Cellulolytic activity of brown-rot Antrodia sinuosa at the initial stage of cellulose degradation
-
Junko Sugano
,
Riikka Linnakoski
,
Seppo Huhtinen
Abstract
The initial stage of cellulose degradation has been studied via in vitro assays of fungi isolated from rotten wood in a boreal forest. Among the 37 isolates, Antrodia sinuosa appeared to be an effective cellulose degrader and was selected for studying the initial degradation process. In the liquid cultivation with carboxymethylcellulose (CMC), the increase of the mycelial dry weight coincided with the pH decrease of the culture medium from pH 5.7 to 3.9, between the 3rd and 6th cultivation day. At the same time, the cellulolytic activity increased; the CMCase activity increased sharply and the reducing sugars reached their maximum concentration in the culture medium. It seems that the decreasing pH enables the cellulose degradation by A. sinuosa at an early stage of the process. The results of this study may be useful for a more efficient industrial application of biomass by means of brown-rot fungi.
Funding source: KONE Foundation
Award Identifier / Grant number: 33-2378
Award Identifier / Grant number: 44-8103
Award Identifier / Grant number: 55-15747
Award Identifier / Grant number: 71-28532
Funding statement: JS was financially supported by the University of Turku and the KONE Foundation, Funder Id: 10.13039/501100005781 (grant numbers 33-2378, 44-8103, 55-15747, 71-28532), Finland. RL was financially supported by the University of Helsinki.
Acknowledgments
We thank the staff at the Botanical Garden, the University of Turku and the University of Eastern Finland for their supports in conducting this study. We appreciate Joanna Kowalczyk, Kristiina Hildén, Elizabeth Nyman and Oili Kiikkilä for commenting on and proofreading this paper.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Employment or leadership: None declared.
Honorarium: None declared.
References
Agematu, H., Takahashi, T., Hamano, Y. (2017) Continuous volatile fatty acid production from lignocellulosic biomass by a novel rumen-mimetic bioprocess. J. Biosci. Bioeng. 124:528–533.10.1016/j.jbiosc.2017.06.006Search in Google Scholar PubMed
Arantes, V., Goodell, B. (2014) Current understanding of brown-rot fungal biodegradation mechanisms: A review. In: Deterioration and protection of sustainable biomaterials. Eds. Schultz, T.P., Goodell, B., Nicholas, D.D. Oxford University Press, Oxford. pp. 3–21.10.1021/bk-2014-1158.ch001Search in Google Scholar
Bak, J.S., Ko, J.K., Choi, I-G., Park, Y-C., Seo, J-H., Kim, K.H. (2009) Fungal pretreatment of lignocellulose by Phanerochaete chrysosporium to produce ethanol from rice straw. Biotechnol. Bioeng. 104:471–482.10.1002/bit.22423Search in Google Scholar PubMed
Balan, V. (2014) Current challenges in commercially producing biofuels from lignocellulosic biomass. ISRN Biotechnol. 2014: Article ID 463074, 31 pages.10.1155/2014/463074Search in Google Scholar PubMed PubMed Central
Baldrian, P. (2008) Chapter 2 Enzymes of saprotrophic basidiomycetes. Br. Mycol. Soc. Symp. 28:19–41.10.1016/S0275-0287(08)80004-5Search in Google Scholar
Bigelow, D.M., Gilbertson, R.L., Matheron, M.E. (1998) Cultural studies of fungi causing brown rot in heartwood of living lemon trees in Arizona. Mycol. Res. 102:257–262.10.1017/S0953756297004723Search in Google Scholar
Brischke, C., Welzbacher, C.R., Huckfeldt, T. (2008) Influence of fungal decay by different basidiomycetes on the structural integrity of Norway spruce wood. Holz Roh Werkst. 66:433–438.10.1007/s00107-008-0257-1Search in Google Scholar
Casieri, L., Anastasi, A., Prigione, V., Varese, G.C. (2010) Survey of ectomycorrhizal, litter-degrading, and wood-degrading Basidiomycetes for dye decolorization and ligninolytic enzyme activity. Antonie van Leeuwenhoek 98:483–504.10.1007/s10482-010-9466-9Search in Google Scholar PubMed
Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., Sayers, E.W. (2015) GenBank. Nucleic Acids Res. 44:D67–72.10.1093/nar/gkv1276Search in Google Scholar PubMed PubMed Central
Cohen, R., Suzuki, M.R., Hammel, K.E. (2005) Processive endoglucanase active in crystalline cellulose hydrolysis by the brown rot basidiomycete Gloeophyllum trabeum. Appl. Environ. Microbiol. 71:2412–2417.10.1128/AEM.71.5.2412-2417.2005Search in Google Scholar PubMed PubMed Central
Dashtban, M., Maki, M., Leung, K.T., Mao, C., Qin, W. (2010) Cellulase activities in biomass conversion: measurement methods and comparison. Crit. Rev. Biotechnol. 30:302–309.10.3109/07388551.2010.490938Search in Google Scholar PubMed
Deepa, B., Abraham, E., Cordeiro, N., Mozetic, M., Mathew, A.P., Oksman, K., Faria, M., Thomas, S., Pothan, L.A. (2015) Utilization of various lignocellulosic biomass for the production of nanocellulose: a comparative study. Cellulose 22:1075–1090.10.1007/s10570-015-0554-xSearch in Google Scholar
Dias, A.A., Freitas, G.S., Marques, G.S.M., Sampaio, A., Fraga, I.S., Rodrigues, M.A.M., Evtuguin, D.V., Bezerra, R.M.F. (2010) Enzymatic saccharification of biologically pre-treated wheat straw with white-rot fungi. Bioresour. Technol. 101:6045–6050.10.1016/j.biortech.2010.02.110Search in Google Scholar PubMed
Elisashvili, V., Kachlishvili, E., Penninckx, M. (2008) Effect of growth substrate, method of fermentation, and nitrogen source on lignocellulose-degrading enzymes production by white-rot basidiomycetes. J. Ind. Microbiol. Biotechnol. 35:1531–1538.10.1007/s10295-008-0454-2Search in Google Scholar PubMed
Fu, C.C., Hung, T.C., Chen, J.Y., Su, C.H., Wu, W.T. (2010) Hydrolysis of microalgae cell walls for production of reducing sugar and lipid extraction. Bioresour. Technol. 101:8750–8754.10.1016/j.biortech.2010.06.100Search in Google Scholar PubMed
Gardes, M., Bruns, T.D. (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Mol. Ecol. 2:113–118.10.1111/j.1365-294X.1993.tb00005.xSearch in Google Scholar PubMed
Ghose, T.K. (1987) Measurement of cellulase activities. Pure Appl. Chem. 59:257–268.10.1351/pac198759020257Search in Google Scholar
Guerriero, G., Hausman, J-F., Strauss, J., Ertan, H., Siddiqui, K.S. (2016) Lignocellulosic biomass: biosynthesis, degradation, and industrial utilization. Eng. Life Sci. 16:1–16.10.1002/elsc.201400196Search in Google Scholar
Gupta, P.K., Durzan, D.J. (1985) Shoot multiplication from mature trees of Douglas-fir (Pseudotsuga menziesii) and sugar pine (Pinus lambertiana). Plant Cell Rep. 4:177–179.10.1007/BF00269282Search in Google Scholar PubMed
Ha, S-J., Galazka, J.M., Kim, S.R., Choi, J-H., Yang, X., Seo, J-H., Glass, N.L., Cate, J.H.D., Jin, Y-S. (2011) Engineered Saccharomyces cerevisiae capable of simultaneous cellobiose and xylose fermentation. PNAS 108:504–509.10.1073/pnas.1010456108Search in Google Scholar PubMed PubMed Central
Highley, T.L. (1980) Cellulose degradation by cellulose-clearing and non-cellulose clearing brown-rot fungi. Appl. Environ. Microbiol. 40:1145–1147.10.1128/aem.40.6.1145-1147.1980Search in Google Scholar PubMed PubMed Central
Himmel, M.E., Ding, S-Y., Johnson, D.K., Adney, W.S., Nimlos, M.R., Brady, J.W., Foust, T.D. (2007) Biomass recalcitrance: Engineering plants and enzymes for biofuels production. Science 315:804–807.10.1126/science.1137016Search in Google Scholar PubMed
Keller, F.A., Hamilton, J.E., Nguyen, Q.A. (2003) Microbial pretreatment of biomass: Potential for reducing severity of thermochemical biomass pretrearment. Appl. Biochem. Biotech. 105:27–41.10.1385/ABAB:105:1-3:27Search in Google Scholar
Kogo, T., Yoshida, Y., Koganei, K., Matsumoto, H., Watanabe, T.,Ogihara, J., Kasumi, T. (2017) Production of rice straw hydrolysis enzymes by the fungi Trichoderma reesei and Humicola insolens using rice straw as a carbon source. Bioresour. Technol. 233:67–73.10.1016/j.biortech.2017.01.075Search in Google Scholar PubMed
Kumar, R., Singh, S., Singh, O.V. (2008) Bioconversion of lignocellulosic biomass: biochemical and molecular perspectives. J. Ind. Microbiol. Biotechnol. 35:377–391.10.1007/s10295-008-0327-8Search in Google Scholar PubMed
Kumar, M., Campbell, L., Turner, S. (2016) Secondary cell walls: biosynthesis and manipulation. J. Exp. Bot. 67:515–531.10.1093/jxb/erv533Search in Google Scholar PubMed
Lee, L-W., Kim, H-Y., Koo, B-W., Choi, D-H., Kwon, M., Choi, I-G. (2008) Enzymatic saccharification of biologically pretreated Pinus densiflora using enzymes from brown rot fungi. J. Biosci. Bioeng. 106:162–167.10.1263/jbb.106.162Search in Google Scholar PubMed
Longoni, P., Rodolfi, M., Pantaleoni, L., Doria, E., Concia, L., Picco, A.M., Cella, R. (2012) Functional analysis of the degradation of cellulosic substrates by a Chaetomium globosum endophytic isolate. Appl. Environ. Microbiol. 78:3693–3705.10.1128/AEM.00124-12Search in Google Scholar PubMed PubMed Central
Lowe, S.E., Theodorou, M.K., Trinci, A.P.J. (1987) Cellulase and xylanase of an anaerobic rumen fungus grown on wheat straw holocellulose, cellulose, and xylan. Appl. Environ. Microb. 53:1216–1223.10.1128/aem.53.6.1216-1223.1987Search in Google Scholar PubMed PubMed Central
Lynd, L.R., Weimer, P.J., van Zyl, W.H., Pretorius, I.S. (2002) Microbial cellulose utilization: fundamental and biotechnology. Microbiol. Mol. Biol. R. 66:506–577.10.1128/MMBR.66.3.506-577.2002Search in Google Scholar PubMed PubMed Central
Mansfield, S.D., Saddler, J.N., Gübitz, G.M. (1998) Characterization of endoglucanases from the brown rot fungi Gloeophyllum sepiarium and Gloeophyllum trabeum. Enzyme Microb. Tech. 23:133–140.10.1016/S0141-0229(98)00033-7Search in Google Scholar
Matheron, M.E., Porchas, M., Bigelow, D.M. (2006) Factors affecting the development of wood rot on lemon trees infected with Antrodia sinuosa, Coniophora eremophila, and a Nodulisporium sp. Plant Dis. 90:554–558.10.1094/PD-90-0554Search in Google Scholar PubMed
Mathews, S.L., Grunden, A.M., Pawlak, J. (2016) Degradation of lignocellulose and lignin by Paenibacillus glucanolyticus. Int. Biodeterior. Biodegradation. 110:79–86.10.1016/j.ibiod.2016.02.012Search in Google Scholar
Mosier, N., Wyman, C., Dale, B., Elander, R., Lee, Y.Y., Holtzapple, M., Ladisch, M. (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresource Technol. 96:673–686.10.1016/j.biortech.2004.06.025Search in Google Scholar PubMed
Quiroz-Castañeda, R.E., Martínez-Anaya, C., Cuervo-Soto, L.I., Segovia, L., Folch-Mallol, J.L. (2011) Loosenin, a novel protein with cellulose-disrupting activity from Bjerkandera adusta. Microb. Cell. Fact. 10:8.10.1186/1475-2859-10-8Search in Google Scholar PubMed PubMed Central
Renvall, P. (1995) Community structure and dynamics of wood-rotting Basidiomycetes on decomposing conifer trunks in northern Finland. Karstenia 35:1–51.10.29203/ka.1995.309Search in Google Scholar
Rytioja, J., Hildén, K., Yuzon, J., Hatakka, A., de Vries, R.P., Mäkelä,M.R. (2014) Plant-polysaccharide-degradation enzymes from basidiomycetes. Microbiol. Mol. Biol. R. 78:614–649.10.1128/MMBR.00035-14Search in Google Scholar PubMed PubMed Central
Schmidt, O., Moreth, U. (1996) Biological characterization of Poria indoor brown-rot fungi. Holzforschung 50:105–110.10.1515/hfsg.1996.50.2.105Search in Google Scholar
Shi, J., Sharma-Shivappa, R.R., Chinn, M., Howell, N. (2009) Effect of microbial pretreatment on enzymatic hydrolysis and fermentation of cotton stalks for ethanol production. Biomass Bioenergy 33:88–96.10.1016/j.biombioe.2008.04.016Search in Google Scholar
Shirkavand, E., Baroutian, S., Gapes, D.J., Young, B.R. (2016) Combination of fungal and physicochemical processes for lignocellulosic biomass pretreatment – a review. Renew. Sustainable Energy Rev. 54:217–234.10.1016/j.rser.2015.10.003Search in Google Scholar
Shu, C.H., Lung, M.Y. (2004) Effect of pH the production and molecular weight distribution of exopolysaccharide by Antrodia camphorata in batch cultures. Process Biochem. 39:931–937.10.1016/S0032-9592(03)00220-6Search in Google Scholar
Sindhu, R., Binod, P., Pandey, A. (2016) Biological pretreatment of lignocellulosic biomass – an overview. Bioresour. Technol. 199:76–82.10.1016/j.biortech.2015.08.030Search in Google Scholar PubMed
Sternberg, D. (1976) β-glucosidase of Trichoderma: Its biosynthesis and role in saccharification of cellulose. Appl. Environ. Microbiol. 31:648–654.10.1128/aem.31.5.648-654.1976Search in Google Scholar PubMed PubMed Central
Tanaka, H., Koike, K., Itakura, S., Enoki, A. (2009) Degradation of wood and enzyme production by Ceriporiopsis subvermispora. Enzyme Microb. Technol. 45:384–390.10.1016/j.enzmictec.2009.06.003Search in Google Scholar
Tomšovský, M., Popelářová, P., Baldrian, P. (2009) Production and regulation of lignocellulose-degrading enzymes of Poria-like wood-inhabiting basidiomycetes. Folia. Microbiol. 54:74–80.10.1007/s12223-009-0011-zSearch in Google Scholar PubMed
van Kuijk, S.J.A., Sonnenberg, A.S.M., Baars, J.J.P., Hendriks, W.H., Cone, J.W. (2015) Fungal treatment of lignocellulosic biomass: importance of fungal species colonization and time on chemical composition and in vitro rumen degradability. Anim. Feed Sci. Tech. 209:40–50.10.1016/j.anifeedsci.2015.07.026Search in Google Scholar
Wan, C., Li, Y. (2012) Fungal pretreatment of lignocellulose biomass. Biotechnol. Adv. 30:1447–1457.10.1016/j.biotechadv.2012.03.003Search in Google Scholar PubMed
White, T.J., Bruns, T., Lee, S., Taylor, J.W. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Method and Applications. Eds. Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T J. Academic Press, Inc., New York. pp. 315–322.10.1016/B978-0-12-372180-8.50042-1Search in Google Scholar
Wood, T.M., Bhat, K.M. (1988) Methods for measuring cellulase activities. Methods Enzymol. 160:87–112.10.1016/0076-6879(88)60109-1Search in Google Scholar
Wu, M.D., Chen, M.J., Wang, W.Y., Huang, H.C., Yuan, G.F., Chen, J.J., Chen, I.S., Wang, B.C. (2011) Antioxidant activities of extracts and metabolites isolated from the fungus Antrodia cinnamomea. Nat. Prod. Res. 25:1488–1496.10.1080/14786410903132563Search in Google Scholar PubMed
Xu, C., Ma, F., Zhang, X. (2009) Lignocellulose degradation and enzyme production by Irpex lacteus CD2 during solid-state fermentation of corn stover. J. Biosci. Bioeng. 108:372–375.10.1016/j.jbiosc.2009.04.023Search in Google Scholar PubMed
Yoon, J.J., Kim, K.Y., Cha, C.J. (2008) Purification and characterization of thermostable β-glucosidase from the brown-rot basidiomycete Fomitopsis palustris grown on microcrystalline cellulose. J. Microbiol. 46:51–55.10.1007/s12275-007-0230-4Search in Google Scholar PubMed
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/hf-2018-0145).
©2019 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Original Articles
- Synchrotron X-ray measurements of cellulose in wood cell wall layers of Pinus densiflora in the transmission and reflectance modes. Part 1: results without loading
- NIR hyperspectral imaging (NIR-HI) and μXRD for determination of the transition between juvenile and mature wood of Pinus sylvestris L.
- Characterization of the pits in parenchyma cells of the moso bamboo [Phyllostachys edulis (Carr.) J. Houz.] culm
- Identification of chemical constituents from the bark of Larix kaempferi and their tyrosinase inhibitory effect
- Oxygen delignification: laboratory evaluation of the impact of dissolved organic matter, sodium carbonate and sodium thiosulfate
- A study of thermo-hydro-treated (THT) birch wood by chemical analysis and Py-GC/MS
- Thermally modified (TM) beech wood: compression properties, fracture toughness and cohesive law in mode II obtained from the three-point end-notched flexure (3ENF) test
- Cellulolytic activity of brown-rot Antrodia sinuosa at the initial stage of cellulose degradation
- Ligninases remove phenolic inhibitors and facilitate yeast growth in lignocellulosic hydrolysate
- Development of a reinforced styrene-free unsaturated polyester composite based on bamboo fibers
- Functionalisation of poly(ethylene terephthalate) (PET) surfaces with two cationised xylans by means of two anchoring polymers
Articles in the same Issue
- Frontmatter
- Original Articles
- Synchrotron X-ray measurements of cellulose in wood cell wall layers of Pinus densiflora in the transmission and reflectance modes. Part 1: results without loading
- NIR hyperspectral imaging (NIR-HI) and μXRD for determination of the transition between juvenile and mature wood of Pinus sylvestris L.
- Characterization of the pits in parenchyma cells of the moso bamboo [Phyllostachys edulis (Carr.) J. Houz.] culm
- Identification of chemical constituents from the bark of Larix kaempferi and their tyrosinase inhibitory effect
- Oxygen delignification: laboratory evaluation of the impact of dissolved organic matter, sodium carbonate and sodium thiosulfate
- A study of thermo-hydro-treated (THT) birch wood by chemical analysis and Py-GC/MS
- Thermally modified (TM) beech wood: compression properties, fracture toughness and cohesive law in mode II obtained from the three-point end-notched flexure (3ENF) test
- Cellulolytic activity of brown-rot Antrodia sinuosa at the initial stage of cellulose degradation
- Ligninases remove phenolic inhibitors and facilitate yeast growth in lignocellulosic hydrolysate
- Development of a reinforced styrene-free unsaturated polyester composite based on bamboo fibers
- Functionalisation of poly(ethylene terephthalate) (PET) surfaces with two cationised xylans by means of two anchoring polymers
