Abstract
Fungi can improve stover digestibility due to their ability to secrete oxidative enzymes that depolymerize lignin, allowing the rumen microorganisms to access the polysaccharides of the plant cell wall. Some ascomycetes have shown good delignification capability; however, they have been scarcely evaluated for their ability to improve corn stover (CS) ruminal digestibility. We evaluated the laccase induction by CS of the CMU-196 strain of the ascomycete fungus Didymosphaeria sp. (syn. = Paraconiothyrium sp.). Also, we analyzed the capacity of such strain to modify the cell wall of CS and to improve its digestion by the ruminal microbiota. The CMU-196 strain showed a maximum extracellular laccase activity of 39.74 ± 0.24 U/L when an aqueous stover extract (SE, 10% v/v) was added to the growth medium. The addition of ground stover (GS, 2% w/v) increased the activity to a maximum of 262.27 ± 0.58 U/L. In solid-state fermentation (SSF) assays of GS, the strain degrades cell walls, destabilizing the vessels and tracheids of plant biomass; the protein content reaches a maximum of 33.2 g/kg dry matter (DM) at 70 days, while the crude fiber content shows the highest level of 314 g/kg DM at 14 days. SSF treatment of the CS increased the in vitro ruminal production of gas in a fraction that was considered nondigestible at 18 h, and gas production increased by 14% with respect to the untreated GS at 14 days. The CMU-196 strain can digest the plant cell wall and improve ruminal CS digestibility at a level equivalent to several basidiomycete species.
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References
A.O.A.C. (1984) Official methods of analysis. Association of Official Analytical Chemists. E.U.A. 21st Ed. Washington, D.C.
Abo-Donia FM, Abdel-Azim SN, Elghandour MM, Salem AZ, Buendía G, Soliman NAM (2014) Feed intake, nutrient digestibility and ruminal fermentation activities in sheep-fed peanut hulls treated with Trichoderma viride or urea. Trop Anim Health Prod 46:221–228. https://doi.org/10.1007/s11250-013-0479-z
Akinfemi A, Adu OA, Adebiyi OA (2009) Use of white rot-fungi in upgrading maize straw and, the resulting impact on chemical composition and in vitro digestibility. Livest Res Rural Dev 21:#162. http://www.lrrd.org/lrrd21/10/akin21162.htm
Anderson AJ, Kwon SI, Carnicero A, Falcón MA (2005) Two isolates of Fusarium proliferatum from different habitats and global locations have similar abilities to degrade lignin. FEMS Microbiol Lett 249:149–155. https://doi.org/10.1016/j.femsle.2005.06.014
Ariyawansa HA, Tanaka K, Thambugala KM, Phookamsak R, Tian Q, Camporesi E, Hongsanan S, Monkai J, Wanasinghe DN, Chukeatirote E, Kang JC, Xu JC, McKenzie EHC, Jones EBG, Hyde KD (2014) A molecular phylogenetic reappraisal of the Didymosphaeriaceae (=Montagnulaceae). Fungal Divers 68:69–104. https://doi.org/10.1007/s13225-014-0305-6
Arredondo-Santoyo M, Vázquez-Garcidueñas MS, Vázquez-Marrufo G (2018) Identification and characterization of the biotechnological potential of a wild strain of Paraconiothyrium sp. Biotechnol Prog 34:846–857. https://doi.org/10.1002/btpr.2653
Barbosa AM, Dekker RFH, Hardy GS (1996) Veratryl alcohol as an inducer of laccase by an ascomycete, Botryosphaeria sp., when screened on the polymeric dye Poly R-478. Lett Appl Microbiol 23:93–96. https://doi.org/10.1111/j.1472-765X.1996.tb00038.x
Bonugli-Santos RC, Durrant LR, Da Silva M, Sette LD (2010) Production of laccase, manganese peroxidase and lignin peroxidase by Brazilian marine-derived fungi. Enzym Microb Technol 46:32–37. https://doi.org/10.1016/j.enzmictec.2009.07.014
Boonmee S, D’souza MJ, Luo Z, Pinruan U, Tanaka K, Su H, Bhat DJ, McKenzie EHC, Jones EBG, Taylor JE, Phillips AJ, Hirayama K, Eungwanichayapant PD, Hyde KD (2016) Dictyosporiaceae fam. nov. Fungal Divers 80:457–482. https://doi.org/10.1007/s13225-016-0363-z
Buranov AU, Mazza G (2008) Lignin in straw of herbaceous crops. Ind Crop Prod 28:237–259. https://doi.org/10.1016/j.indcrop.2008.03.008
Cázares-García SV, Arredondo-Santoyo M, Vázquez-Marrufo G, Vázquez-Garcidueñas MS, Robinson-Fuentes VA, Gómez-Reyes VM (2016) Typing and selection of wild strains of Trichoderma spp. producers of extracellular laccase. Biotechnol Prog 32:787–798. https://doi.org/10.1002/btpr.2237
Chang AJ, Fan J, Wen X (2012) Screening of fungi capable of highly selective degradation of lignin in rice straw. Int Biodeterior Biodegrad 72:26–30. https://doi.org/10.1016/j.ibiod.2012.04.013
Chen SF, Mowery RA, Scarlata CJ, Chambliss CK (2007) Compositional analysis of water-soluble materials in corn stover. J Agric Food Chem 55:5912–5918. https://doi.org/10.1021/jf0700327
Cone JW, van Gelder AH, Driehuis F (1997) Description of gas production profiles with a three-phasic model. Anim Feed Sci Technol 66:31–45. https://doi.org/10.1016/S0377-8401(96)01147-9
Crous PW, Wingfield MJ, Burgess TI, Hardy GSJ, Barber PA, Alvarado P, Barnes CW, Buchanan PK, Heykoop M, Moreno G, Thangavel R, van der Spuy S, Barili A, Barrett S, Cacciola SO, Cano-Lira JF, Crane C, Decock C, Gibertoni TB, Guarro J, Guevara-Suarez M, Hubka V, Kolařík M, Lira CRS, Ordoñez ME, Padamsee M, Ryvarden L, Soares AM, Stchigel AM, Sutton DA, Vizzini A, Weir BS, Acharya K, Aloi F, Baseia IG, Blanchette RA, Bordallo JJ, Bratek Z, Butler T, Cano-Canals J, Carlavilla JR, Chander J, Cheewangkoon R, Cruz RHSF, da Silva M, Dutta AK, Ercole E, Escobio V, Esteve-Raventós F, Flores JA, Gené J, Góis JS, Haines L, Held BW, Jung MH, Hosaka K, Jung T, Jurjević Ž, Kautman V, Kautmanova I, Kiyashko AA, Kozanek M, Kubátová A, Lafourcade M, la Spada F, Latha KPD, Madrid H, Malysheva EF, Manimohan P, Manjón JL, Martín MP, Mata M, Merényi Z, Morte A, Nagy I, Normand AC, Paloi S, Pattison N, Pawłowska J, Pereira OL, Petterson ME, Picillo B, Raj KNA, Roberts A, Rodríguez A, Rodríguez-Campo FJ, Romański M, Ruszkiewicz-Michalska M, Scanu B, Schena L, Semelbauer M, Sharma R, Shouche YS, Silva V, Staniaszek-Kik M, Stielow JB, Tapia C, Taylor PWJ, Toome-Heller M, Vabeikhokhei JMC, van Diepeningen A, van Hoa N, M V, Wiederhold NP, Wrzosek M, Zothanzama J, Groenewald JZ (2017) Fungal planet description sheets: 558–624. Persoonia 38:240–384. https://doi.org/10.3767/003158517X698941
Deacon LJ, Pryce-Miller EJ, Frankland JC, Bainbridge BW, Moore PD, Robinson CH (2006) Diversity and function of decomposer fungi from a grassland soil. Soil Biol Biochem 38:7–20. https://doi.org/10.1016/j.soilbio.2005.04.013
Díaz-Godínez G, Sánchez C (2002) In situ digestibility and nutritive value of maize straw generated after Pleurotus ostreatus cultivation. Can J Anim Sci 82:617–619. https://doi.org/10.4141/A02-031
Du B, Sharma LN, Becker C, Chen SF, Mowery RA, van Walsum GP, Chambliss CK (2010) Effect of varying feedstock–pretreatment chemistry combinations on the formation and accumulation of potentially inhibitory degradation products in biomass hydrolysates. Biotechnol Bioeng 107:430–440. https://doi.org/10.1002/bit.22829
Eichlerová I, Homolka L, Žifčáková L, Lisá L, Dobiášová P, Baldrian P (2015) Enzymatic systems involved in decomposition reflects the ecology and taxonomy of saprotrophic fungi. Fungal Ecol 13:10–22. https://doi.org/10.1016/j.funeco.2014.08.002
Enaud E, Trovaslet M, Naveau F, Decristoforo A, Bizet S, Vanhulle S, Jolivalt C (2011) Laccase chloride inhibition reduction by an anthraquinonic substrate. Enzym Microb Technol 49:517–525. https://doi.org/10.1016/j.enzmictec.2011.07.007
Feng X, Chen H, Xue D, Yao S (2013) Enhancement of laccase activity by marine-derived deuteromycete Pestalotiopsis sp. J63 with agricultural residues and inducers. Chin J Chem Eng 21:1182–1189. https://doi.org/10.1016/S1004-9541(13)60567-4
Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kües U, Kumar TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, St. John F, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719. https://doi.org/10.1126/science.1221748
Forootanfar H, Faramarzi MA, Shahverdi AR, Yazdi MT (2011) Purification and biochemical characterization of extracellular laccase from the ascomycete Paraconiothyrium variabile. Bioresour Technol 102:1808–1814. https://doi.org/10.1016/j.biortech.2010.09.043
Gao H, Wang Y, Zhang W, Wang W, Mu Z (2011) Isolation, identification and application in lignin degradation of an ascomycete GHJ-4. Afr J Biotechnol 10:4166–4174. https://doi.org/10.5897/AJB10.2250
Glass NL, Schmoll M, Cate JH, Coradetti S (2013) Plant cell wall deconstruction by ascomycete fungi. Annu Rev Microbiol 67:477–498. https://doi.org/10.1146/annurev-micro-092611-150044
Gómez-Mendoza DP, Junqueira M, de Vale LHF, Domont GB, Ferreira Filho EX, MVD S, CAO R (2014) Secretomic survey of Trichoderma harzianum grown on plant biomass substrates. J Proteome Res 13:1810–1822. https://doi.org/10.1021/pr400971e
Grabber JH (2005) How do lignin composition, structure, and cross-linking affect degradability? A review of cell wall model studies. Crop Sci 45:820–831. https://doi.org/10.2135/cropsci2004.0191
Hansen GH, Lübeck M, Frisvad JC, Lübeck PS, Andersen B (2015) Production of cellulolytic enzymes from ascomycetes: comparison of solid state and submerged fermentation. Process Biochem 50:1327–1341. https://doi.org/10.1016/j.procbio.2015.05.017
He Y, Dijkstra J, Sonnenberg AS, Mouthier TM, Kabel MA, Hendriks WH, Cone JW (2019) The nutritional value of the lower maize stem cannot be improved by ensiling nor by a fungal treatment. Anim Feed Sci Technol 247:92–102. https://doi.org/10.1016/j.anifeedsci.2018.11.002
Janusz G, Pawlik A, Sulej J, Świderska-Burek U, Jarosz-Wilkołazka A, Paszczyński A (2017) Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiol Rev 41:941–962. https://doi.org/10.1093/femsre/fux049
Kaparaju P, Felby C (2010) Characterization of lignin during oxidative and hydrothermal pre-treatment processes of wheat straw and corn stover. Bioresour Technol 101:3175–3181. https://doi.org/10.1016/j.biortech.2009.12.008
Kepp KP (2015) Halide binding and inhibition of laccase copper clusters: the role of reorganization energy. Inorg Chem 54:476–483. https://doi.org/10.1021/ic5021466
Khambhaty Y, Ananth S, Sreeram KJ, Rao JR, Nair BU (2015) Dual utility of a novel, copper enhanced laccase from Trichoderma aureoviridae. Int J Biol Macromol 81:69–75. https://doi.org/10.1016/j.ijbiomac.2015.07.051
Koukol O, Baldrian P (2012) Intergeneric variability in enzyme production of microfungi from pine litter. Soil Biol Biochem 49:1–3. https://doi.org/10.1016/j.soilbio.2012.02.004
Krueger MC, Bergmann M, Schlosser D (2016) Widespread ability of fungi to drive quinone redox cycling for biodegradation. FEMS Microbiol Lett 363:fnw105. https://doi.org/10.1093/femsle/fnw105
Kunitake E, Kobayashi T (2017) Conservation and diversity of the regulators of cellulolytic enzyme genes in Ascomycete fungi. Curr Genet 63:951–958. https://doi.org/10.1007/s00294-017-0695-6
Liers C, Arnstadt T, Ullrich R, Hofrichter M (2011) Patterns of lignin degradation and oxidative enzyme secretion by different wood-and litter-colonizing basidiomycetes and ascomycetes grown on beech-wood. FEMS Microbiol Ecol 78:91–102. https://doi.org/10.1111/j.1574-6941.2011.01144.x
Lorenzo M, Moldes D, Couto SR, Sanromán MAA (2005) Inhibition of laccase activity from Trametes versicolor by heavy metals and organic compounds. Chemosphere 60:1124–1128. https://doi.org/10.1016/j.chemosphere.2004.12.051
Mäkelä MR, Bredeweg EL, Magnuson JK, Baker SE, de Vries RP, Hildén K (2016) Fungal ligninolytic enzymes and their applications. Microbiol Spectr 4:FUNK-0017-2016. https://doi.org/10.1128/microbiolspec.FUNK-0017-2016
Mäkelä MR, Bouzid O, Robl D, Post H, Peng M, Heck A, Altelaar M, de Vries RP (2017) Cultivation of Podospora anserina on soybean hulls results in an efficient enzyme cocktail for plant biomass hydrolysis. New Biotech 37:162–171. https://doi.org/10.1016/j.nbt.2017.02.002
Martín-Sampedro R, Fillat Ú, Ibarra D, Eugenio ME (2015) Towards the improvement of Eucalyptus globulus chemical and mechanical pulping using endophytic fungi. Int Biodeterior Biodegrad 105:120–126. https://doi.org/10.1016/j.ibiod.2015.08.023
Meshram V, Saxena S, Paul K, Gupta M, Kapoor N (2017) Production, purification and characterisation of a potential fibrinolytic protease from endophytic Xylaria curta by solid substrate fermentation. Appl Biochem Biotechnol 181:1496–1512. https://doi.org/10.1007/s12010-016-2298-y
Montañez-Valdez OD, Avellaneda-Cevallos JH, Guerra-Medina CE, Reyes-Gutiérrez JA, Peña-Galeas MM, Casanova-Ferrín LM, Herrera-Herrera RC (2015) Chemical composition and ruminal disappearance of maize stover treated with Pleurotus djamor. Life Sci J 12:55–60 http://www.lifesciencesite.com/lsj/life1202s15/
Moyo CE, Beckett RP, Trifonova TV, Minibayeva FV (2017) Extracellular redox cycling and hydroxyl radical production occurs widely in lichenized Ascomycetes. Fungal Biol 121:582–588. https://doi.org/10.1016/j.funbio.2017.03.005
Nagai M, Sato T, Watanabe H, Saito K, Kawata M, Enei H (2002) Purification and characterization of an extracellular laccase from the edible mushroom Lentinula edodes, and decolorization of chemically different dyes. Appl Microbiol Biotechnol 60:327–335. https://doi.org/10.1007/s00253-002-1109-2
Nayan N, Sonnenberg AS, Hendriks WH, Cone JW (2018) Variation in the solubilization of crude protein in wheat straw by different white-rot fungi. Anim Feed Sci Technol 242:135–143. https://doi.org/10.1016/j.anifeedsci.2018.06.009
Nilsson RLK, Holmgren M, Madavi B, Nilsson RT, Sellstedt A (2016) Adaptability of Trametes versicolor to the lignocellulosic inhibitors furfural, HMF, phenol and levulinic acid during ethanol fermentation. Biomass Bioenergy 90:95–100. https://doi.org/10.1016/j.biombioe.2016.03.030
Niu D, Zuo S, Jiang D, Tian P, Zheng M, Xu C (2018) Treatment using white rot fungi changed the chemical composition of wheat straw and enhanced digestion by rumen microbiota in vitro. Anim Feed Sci Technol 237:46–54. https://doi.org/10.1016/j.anifeedsci.2018.01.005
Paliwal R, Rawat AP, Rawat M, Rai JPN (2012) Bioligninolysis: recent updates for biotechnological solution. Appl Biochem Biotechnol 167:1865–1889. https://doi.org/10.1007/s12010-012-9735-3
Ramírez-Bribiesca JE, Soto-Sánchez A, Hernández-Calva LM, Salinas-Chavira J, Galaviz-Rodríguez JR, Cruz-Monterrosa RG, Vargas-López S (2010) Influence of Pleurotus ostreatus spent corn straw on performance and carcass characteristics of feedlot Pelibuey lambs. Indian J Anim Sci 80:754–757 http://epubs.icar.org.in/ejournal/index.php/IJAnS/issue/view/20
Ravindran R, Jaiswal AK (2016) A comprehensive review on pre-treatment strategy for lignocellulosic food industry waste: challenges and opportunities. Bioresour Technol 199:92–102. https://doi.org/10.1016/j.biortech.2015.07.106
Rico A, Rencoret J, del Río JC, Martínez AT, Gutiérrez A (2014) Pretreatment with laccase and a phenolic mediator degrades lignin and enhances saccharification of Eucalyptus feedstock. Biotechnol Biofuels 7:6. https://doi.org/10.1186/1754-6834-7-6
Ruan Z, Hollinshead W, Isaguirre C, Tang YJ, Liao W, Liu Y (2015) Effects of inhibitory compounds in lignocellulosic hydrolysates on Mortierella isabellina growth and carbon utilization. Bioresour Technol 183:18–24. https://doi.org/10.1016/j.biortech.2015.02.026
Shanmugam S, Hari A, Ulaganathan P, Yang F, Krishnaswamy S, Wu YR (2018) Potential of biohydrogen generation using the delignified lignocellulosic biomass by a newly identified thermostable laccase from Trichoderma asperellum strain BPLMBT1. Int J Hydrog Energy 43:3618–3628. https://doi.org/10.1016/j.ijhydene.2018.01.016
Singh S, Harms H, Schlosser D (2014) Screening of ecologically diverse fungi for their potential to pretreat lignocellulosic bioenergy feedstock. Appl Microbiol Biotechnol 98:3355–3370. https://doi.org/10.1007/s00253-014-5563-4
Theodorou KM, Williams AB, Dahona SM, McAllan BA, France J (1994) A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Anim. Feed Sci Technol 48:185–197. https://doi.org/10.1016/0377-8401(94)90171-6
Tian C, Beeson WT, Iavarone AT, Sun J, Marletta MA, Cate JH, Glass NL (2009) Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa. Proc Natl Acad Sci U S A 106:22157–22162. https://doi.org/10.1073/pnas.0906810106
Tuyen VD, Cone JW, Baars JJP, Sonnenberg ASM, Hendriks WH (2012) Fungal strain and incubation period affect chemical composition and nutrient availability of wheat straw for rumen fermentation. Bioresour Technol 111:336–342. https://doi.org/10.1016/j.biortech.2012.02.001
Tuyen VD, Phuong HN, Cone JW, Baars JJP, Sonnenberg ASM, Hendriks WH (2013) Effect of fungal treatments of fibrous agricultural by-products on chemical composition and in vitro rumen fermentation and methane production. Bioresour Technol 129:256–263. https://doi.org/10.1016/j.biortech.2012.10.128
Van Dyk JS, Pletschke BI (2012) A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes—factors affecting enzymes, conversion and synergy. Biotechnol Adv 30:1458–1480. https://doi.org/10.1016/j.biotechadv.2012.03.002
Van Kuijk SJA, Sonnenberg ASM, Baars JJP, Hendriks WH, Cone JW (2015) Fungal treated lignocellulosic biomass as ruminant feed ingredient: a review. Biotechnol Adv 33:191–202. https://doi.org/10.1016/j.biotechadv.2014.10.014
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
Verkley GJM, Da Silva M, Wicklow DT, Crous PW (2004) Paraconiothyrium, a new genus to accommodate the mycoparasite Coniothyrium minitans, anamorphs of Paraphaeosphaeria, and four new species. Stud Mycol 50:323–335
Verkley GJM, Dukik K, Renfurm R, Göker M, Stielow JB (2014) Novel genera and species of coniothyrium-like fungi in Montagnulaceae (Ascomycota). Persoonia 32:35–51. https://doi.org/10.3767/003158514X679191
White S, McIntyre M, Berry DR, McNeil B (2002) The autolysis of industrial filamentous fungi. Crit Rev Biotechnol 22:1–14. https://doi.org/10.1080/07388550290789432
Xie N, Chapeland-Leclerc F, Silar P, Ruprich-Robert G (2014) Systematic gene deletions evidences that laccases are involved in several stages of wood degradation in the filamentous fungus Podospora anserina. Environ Microbiol 16:141–161. https://doi.org/10.1111/1462-2920.12253
Zhang Z, Xia L, Wang F, Lv P, Zhu M, Li J, Chen K (2015) Lignin degradation in corn stalk by combined method of H2O2 hydrolysis and Aspergillus oryzae CGMCC5992 liquid-state fermentation. Biotechnol Biofuels 8:183. https://doi.org/10.1186/s13068-015-0362-4
Zuo S, Niu D, Zheng M, Jiang D, Tian P, Li R, Xu C (2018) Effect of Irpex lacteus, Pleurotus ostreatus and Pleurotus cystidiosus pretreatment of corn stover on its improvement of the in vitro rumen fermentation. J Sci Food Agric https://doi.org/10.1002/jsfa.8951, 98, 4287, 4295
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We thank CONACYT for the graduate scholarship granted to MAS (no. 226634). This project received support from the CIC-UMSNH within the 2018 research program.
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Arredondo-Santoyo, M., Herrera-Camacho, J., Vázquez-Garcidueñas, M.S. et al. Corn stover induces extracellular laccase activity in Didymosphaeria sp. (syn. = Paraconiothyrium sp.) and exhibits increased in vitro ruminal digestibility when treated with this fungal species. Folia Microbiol 65, 849–861 (2020). https://doi.org/10.1007/s12223-020-00795-4
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DOI: https://doi.org/10.1007/s12223-020-00795-4