu & Zhengxiang Wang

  2. Key Laboratory of Industrial Fermentation Microbiology, Ministry of Education, College of Biotechnology, Tianjin University of Science and Technology, Tianjin, 300457, China

    Zhixin Chen, Hongbin Wang & Zhengxiang Wang

  3. Department of Biotechnology and Food Technology, Faculty of Applied Sciences, Durban University of Technology, Durban, 4001, South Africa

    Nokuthula Peace Mchunu, Kugenthiren Permaul & Suren Singh

  4. College of Biological Science and Technology, Fuzhou University, Fuzhou, 350116, China

    Dandan Niu

Authors
  1. Zixing Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhixin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hongbin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kangming Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peng Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaoguang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nokuthula Peace Mchunu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kugenthiren Permaul
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Suren Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Dandan Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Zhengxiang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhengxiang Wang.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dong, Z., Chen, Z., Wang, H. et al. Tandem mass tag-based quantitative proteomics analyses reveal the response of Bacillus licheniformis to high growth temperatures. Ann Microbiol 67, 501–510 (2017). https://doi.org/10.1007/s13213-017-1279-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-017-1279-x

Keywords

Search

Navigation