SpringerLink
Log in

Expression and characterization of a novel endo-1,4-β-xylanase produced by Streptomyces griseorubens JSD-1 isolated from compost-treated soil

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

Abstract

Streptomyces griseorubens JSD-1 is an isolate sourced from compost-treated soil that can utilize xylan as the unique carbon source for growth; xylanlytic genes related to this process were expected to be crucial. However, little is known about the genetic basic of utilizing xylan in this isolate. To further investigate the molecular mechanism of xylan metabolism, genome sequencing was carried out. The draft genome obtained has been deposited with GenBank. Endo-1,4-β-xylanase (Xyn) was acquired, followed by characterization of its cellular localization and expression profiles. Xyn proved to be a novel enzyme, differing from xylanases from similar species according to combined analyses from multiple sequence alignments and putative three-dimensional structure modeling. Moreover, recombinant expression was optimized in heterogeneous hosts to further determine optimum pH and temperature conditions as well as residual activity in the presence of metal ions and inhibitors. Finally, substrate specificity and kinetic parameters were also studied. In conclusion, our findings illustrate the genetic background related to xylan metabolism in this isolate. In addition, a novel Xyn that is expected to have potential in the bio-degradation of hemicellulosic materials was expressed, purified and characterized.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

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

    Article  CAS  PubMed  Google Scholar 

  • Amore A, Pepe O, Ventorino V, Birolo L, Giangrande C, Faraco V (2010) Cloning and recombinant expression of a cellulase from the cellulolytic strain Streptomyces sp. G12 isolated from compost. Microb Cell Fact 11:164

    Article  Google Scholar 

  • Bentley SD, Chater KF, Cerdeño-Tárraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O’Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147

    Article  PubMed  Google Scholar 

  • Berens S, Kaspari H, Klemme JH (1996) Purification and characterization of two different xylanases from the thermophilic actinomycete Microtetraspora flexuosa SIIX. Antonie Van Leeuwenhoek 69:235–241

    Article  CAS  PubMed  Google Scholar 

  • Bienfait B, Ertl P (2013) JSME: a free molecule editor in JavaScript. J Cheminform 5(24):363–371

    Google Scholar 

  • Chi WJ, Lim JH, Park DY, Park JS, Hong SK (2013) Production and characterization of a thermostable endo-type β-xylanase produced by a newly-isolated Streptomyces thermocarboxydus subspecies MW8 strain Jeju Island. Process Biochem 48:1736–1743

    Article  CAS  Google Scholar 

  • Collins T, Gerday C, Feller G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 29:3–23

    Article  CAS  PubMed  Google Scholar 

  • Ding CH, Jiang ZQ, Li XT, Li LT, Kusakabe (2004) High activity xylanase production by Streptomyces olivaceoviridis E-86. World J Microbiol Biotechnol 20:7–10

    Article  CAS  Google Scholar 

  • Dube E, Shareck F, Hurtubise Y, Daneault C, Beauregard M (2008) Homologous cloning, expression, and characterisation of a laccase from Streptomyces coelicolor and enzymatic decolourisation of an indigo dye. Appl Microbiol Biotechnol 79:597–603

    Article  CAS  PubMed  Google Scholar 

  • Eiben S, Bartelmas H, Urlacher VB (2007) Construction of a thermostable cytochrome P450 chimera derived self-sufficient mesophilic parents. Appl Microbiol Biotechnol 75:1055–1061

    Article  CAS  PubMed  Google Scholar 

  • Feng H, Zhi YE, Shi WW, Mao L, Zhou P (2013) Isolation, identification and characterization of a straw degrading Streptomyces griseorubens JSD-1. Afr J Microbiol Res 7:2730–2735

    Google Scholar 

  • Feng H, Zhi Y, Sun Y, Wei X, Luo Y, Zhou P (2014) Draft genome sequence of a novel Streptomyces griseorubens strain JSD-1, active in carbon and nitrogen recycling. Genome Announc 2(4):e00650–14

  • Garcia-Fruitos E, Vazquez E, Diez-Gil C, Corchero JL, Seras-Franzoso J, Ratera I, Veciana J, Villaverde A, Veciana J (2012) Bacterial inclusion bodies: making gold from waste. Trends Biotechnol 30:65–70

    Article  CAS  PubMed  Google Scholar 

  • George SP, Ahmad A, Rao MB (2001) Studies on carboxymethyl cellulase produced by an alkalothermophilic actinomycete. Bioresour Technol 77:171–175

    Article  CAS  PubMed  Google Scholar 

  • Godden B, Ball AS, Helvensteian P, McCarthy A, Penninckx MJ (1992) Towards elucidation of the lignin degradation pathway in actinomycetes. J Gen Microbiol 138:2441–2448

    Article  CAS  Google Scholar 

  • Han J, Choi Y, Kim W, Jeon YH, Lee SK, Lee B, Ryu K (2010) Condon optimization enhances protein expression of human peptide deformylase in E. coli. Protein Expres Purif 70:224–230

    Article  CAS  Google Scholar 

  • Han X, Li M, Ding Z, Zhao J, Ji K, Wen M, Lu T (2012) Genome sequence of Streptomyces auratus strain AGR0001, a phoslactomycin-producing actinomycete. J Bacteriol 194:5472–5473

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hendriks ATWM, Zeeman G (2009) Pretreatments to enhance the digestibility of lignocellulosic biomass. Bioresour Technol 100:10–18

    Article  CAS  PubMed  Google Scholar 

  • Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526–531

    Article  PubMed  Google Scholar 

  • Juturu V, Wu JC (2014) Microbial cellulases: engineering, production and applications. Renew Sust Energ Rev 33:188–203

    Article  CAS  Google Scholar 

  • Kelley LA, Sternberg MJE (2009) Protein structure prediction on the web: a case study using the Phyre server. Nat Protoc 4:363–371

    Article  CAS  PubMed  Google Scholar 

  • Kim DY, Ham SJ, Kim HJ, Kim J, Lee MH, Cho HY, Shin DH, Rhee YH, Son KH, Park HY (2012) Novel modular endo-β-1,4-xylanase with transglycosylation activity from Cellulosimicrobium sp. strain HY-13 that is homologous to inverting GH family 6 enzymes. Bioresour Technol 107:25–32

    Article  CAS  PubMed  Google Scholar 

  • Knob A, Terrasan C, Carmona (2010) β-Xylosidases from filamentous fungi: an overview. World J Microbiol Biotechnol 26:389–407

    Article  CAS  Google Scholar 

  • Leskinen S, Mantyla A, Fagerstrom R, Vehmaanpera J, Lantto R, Paloheimo M (2005) Thermostable xylanases, Xyn10A and Xyn11A, from the actinomycete Nonomuraea flexuosa: isolation of the genes and characterization of recombinant Xyn11A polypeptides produced in Trichoderma reesei. Appl Microbiol Biotechnol 67:495–505

    Article  CAS  PubMed  Google Scholar 

  • Li X, She Y, Sun B, Song H, Zhu Y, Lv Y, Song H (2010) Purification and characterization of a cellulase-free, thermostable xylanase from Streptomyces rameus L2001 and its biobleaching effect on wheat straw pulp. Biochem Eng J 52:71–78

    Article  CAS  Google Scholar 

  • Li XJ, Zheng RC, Wu ZM, Ding X, Zheng YG (2014) Thermophilic esterase from Thermomyces lanuginosus: molecular cloning, functional expression and biochemical characterization. Protein Expres Purif 101:1–7

    Article  Google Scholar 

  • Lichty JJ, Malecki JL, Agnew HD, Michelson-Horowitz DJ, Tan S (2005) Comparison of affinity tags for protein purification. Protein Expres Purif 41:98–105

    Article  CAS  Google Scholar 

  • Mamo G, Hatti-Kaul R, Mattiasson B (2006) A thermostable alkaline active endo-β-1-4-xylanase from Bacillus halodurans S7: purification and characterization. Enzyme Microb Technol 39:1492–1498

    Article  CAS  Google Scholar 

  • Mandal A, Kar S, Mohapatra PKD, Maity C, Pati BR, Mondal KC (2012) Regulation of xylanase biosynthesis in Bacillus cereus BSA1. Appl Biochem Biotechnol 167:1052–1060

    Article  CAS  PubMed  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Biochem 31:426–428

    CAS  Google Scholar 

  • Myronovskyi M, Tokovenko B, Manderscheid N, Petzke L, Luzhetskyy A (2013) Complete genome sequence of Streptomyces fulvissimus. J Biotechnol 168:117–118

    Article  CAS  PubMed  Google Scholar 

  • Nascimento RP, Coelho RRR, Marques S, Alves L, Gírio FM, Bon EPS, Amaral-Collaco MT (2002) Production and partial characterisation of xylanase from Streptomyces sp. strain AMT-3 isolated from Brazilian cerrado soil. Enzyme Microb Technol 31:549–555

  • Ninawe S, Kuhad RC (2005) Use of xylan-rich cost effective agro-residues in the production of xylanase by Streptomyces cyaneus SN32. J Appl Microbiol 99:1141–1148

    Article  CAS  PubMed  Google Scholar 

  • Ohnishi Y, Ishikawa J, Hara H, Suzuki H, Ikenoya M, Ikeda H, Yamashita A, Hat-tori M, Horinouchi S (2008) Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J Bacteriol 190:4050–4060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pagano M (1999) Application of electrophoresis and related methods, such as western blotting and zymography to the study of some proteins and enzymes. Anal Chim Acta 383:119–125

    Article  CAS  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) Signal 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  CAS  PubMed  Google Scholar 

  • Qing Q, Wyman CE (2011) Hydrolysis of different chain length xylooliogmers by cellulase and hemicellulase. Bioresour Technol 102:1359–1366

    Article  CAS  PubMed  Google Scholar 

  • Rahman MA, Choi YH, Pradeep GC, Choi YS, Choi EJ, Cho SS, Yoo JC (2014) A novel low molecular weigh endo-xylanase from Streptomyces sp. CS628 cultivated in wheat bran. Appl Biochem Biotechnol 173:1469–1480

    Article  CAS  PubMed  Google Scholar 

  • Raina S, Missiakas D (1997) Making and breaking disulfide bonds. Annu Rev Microbiol 51:179–202

    Article  CAS  PubMed  Google Scholar 

  • Rietsch A, Belin D, Martin N, Beckwith J (1996) An in vivo pathway for disulfide bond isomerization in Escherichia coli. Proc Natl Acad Sci USA 93:13048–13053

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shi QQ, Sun J, Yu HL, Li CX, Bao J, Xu JH (2011) Catalytic performance of corn stover hydrolysis by a new isolate Penicillium sp. ECU0913 producing both cellulase and xylanase. Appl Biochem Biotechnol 164:816–830

    Article  Google Scholar 

  • Sriyapai T, Somyoosap P, Matsui K, Kawai F, Chansiri K (2011) Cloning of a thermostable xylanase from Actinomadura sp. S14 and its expression in Escherichia coli and Pichia pastoris. J Biosci Bioeng 111:528–536

    Article  CAS  PubMed  Google Scholar 

  • Subramaniyan S, Prema P (2012) Biotechnology of microbial xylanases: enzymology, molecular biology, and application. Degradation of xylan to d-xylose by recombinant Saccharomyces cerevisiae coexpressing the Aspergillus niger beta-xylosidase (xlnD) and the Trichoderma reesei xylanase II (Xyn2) genes. Crit Rev Biotechnol 22:33–64

    Article  Google Scholar 

  • van Zyl WH, La Grange DC, Pretorius IS, Claeyssens M (2001) Degradation of xylan to d-xylose by recombinant Saccharomyces cerevisiae coexpressing the Aspergillus niger-Xylosidase (xlnD) and the Trichoderma reesei xylanase II (Xyn2) genes. Appl Environ Microbiol 67:5512–5519

    Article  PubMed Central  PubMed  Google Scholar 

  • Walia A, Mehta P, Chauhan A, Kulshrestha S, Shirkot CK (2014) Purification and characterization of cellulase-free low molecular weight endo β-1,4 xylanase from an alkalophilic Cellulosimicrobium cellulans CKMX1 isolated from mushroom compost. World J Microbiol Biotechnol 30:2597–2608

    Article  CAS  PubMed  Google Scholar 

  • Wong KKY, Tan LUL, Saddler JN (1988) Multiplicity of β-1,4-xylanase in microorganisms: functions and applications. Microbiol Rev 52:305–317

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wyman CE, Dale BE, Elander RT, Holtzapple M, Ladisch MR, Lee YY (2005) Coordinated development of leading biomass pretreatment technologies. Bioresour Technol 96:1959–1966

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the National High Technology Research and Development Program of China (2012AA101405), Special Fund for Agro-scientific Research in the Public Interest of China (200903056), the National Natural Science Foundation of China (31201682), the National Natural Science Foundation of China (20977062) and the Municipal Natural Science Foundation of Shanghai, China (13ZR1421700). We are also grateful for the sequencing service provided by Personal Biotechnology Co., Ltd. Shanghai, China.

Author information

Authors and Affiliations

  1. School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240, China

    Haiwei Feng, Yu**g Sun, Yuee Zhi, Liang Mao, Yanqing Luo, Lurong Xu, Lumei Wang & Pei Zhou

  2. Key Laboratory of Urban Agriculture (South), Ministry of Agriculture, Shanghai Jiao Tong University, Shanghai, 200240, China

    Haiwei Feng, Yuee Zhi, Liang Mao, Yanqing Luo, Lurong Xu, Lumei Wang & Pei Zhou

  3. Bor S. Luh Food Safety Research Center, Shanghai Jiao Tong University, Shanghai, 200240, China

    Haiwei Feng, Yuee Zhi, Liang Mao, Yanqing Luo, Lurong Xu, Lumei Wang & Pei Zhou

Authors
  1. Haiwei Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu**g Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuee Zhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Liang Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanqing Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lurong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lumei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Pei Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pei Zhou.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Feng, H., Sun, Y., Zhi, Y. et al. Expression and characterization of a novel endo-1,4-β-xylanase produced by Streptomyces griseorubens JSD-1 isolated from compost-treated soil. Ann Microbiol 65, 1771–1779 (2015). https://doi.org/10.1007/s13213-014-1016-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-014-1016-7

Keywords

Search

Navigation