Skip to main content
SpringerLink
Log in

Bioconversion of pineapple pomace for xylooligosaccharide synthesis using surface display of xylanase on Escherichia coli

  • Original Article
  • Published:
Biomass Conversion and Biorefinery Aims and scope Submit manuscript

Abstract

Cell surface display of xylanase on Escherichia coli was used for the hydrolysis of hemicellulose from pineapple pomace. The feasibility of bioconversion of lignocellulosic biomass into xylooligosaccharides (XOS) was investigated. In this study, pineapple pomace was pretreated, and the hemicellulose fraction was obtained for reaction with the whole-cell biocatalyst. FESEM and FTIR analyses were used to observe morphological and compositional changes of pineapple pomace respectively after pretreatment. Factors affecting hydrolysis reaction were investigated and optimized using the Box-Behnken Design. The highest amount of reducing sugar was produced at pH 7.5, cell loading of 100 g/L wet cell weight, and temperature of 30 °C. The amount of reducing sugar produced was 2.129 mg/ml. HPLC analysis indicated that the XOS produced were xylobiose and xylotriose with a total yield of 5.4 mg/g of pineapple hemicellulose. FESEM analysis on the surface structure of pineapple pomace after the hydrolysis reaction showed clear signs of degradation by xylanase. Based on the results presented, it can be deduced that the application of cell surface display on E. coli for degradation of lignocellulosic biomass is possible and should be explored as it offers great potential for the production of XOS in industry.

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
Fig. 6

Similar content being viewed by others

Data availability

All data and materials have been provided in this manuscript.

References

  1. Rabetafika HN, Bchir B, Blecker C, Paquot M, Wathelet B (2014) Comparative study of alkaline extraction process of hemicelluloses from pear pomace. Biomass Bioenergy 61:254–264. https://doi.org/10.1016/j.biombioe.2013.12.022

    Article  Google Scholar 

  2. Board OPoMPI (2016) Maklumat Statistik Industri Nenas 2016. http://www.mpib.gov.my/penerbitan/. Accessed 25 Aug 2019

  3. Sukruansuwan V, Napathorn SC (2018) Use of agro-industrial residue from the canned pineapple industry for polyhydroxybutyrate production by Cupriavidus necator strain A-04. Biotechnol Biofuels 11(1):202. https://doi.org/10.1186/s13068-018-1207-8

    Article  Google Scholar 

  4. Samanta A, Jayapal N, Jayaram C, Roy S, Kolte A, Senani S, Sridhar M (2015) Xylooligosaccharides as prebiotics from agricultural by-products: production and applications. Bioact Carbohydrates Diet Fibre 5(1):62–71

    Article  Google Scholar 

  5. Carvalho AFA, de Oliva NP, Da Silva DF, Pastore GM (2013) Xylo-oligosaccharides from lignocellulosic materials: chemical structure, health benefits and production by chemical and enzymatic hydrolysis. Food Res Int 51(1):75–85

    Article  Google Scholar 

  6. de Freitas C, Carmona E, Brienzo M (2019) Xylooligosaccharides production process from lignocellulosic biomass and bioactive effects. Bioact Carbohydrates Diet Fibre 18:100184. https://doi.org/10.1016/j.bcdf.2019.100184

    Article  Google Scholar 

  7. Otieno DO, Ahring BK (2012) The potential for oligosaccharide production from the hemicellulose fraction of biomasses through pretreatment processes: xylooligosaccharides (XOS), arabinooligosaccharides (AOS), and mannooligosaccharides (MOS). Carbohydr Res 360:84–92. https://doi.org/10.1016/j.carres.2012.07.017

    Article  Google Scholar 

  8. Aachary AA, Prapulla SG (2011) Xylooligosaccharides (XOS) as an emerging prebiotic: microbial synthesis, utilization, structural characterization, bioactive properties, and applications. Compr Rev Food Sci Food Saf 10(1):2–16

    Article  Google Scholar 

  9. Qu W, Xue Y, Ding Q (2015) Display of fungi xylanase on Escherichia coli cell surface and use of the enzyme in xylan biodegradation. Curr Microbiol 70:1–7. https://doi.org/10.1007/s00284-015-0781-2

    Article  Google Scholar 

  10. Park TJ, Heo NS, Yim SS, Park JH, Jeong KJ, Lee SY (2013) Surface display of recombinant proteins on Escherichia coli by BclA exosporium of Bacillus anthracis. Microb Cell Factories 12(1):81. https://doi.org/10.1186/1475-2859-12-81

    Article  Google Scholar 

  11. Chen YP, Hwang IE, Lin CJ, Wang HJ, Tseng CP (2012) Enhancing the stability of xylanase from Cellulomonas fimi by cell-surface display on Escherichia coli. J Appl Microbiol 112(3):455–463. https://doi.org/10.1111/j.1365-2672.2012.05232.x

    Article  Google Scholar 

  12. Schüürmann J, Quehl P, Festel G, Jose J (2014) Bacterial whole-cell biocatalysts by surface display of enzymes: toward industrial application. Appl Microbiol Biotechnol 98(19):8031–8046. https://doi.org/10.1007/s00253-014-5897-y

    Article  Google Scholar 

  13. Lowe CR (2001) Combinatorial approaches to affinity chromatography. Curr Opin Chem Biol 5(3):248–256. https://doi.org/10.1016/S1367-5931(00)00199-X

    Article  Google Scholar 

  14. Straathof AJJ (2011) 2.57 - The proportion of downstream costs in fermentative production processes. In: Moo-Young M (ed) Comprehensive biotechnology, 2nd edn. Academic Press, Burlington, pp 811–814. https://doi.org/10.1016/B978-0-08-088504-9.00492-X

    Chapter  Google Scholar 

  15. van Bloois E, Winter RT, Kolmar H, Fraaije MW (2011) Decorating microbes: surface display of proteins on Escherichia coli. Trends Biotechnol 29(2):79–86

    Article  Google Scholar 

  16. Wee MYJ, Murad AMA, Bakar FDA, Low KO, Illias RM (2019) Expression of xylanase on Escherichia coli using a truncated ice nucleation protein of Erwinia ananas (InaA). Process Biochem 78:25–32

    Article  Google Scholar 

  17. Han JS, Rowell JS (1997) Chemical composition of fibers. Paper and composites from agro-based resources:83–134

  18. Sluiter A, Hames B, Hyman D, Payne C, Ruiz R, Scarlata C, Sluiter J, Templeton D, Wolfe J (2008) Determination of total solids in biomass and total dissolved solids in liquid process samples National Renewable Energy Laboratory 9

  19. Azelee NIW, Jahim JM, Rabu A, Murad AMA, Bakar FDA, Illias RM (2014) Efficient removal of lignin with the maintenance of hemicellulose from kenaf by two-stage pretreatment process. Carbohydr Polym 99:447–453

    Article  Google Scholar 

  20. Zulyadi NH, Saleh SH, Sarijo SH (2016) Fractionation of hemicellulose from rice straw by alkaline extraction and ethanol precipitation. Malaysian J Analytical Sci 20(2):329–334

    Article  Google Scholar 

  21. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31(3):426–428. https://doi.org/10.1021/ac60147a030

    Article  Google Scholar 

  22. Ban-Koffi L, Han Y (1990) Alcohol production from pineapple waste. World J Microbiol Biotechnol 6(3):281–284

    Article  Google Scholar 

  23. Zhao L-C, Wang Y, Lin J-F, Guo L-Q (2012) Adsorption and kinetic behavior of recombinant multifunctional xylanase in hydrolysis of pineapple stem and bagasse and their hemicellulose for Xylo-oligosaccharide production. Bioresour Technol 110:343–348. https://doi.org/10.1016/j.biortech.2012.01.076

    Article  Google Scholar 

  24. Banerjee S, Patti AF, Ranganathan V, Arora A (2019) Hemicellulose based biorefinery from pineapple peel waste: Xylan extraction and its conversion into xylooligosaccharides. Food Bioprod Process 117:38–50. https://doi.org/10.1016/j.fbp.2019.06.012

    Article  Google Scholar 

  25. Glasser WG, Kaar WE, Jain RK, Sealey JE (2000) Isolation options for non-cellulosic heteropolysaccharides (HetPS). Cellulose 7(3):299–317. https://doi.org/10.1023/A:1009277009836

    Article  Google Scholar 

  26. Peng H, Wang N, Hu Z, Yu Z, Liu Y, Zhang J, Ruan R (2012) Physicochemical characterization of hemicelluloses from bamboo (Phyllostachys pubescens Mazel) stem. Ind Crop Prod 37(1):41–50. https://doi.org/10.1016/j.indcrop.2011.11.031

    Article  Google Scholar 

  27. Xu F, Sun J, Geng Z, Liu C, Ren J, Sun R, Fowler P, Baird M (2007) Comparative study of water-soluble and alkali-soluble hemicelluloses from perennial ryegrass leaves (Lolium peree). Carbohydr Polym 67(1):56–65

    Article  Google Scholar 

  28. Rohman A, van Oosterwijk N, Puspaningsih NNT, Dijkstra BW (2018) Structural basis of product inhibition by arabinose and xylose of the thermostable GH43 β-1,4-xylosidase from Geobacillus thermoleovorans IT-08. PLoS One 13(4):e0196358. https://doi.org/10.1371/journal.pone.0196358

    Article  Google Scholar 

  29. Romsaiyud A, Songkasiri W, Nopharatana A, Chaiprasert P (2009) Combination effect of pH and acetate on enzymatic cellulose hydrolysis. J Environ Sci 21(7):965–970. https://doi.org/10.1016/S1001-0742(08)62369-4

    Article  Google Scholar 

  30. Raspe DT, Cardozo Filho L, da Silva C (2013) Effect of additives and process variables on enzymatic hydrolysis of Macauba kernel oil (Acrocomia aculeata). Int J Chem Eng 2013:1–8

    Article  Google Scholar 

  31. Goswami D, Basu JK, De S (2009) Optimization of process variables in castor oil hydrolysis by Candida rugosa lipase with buffer as dispersion medium. Biotechnol Bioprocess Eng 14(2):220–224

    Article  Google Scholar 

  32. Azelee NIW, Jahim JM, Ismail AF, Fuzi SFZM, Rahman RA, Ghazali NF, Illias RM (2016) Enzymatic hydrolysis of pretreated kenaf using a recombinant xylanase: effects of reaction conditions for optimum hemicellulose hydrolysis. Am J Agric Biol Sci 11(2):54–66

    Article  Google Scholar 

  33. Hardt N, Janssen A, Boom R, van der Goot A (2014) Factors impeding enzymatic wheat gluten hydrolysis at high solid concentrations. Biotechnol Bioeng 111(7):1304–1312

    Article  Google Scholar 

  34. Bin Abdul Wahab MKH, Bin Jonet MA, Illias RM (2016) Thermostability enhancement of xylanase Aspergillus fumigatus RT-1. J Mol Catal B Enzym 134:154–163

    Article  Google Scholar 

  35. Nasirpour N, Mousavi SM (2018) RSM based optimization of PEG assisted ionic liquid pretreatment of sugarcane bagasse for enhanced bioethanol production: effect of process parameters. Biomass Bioenergy 116:89–98

    Article  Google Scholar 

  36. Slonczewski JL, Rosen BP, Alger JR, Macnab RM (1981) pH homeostasis in Escherichia coli: measurement by 31P nuclear magnetic resonance of methylphosphonate and phosphate. Proc Natl Acad Sci 78(10):6271–6275

    Article  Google Scholar 

  37. White S, Tuttle F, Blankenhorn D, Dosch D, Slonczewski J (1992) pH dependence and gene structure of inaA in Escherichia coli. J Bacteriol 174(5):1537–1543

    Article  Google Scholar 

  38. Detzel C, Maas R, Jose J (2011) Autodisplay of nitrilase from Alcaligenes faecalis in E. coli yields a whole cell biocatalyst for the synthesis of enantiomerically pure (R)-mandelic acid. ChemCatChem 3(4):719–725

    Article  Google Scholar 

  39. Samanta A, Jayapal N, Kolte A, Senani S, Sridhar M, Mishra S, Prasad C, Suresh K (2013) Application of pigeon pea (Cajanus cajan) stalks as raw material for xylooligosaccharides production. Appl Biochem Biotechnol 169(8):2392–2404

    Article  Google Scholar 

  40. M-q L, Huo W-k XX, X-y W (2017) Recombinant Bacillus amyloliquefaciens xylanase A expressed in Pichia pastoris and generation of xylooligosaccharides from xylans and wheat bran. Int J Biol Macromol 105:656–663. https://doi.org/10.1016/j.ijbiomac.2017.07.073

    Article  Google Scholar 

  41. Chang S, Guo Y, Wu B, He B (2017) Extracellular expression of alkali tolerant xylanase from Bacillus subtilis Lucky9 in E. coli and application for xylooligosaccharides production from agro-industrial waste. Int J Biol Macromol 96:249–256

    Article  Google Scholar 

  42. Salas-Veizaga DM, Villagomez R, Linares-Pastén JA, Carrasco C, Álvarez MT, Adlercreutz P, Nordberg Karlsson E (2017) Extraction of glucuronoarabinoxylan from quinoa stalks (Chenopodium quinoa Willd.) and evaluation of xylooligosaccharides produced by GH10 and GH11 xylanases. J Agric Food Chem 65(39):8663–8673

    Article  Google Scholar 

  43. Khat-Udomkiri N, Sivamaruthi BS, Sirilun S, Lailerd N, Peerajan S, Chaiyasut C (2018) Optimization of alkaline pretreatment and enzymatic hydrolysis for the extraction of xylooligosaccharide from rice husk. AMB Express 8(1):115–115. https://doi.org/10.1186/s13568-018-0645-9

    Article  Google Scholar 

Download references

Acknowledgments

We thank Lee Pineapple Company Pte. Ltd. for providing the pineapple waste used in this study.

Funding

This work was supported by the Universiti Teknologi Malaysia [grant number Q.J130000.2409.04G21] and Malaysia Genome Institute, Ministry of Science, Technology and Innovation Malaysia [grant number FP0813B029(K2)].

Author information

Authors and Affiliations

  1. Faculty of Engineering, Department of Bioprocess Engineering, School of Chemical and Energy Engineering, Universiti Teknologi Malaysia, 81310, Skudai, Johor, Malaysia

    Mei Yuin Joanne Wee, Nur Izyan Wan Azelee, Samson Pachelles & Rosli Md Illias

  2. Faculty of Science and Technology, School of Biosciences and Biotechnology, Universiti Kebangsaan Malaysia, 43600, Bangi, Selangor, Malaysia

    Abdul Munir Abd. Murad & Farah Diba Abu Bakar

Authors
  1. Mei Yuin Joanne Wee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nur Izyan Wan Azelee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Samson Pachelles
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abdul Munir Abd. Murad
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Farah Diba Abu Bakar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rosli Md Illias
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosli Md Illias.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

All authors have agreed to the submission of this manuscript to this journal.

Code availability

Not applicable.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wee, M.Y.J., Azelee, N.I.W., Pachelles, S. et al. Bioconversion of pineapple pomace for xylooligosaccharide synthesis using surface display of xylanase on Escherichia coli. Biomass Conv. Bioref. 12, 6003–6014 (2022). https://doi.org/10.1007/s13399-020-01041-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13399-020-01041-0

Keywords

Search

Navigation