Thanks to visit codestin.com
Credit goes to link.springer.com

Skip to main content
Springer Nature Link
Log in

Comprehensive analysis of the cellulolytic system reveals its potential for deconstruction of lignocellulosic biomass in a novel Streptomyces sp.

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The giant snail Achatina fulica is considered an invasive species in most territories in which it was introduced, due to its ability to process a large amount of lignocellulose as a consequence of the presence of a cellulolytic-associated microflora. Streptomyces are well known as crucial agents in the decomposition of complex polymers in soil environments and also as cellulolytic symbionts commonly associated with herbivore insects. Here, we employed a combination of genomic and biochemical tools for a detailed evaluation of the cellulolytic potential of Streptomyces sp. I1.2, an aerobic bacterium isolated from the intestinal lumen of A. fulica in a screening for cellulolytic bacteria. Genomic analysis revealed that the ratio and diversity of CAZy domains and GH families coded by Streptomyces sp. I1.2 are comparable to those present in other highly cellulolytic bacteria. After growth on crystalline cellulose or sugarcane bagasse as sole carbon sources, the functionality of several genes encoding endoglucanases, cellobiohydrolases, xylanases, CBMs, and one β-glucosidase were confirmed by the combination of enzymatic activity measurements, zymography, TLC, and cellulose-binding assays. The endoglucanases secreted by this isolate were stable at 50 °C and exhibited activity over a broad pH range between 4.0 and 8.0. The endoglucanases and cellobiohydrolases secreted by Streptomyces sp. I1.2 exhibited specific activities that were similar to the levels present in a commercial cellulase preparation from Trichoderma reesei, while I1.2 xylanase levels were even 350 % higher. The results presented here show that Streptomyces sp. I1.2 is promising for future biotechnological applications, since it is able to produce endoglucanases, cellobiohydrolases, and xylanases in appreciable amounts when grown on a low-cost residue such as sugarcane bagasse.

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+
from £29.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

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
Fig. 7

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

References

  • Adams AS, Jordan MS, Adams SM, Suen G, Goodwin LA, Davenport KW, Currie CR, Raffa KF (2011) Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio. ISME J 5:1323–1331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson I, Abt B, Lykidis A, Klenk HP, Kyrpides N, Ivanova N (2012) Genomics of aerobic cellulose utilization systems in actinobacteria. PLoS One 7:e39331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aziz, RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, OverbeeK RS, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A and Zagnitko O. (2008). The RAST Server: Rapid Annotations using Subsystems Technology. BMC Genomics 2008 9:75

  • Bailey MJ, Biely P, Poutanen K (1992) Interlaboratory testing of methods for assay of xylanase activity. J Biotechnol 23:257–270

    Article  CAS  Google Scholar 

  • Bentley SD, Chater KF, Cerdeno-Tarraga 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 

  • Bignell DE, Anderson JM, Crosse R (1991) Isolation of facultatively aerobic actinomycetes from the gut, parent soil and mound materials of the termites Procubitermes aburiensis and Cubitermes severus. FEMS Microbiol Ecol 8:151–159

    Article  Google Scholar 

  • Book AJ, Lewin GR, McDonald BR, Takasuka TE, Doering DT, Adams AS, Blodgett JA, Clardy J, Raffa KF, Fox BG, Currie CR (2014) Cellulolytic Streptomyces strains associated with herbivorous insects share a phylogenetically linked capacity to degrade lignocellulose. Appl Environ Microbiol 80(15):4692–4701

    Article  PubMed  PubMed Central  Google Scholar 

  • Book AJ, Lewin GR, McDonald BR, Takasuka TE, Wendt-Pienkowski E, Doering DT, Suh E, Raffa KF, Fox BG, Currie CR (2016) Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression. PLoS Biol 14(6):e1002475

    Article  PubMed  PubMed Central  Google Scholar 

  • Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The carbohydrate-active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238

    Article  CAS  PubMed  Google Scholar 

  • Da Vinha FN, Gravina-Oliveira MP, Franco MN, Macrae A, Bon EPS, Nascimento RP, Coelho RR (2011) Cellulase production by Streptomyces viridobrunneus SCPE-09 using lignocellulosic biomass as inducer substrate. Appl Biochem Biotechnol 164:256–267

    Article  PubMed  Google Scholar 

  • Deboy RT, Mongodin EF, Fouts DE, Tailford LE, Khouri H, Emerson JB, Mohamoud Y, Watkins K, Henrissat B, Gilbert HJ, Nelson KE (2008) Insights into plant cell wall degradation from the genome sequence of the soil bacterium Cellvibrio japonicus. J Bacteriol 190:5455–5463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deshpande MV, Eriksson KE, Pettersson LG (1984) An assay for selective determination of exo-1,4,-β-glucanases in a mixture of cellulolytic enzymes. Anal Biochem 138:481–487

    Article  CAS  PubMed  Google Scholar 

  • Dimarogona M, Topakas E, Olsson L, Christakopoulos P (2012) Lignin boosts the cellulase performance of a GH-61 enzyme from Sporotrichum thermophile. Bioresour Technol 110:480–487

    Article  CAS  PubMed  Google Scholar 

  • Doi RH (2008) Cellulases of mesophilic microorganisms: cellulosome and noncellulosome producers. Ann N Y Acad Sci 1125:267–279

    Article  CAS  PubMed  Google Scholar 

  • Edwards MC, Henriksen ED, Yomano LP, Gardner BC, Sharma LN, Ingram LO, Doran Peterson J (2011) Addition of genes for cellobiase and pectinolytic activity in Escherichia coli for fuel ethanol production from pectin-rich lignocellulosic biomass. Appl Environ Microbiol 77:5184–5191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Naggar NEA, Abdelwahed NAM (2012) Optimization of process parameters for the production of alkali-tolerant carboxymethyl cellulase by newly isolated Streptomyces sp. strain NEAE-D. Afr J Biotechnol 11:1185–1196

    CAS  Google Scholar 

  • Figueras M, Beaz-Hidalgo R, Hossain MJ, Liles MR (2014) Taxonomic affiliation of new genomes should be verified using average nucleotide identity and multilocus phylogenetic analysis. Genome Announc 2(6):e00927–e00914

    Article  PubMed  PubMed Central  Google Scholar 

  • Forsberg Z, Vaaje-Kolstad G, Westereng B, Bunaes AC, Stenstrom Y, Mackenzie A, Sørlie M, Horn SJ, Eijsink VG (2011) Cleavage of cellulose by a CBM33 protein. Protein Sci 20:1479–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franco-Cirigliano MN, Rezende RC, Gravina-Oliveira MP, Pereira PH, Nascimento RP, Bon EP, Macrae A, Coelho RRR (2013) Streptomyces misionensis PESB-25 produces a thermoacidophilic endoglucanase using sugarcane bagasse and corn steep liquor as the sole organic substrates. Biomed Res Int 2013:584207

    Article  PubMed  PubMed Central  Google Scholar 

  • Garda AL, Fernandez-Abalos JM, Sanchez P, Ruiz-Arribas A, Santamaria RI (1997) Two genes encoding an endoglucanase and a cellulose-binding protein are clustered and co-regulated by a TTA codon in Streptomyces halstedii JM8. Biochem J 324(Pt 2):403–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91

    Article  CAS  PubMed  Google Scholar 

  • Grigorevski-Lima AL, Nascimento RP, Bon EPS, Coellho RRR (2005) Streptomyces drozdowiczii cellulase production using agro-industrial by-products and its potential use in the detergent and textile industries. Enzyme Microb Tech 37:272–277

    Article  Google Scholar 

  • Guo Y, Zheng W, Rong X, Huang Y (2008) A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics. Int J Syst Evol Microbiol 58:149–159

    Article  CAS  PubMed  Google Scholar 

  • Heptinstall J, Stewart JC, Seras M (1986) Fluorimetric estimation of exo-cellobiohydrolase and β-D-glucosidase activities in cellulase from Aspergillus fumigatus Fresenius. Enzyme Microb Tech 8:70–74

    Article  CAS  Google Scholar 

  • Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VG (2012) Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 5:45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hrmova M, De Gori R, Smith BJ, Fairweather JK, Driguez H, Varghese JN, Fincher GB (2002) Structural basis for broad substrate specificity in higher plant β-D-glucan glucohydrolases. Plant Cell 14:1033–1052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu J, Arantes V, Pribowo A, Saddler JN (2013) The synergistic action of accessory enzymes enhances the hydrolytic potential of a “cellulase mixture” but is highly substrate specific. Biotechnol Biofuels 6:112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Yun S, Ounaies Z (2006) Discovery of cellulose as a smart material. Macromolecules 39:4202–4206

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Langston JA, Shaghasi T, Abbate E, Xu F, Vlasenko E, Sweeney MD (2011) Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol 77:7007–7015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Gao P (1997) Isolation and partial properties of cellulose decomposing strain of Cytophaga sp. LX-7 from soil. J Appl Microb 82:73–80

    Article  CAS  Google Scholar 

  • Lucena SA, Moraes CS, Costa SG, De Souza W, Azambuja P, Garcia ES, Genta FA (2013) Miniaturization of hydrolase assays in thermocyclers. Anal Biochem 434:39–43

    Article  CAS  PubMed  Google Scholar 

  • Medve J, Karlsson J, Lee D, Tjernfeld F (1998) Hydrolysis of microcrystalline cellulose by cellobiohydrolase I and endoglucanase II from Trichoderma reesei: adsorption, sugar production pattern, and synergism of the enzymes. Biotechnol Bioeng 59:621–634

    Article  CAS  PubMed  Google Scholar 

  • Miller L (1959) Use of a dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Moormann M, Schlochtermeier A, Schrempf H (1993) Biochemical characterization of a protease involved in the processing of a Streptomyces reticuli cellulase (Avicelase). Appl Environ Microbiol 59:1573–1578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Najmudin S, Guerreiro CI, Carvalho AL, Prates JA, Correia MA, Alves VD, Ferreira LM, Romao MJ, Gilbert HJ, Bolam DN, Fontes CM (2006) Xyloglucan is recognized by carbohydrate-binding modules that interact with β-glucan chains. J Biol Chem 281:8815–8828

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa YS, Kudo M, Loose JS, Ishikawa T, Totani K, Eijsink VG, Vaaje-Kolstad G (2015) A small lytic polysaccharide monooxygenase from Streptomyces griseus targeting α- and β-chitin. FEBS J 282(6):1065–1079

    Article  CAS  PubMed  Google Scholar 

  • Nascimento RP, Junior NA, Pereira N Jr, Bon EP, Coelho RRR (2009) Brewer’s spent grain and corn steep liquor as substrates for cellulolytic enzymes production by Streptomyces malaysiensis. Lett Appl Microbiol 48:529–535

    Article  CAS  PubMed  Google Scholar 

  • Nummi M, Niku-Paavola ML, Lappalainen A, Enari TM, Raunio V (1983) Cellobiohydrolase from Trichoderma reesei. Biochem J 215:677–683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parry NJ, Beever DE, Oewn E, Vandenberghe I, Van Beeumen J, Bhat MK (2001) Biochemical characterization and mechanism of action of a thermostable β-glucosidase purified from Thermoascus aurantiacus. Biochem J 353:117–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pasti MB, Pometto AL III, Nuti MP, Crawford DL (1990) Lignin-solubilizing ability of actinomycetes isolated from termite (Termitidae) gut. Appl Environ Microbiol 56:2213–2218

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perez-Pons JA, Rebordosa X, Querol E (1995) Induction and preliminary characterization of intracellular β-glucosidases from a cellulolytic Streptomyces strain. FEMS Microbiol Lett 128:235–239

    CAS  PubMed  Google Scholar 

  • Pinheiro GL, Correa RF, Cunha RS, Cardoso AM, Chaia C, Clementino MM, Garcia ES, De Souza W, Frases S (2015) Isolation of aerobic cultivable cellulolytic bacteria from different regions of the gastrointestinal tract of giant land snail Achatina fulica. Front Microbiol 6:860

    Article  PubMed  PubMed Central  Google Scholar 

  • Pinto R, Moreira S, Mota M, Gama M (2004) Studies on the cellulose-binding domains adsorption to cellulose. Langmuir 20:1409–1413

    Article  CAS  PubMed  Google Scholar 

  • Qi B, Chen X, Su Y, Wan Y (2011) Enzyme adsorption and recycling during hydrolysis of wheat straw lignocellulose. Bioresour Technol 102:2881–2889

    Article  CAS  PubMed  Google Scholar 

  • Riederer A, Takasuka TE, Makino S, Stevenson DM, Bukhman YV, Elsen NL, Fox BG (2011) Global gene expression patterns in Clostridium thermocellum as determined by microarray analysis of chemostat cultures on cellulose or cellobiose. Appl Environ Microbiol 77:1243–1253

    Article  CAS  PubMed  Google Scholar 

  • Saritha M, Arora A, Singh S, Nain L (2013) Streptomyces griseorubens mediated delignification of paddy straw for improved enzymatic saccharification yields. Bioresour Technol 135:12–17

    Article  CAS  PubMed  Google Scholar 

  • Schäfer A, Konrad R, Kuhnigk T, Kämpfer P, Hertel H, König H (1996) Hemicellulose-degrading bacteria and yeasts from the termite gut. J Appl Bacteriol 80:471–478

    Article  PubMed  Google Scholar 

  • Schlatter D, Fubuh A, Xiao K, Hernandez D, Hobbie S, Kinkel L (2009) Resource amendments influence density and competitive phenotypes of Streptomyces in soil. Microb Ecol 57:413–420

    Article  PubMed  Google Scholar 

  • Schlochtermeier A, Niemeyer F, Schrempf H (1992a) Biochemical and electron microscopic studies of the Streptomyces reticuli cellulase (Avicelase) in its mycelium-associated and extracellular forms. Appl Environ Microbiol 58:3240–3248

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schlochtermeier A, Walter S, Schröder J, Moormann M, Schrempf H (1992b) The gene encoding the cellulase (Avicelase) Cel1 from Streptomyces reticuli and analysis of protein domains. Mol Microbiol 6:3611–3621

    Article  CAS  PubMed  Google Scholar 

  • Schlosser A, Jantos J, Hackmann K, Schrempf H (1999) Characterization of the binding protein-dependent cellobiose and cellotriose transport system of the cellulose degrader Streptomyces reticuli. Appl Environ Microbiol 65:2636–2643

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwarz WH (2001) The cellulosome and cellulose degradation by anaerobic bacteria. Appl Microbiol Biotechnol 56:634–649

    Article  CAS  PubMed  Google Scholar 

  • Sørensen HR, Meyer AS, Pedersen S (2003) Enzymatic hydrolysis of water-soluble wheat arabinoxylan. 1. Synergy between α-L-arabinofuranosidases, endo-1,4-β-xylanases, and β-xylosidase activities. Biotechnol Bioeng 81:726–731

    Article  PubMed  Google Scholar 

  • Takasuka TE, Book AJ, Lewin GR, Currie CR, Fox BG (2013) Aerobic deconstruction of cellulosic biomass by an insect-associated Streptomyces. Sci Rep 3:1030

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Telke AA, Zhuang N, Ghatge SS, Lee SH, Ali-Shah A, Khan H, Um Y, Shin HD, Chung YR, Lee KH, Kim SW (2013) Engineering of family-5 glycoside hydrolase (Cel5A) from an uncultured bacterium for efficient hydrolysis of cellulosic substrates. PLoS One 8:e65727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tolonen AC, Chilaka AC, Church GM (2009) Targeted gene inactivation in Clostridium phytofermentans shows that cellulose degradation requires the family 9 hydrolase Cphy3367. Mol Microbiol 74:1300–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, Sørlie M, Eijsink VG (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330:219–222

    Article  CAS  PubMed  Google Scholar 

  • Wachinger G, Bronnenmeier K, Staudenbauer WL, Schrempf H (1989) Identification of mycelium-associated cellulase from Streptomyces reticuli. Appl Environ Microbiol 55:2653–2657

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson DB (2009) The first evidence that a single cellulase can be essential for cellulose degradation in a cellulolytic microorganism. Mol Microbiol 74:1287–1288

    Article  CAS  PubMed  Google Scholar 

  • Wood TM, Bhat KM (1988) Methods for measuring cellulase activities. Methods Enzymol 160:87–117

    Article  CAS  Google Scholar 

  • Yi Z, Su X, Revindran V, Mackie RI, Cann I (2013) Molecular and biochemical analyses of CbCel9A/Cel48A, a highly secreted multi-modular cellulase by Caldicellulosiruptor bescii during growth on crystalline cellulose. PLoS One 8:e84172

    Article  PubMed  PubMed Central  Google Scholar 

  • Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40:W445–W451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YHP, Himmel ME, Mielenz JR (2006) Outlook for cellulase improvement: screening and selection strategies. Biotechnol Adv 24:452–481

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank the staff of Inmetro for the technical assistance, insightful discussions, and comments.

Author information

Authors and Affiliations

  1. Diretoria de Metrologia Aplicada às Ciências da Vida, Instituto Nacional de Metrologia, Qualidade e Tecnologia - Inmetro, Rio de Janeiro, RJ, Brazil

    Guilherme L. Pinheiro

  2. Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, UFRJ, Rio de Janeiro, RJ, Brazil

    Guilherme L. Pinheiro, Wanderley de Souza & Susana Frases

  3. Laboratório de Metabolismo Macromolecular Firmino Torres de Castro, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

    Allan C. de Azevedo-Martins

  4. Instituto de Biologia Roberto Alcântara Gomes, Departamento de Bioquímica, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

    Rodolpho M. Albano

Authors
  1. Guilherme L. Pinheiro
    View author publications

    Search author on:PubMed Google Scholar

  2. Allan C. de Azevedo-Martins
    View author publications

    Search author on:PubMed Google Scholar

  3. Rodolpho M. Albano
    View author publications

    Search author on:PubMed Google Scholar

  4. Wanderley de Souza
    View author publications

    Search author on:PubMed Google Scholar

  5. Susana Frases
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Susana Frases.

Ethics declarations

Funding

This work was funded by the Brazilian research agencies Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pinheiro, G.L., de Azevedo-Martins, A.C., Albano, R.M. et al. Comprehensive analysis of the cellulolytic system reveals its potential for deconstruction of lignocellulosic biomass in a novel Streptomyces sp.. Appl Microbiol Biotechnol 101, 301–319 (2017). https://doi.org/10.1007/s00253-016-7851-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1007/s00253-016-7851-7

Keywords

Profiles

  1. Susana Frases View author profile