Library Subscription: Guest
Begell Digital Portal Begell Digital Library eBooks Journals References & Proceedings Research Collections
International Journal of Medicinal Mushrooms
IF: 1.423 5-Year IF: 1.525 SJR: 0.431 SNIP: 0.716 CiteScore™: 2.6

ISSN Print: 1521-9437
ISSN Online: 1940-4344

International Journal of Medicinal Mushrooms

DOI: 10.1615/IntJMedMushrooms.2020035958
pages 919-929

Ligno(hemi)cellulolytic Enzyme Profiles during the Developmental Cycle of the Royal Oyster Medicinal Mushroom Pleurotus eryngii (Agaricomycetes) Grown on Supplemented Agri-Wastes

Tao Tao Ni
Institute of Edible Fungi, 1018 Jinqi Road, Shanghai Academy of Agricultural Sciences, Shanghai 201403, P.R. China
Xiaoyan Zhao
Institute of Agri-Food Standards and Testing Technology, 1018 Jinqi Road, Shanghai Academy of Agricultural Sciences, Shanghai 201403, P.R. China
Zengtao Xing
Institute of Agri-Food Standards and Testing Technology, 1018 Jinqi Road, Shanghai Academy of Agricultural Sciences, Shanghai 201403, P.R. China
Qi Tan
National Engineering Research Center of Edible Fungi, Ministry of Science and Technology (MOST), Key Laboratory of Edible Fungal Resources and Utilization (South), Key Laboratory of Agricultural Genetics and Breeding of Shanghai, Institute of Edible Fungi, Shanghai Academy of Agricultural Sciences, Shanghai 201403, China
John A. Buswell
Institute of Edible Fungi, 1018 Jinqi Road, Shanghai Academy of Agricultural Sciences, Shanghai 201403, P.R. China

ABSTRACT

We have determined the production profiles of major ligno(hemi)cellulolytic enzymes at different stages of the mushroom development cycle during industrial scale cultivation of Pleurotus eryngii on supplemented agri-wastes. Endo-1,4-β-glucanase, cellobiohydrolase and endoxylanase levels remained relatively low during substrate colonization, increased sharply when small fruit bodies appeared, and peaked at maturation. β-Glucosidase and β-xylosidase levels decreased when substrate colonization was complete, increased with the appearance of small fruit bodies and primordia, respectively, and reached maxima at maturation. Laccase peaked along with substrate colonization but, after falling sharply in the upper substrate layers, remained relatively low until postinduction. Levels increased slightly when primordia appeared, fell to minimal values during the small and mature fruit body stages, and increased again postharvest. Manganese peroxidase (Mn-P) exhibited a similar pattern initially but high enzyme levels also coincided with primordia formation. Laccase and Mn-P activity patterns were compatible with a lignin-degradation function associated with substrate colonization and, in the former case, a putative role in fruit body morphogenesis. Based on the relatively low levels of polysaccharidases recorded during the initial stages of substrate colonization, we conclude that reducing sugar levels in noncolonized substrate were adequate for sustainable vegetative growth at that stage. We further conclude that the increase in enzyme production later in the developmental cycle was consistent with the replenishment of depleted reducing sugar from cellulose in the growth substrate to levels required for fruit body formation. These data provide new information describing combined temporal and spatial enzyme production profiles throughout the mushroom development cycle under a set of conditions used in industrial scale production.

REFERENCES

  1. Stajic M, Vukojevic J, Duletic-Lausevic S. Biology of Pleurotus eryngii and role in biotechnological processes: A review. Crit Rev Biotechnol. 2009;29:55-66.

  2. Wasser SP, Weis AL. Medicinal properties of substances occurring in higher Basidiomycetes mushrooms: Current perspectives (review). Int J Med Mushrooms. 1999;1:31-62.

  3. Zhang B, Li Y, Zhang F, Linhardt RJ, Zeng G, Zhang A. Extraction, structure and bioactivities of the polysaccharides from Pleurotus eryngii: A review. Int J Biol Macromol. 2020;150:1342-47.

  4. Avni S, Ezove N, Hanani H, Yadid I, Karpovsky M, Hayby H, Gover Y, Hadar Y, Schwarz B, Danay O. Olive mill waste enhances a-glucan content in the edible mushroom Pleurotus eryngii. Int J Mol Sci. 2017;18:1564.

  5. Kikuchi T, Maekawa Y, Tomio A, Masumoto Y, Yamamoto T, Taishi I, Yasuko YT, Tanaka R. Six new ergostane-type steroids from king trumpet mushroom (Pleurotus eryngii) and their inhibitory effects on nitric oxide production. Steroids. 2016;115:9-17.

  6. Cateni F, Zacchigna M, Procida G, Venturella G, Ferraro V, Gargano ML. Polysaccharides from Pleurotus eryngii var. elaeoselini (Agaricomycetes), a new potential culinary-medicinal oyster mushroom from Italy. Int J Med Mushrooms. 2020;22:431-44.

  7. Wasser SP. Medicinal mushroom science: History, current status, future trends and unsolved problems. Int J Med Mushrooms 2010;12:1-16.

  8. Chien R-C, Yang Y-C, Lai EI, Mau J-L. Anti-inflammatory effects of extracts from the medicinal mushrooms Hypsizygus marmoreus and Pleurotus eryngii (Agaricomycetes). Int J Med Mushrooms. 2016;18:477-87.

  9. Yuan B, Zhao LY, Rakariyatham K, Han YH, Gao ZL, Kimatu BM, Hu QH, Xiao H. Isolation of a novel bioactive protein from an edible mushroom Pleurotus eryngii and its anti-inflammatory potential. Food Funct. 2017;8:2175-83.

  10. Choi J-H, Kim D-W, Kim S, Kim S-J. In vitro antioxidant and in vivo hypolipidemic effects of the king oyster culinary-medicinal mushroom, Pleurotus eryngii var. ferulae DDL01 (Agaricomycetes), in rats with high-fat diet-induced fatty liver and hyperlipidemia. Int J Med Mushrooms. 2017;19:107-19.

  11. Sun YA, Hu XL, Li WX. Antioxidant, antitumor and immunostimulatory activities of the polypeptide from Pleurotus eryngii mycelium. Int J Biol Macromol. 2017;97:323-30.

  12. Zhang C, Li SS, Zhang JJ, Hu CL, Che G, Zhou M, Jia L. Antioxidant and hepatoprotective activities of intracellular polysaccharide from Pleurotus eryngii SI-04. Int J Biol Macromol. 2016;91:568-77.

  13. Jia XW, Wang C, Bai YH, Yu JW, Xu CP. Sulfation of the extracellular polysaccharide produced by the king oyster culinary-medicinal mushroom, Pleurotus eryngii (Agaricomycetes), and its antioxidant properties in vitro. Int J Med Mushrooms. 2017;19:355-62.

  14. Vetvicka V, Gover O, Hayby H, Danay O, Ezov N, Hadar Y, Schwartz B. Immunomodulating effects exerted by glucans extracted from the king oyster culinary-medicinal mushroom Pleurotus eryngii (Agaricomycetes) grown in substrates containing various concentrations of olive mill waste. Int J Med Mushrooms. 2019;21:765-81.

  15. Mariga AM, Yang WJ, Mugambi DK, Pei F, Zhao LY, Shao YN, Hu Q. Antiproliferative and immunostimulatory activity of a protein from Pleurotus eryngii. J Sci Food Agric. 2014;94:3152-62.

  16. Mizutani T, Inatomi S, Inazu A, Kawahara E. Hypolipidemic effect of Pleurotus eryngii extract in fat-loaded mice. Nutr Sci Vitaminol (Tokyo). 2010;56:48-53.

  17. Chen JJ, Mao D, Yong YY, Li JL, Wei H, Lu L. Hepatoprotective and hypolipidemic effects of water-soluble polysaccharide extract of Pleurotus eryngii. Food Chem. 2012;130:687-94.

  18. Mori K, Kobayashi C, Tomita T, Inatomi S, Ikeda M. Antiatherosclerotic effect of the edible mushrooms Pleurotus eryngii (Eringi), Grifola frondosa (Maitake) and Hypsizygus marmoreus (Bunashimeji) in apolipoprotein E-deficient mice. Nutr Res. 2008;28:335-42.

  19. Yuan B, Ma N, Zhao L, Zhao E, Gao Z, Wang W, Song M, Zhang G, Hu Q, Xiao H. In vitro and in vivo inhibitory effects of a Pleurotus eryngii protein on colon cancer cells. Food Funct. 2017;8:3553-62.

  20. Xue Z, Zhai L, Yu W, Wang H. Antitumor and immunomodulatory activity of Pleurotus eryngii extract. J Food Chem. 2015:39:19-27.

  21. Ren DY, Wang N, Guo JJ, Yuan L, Yang XB. Chemical characterization of Pleurotus eryngii polysaccharide and its tumor-in-hibitory effects against human hepatoblastoma HepG-2 cells. Carbohydr Polym. 2016;138:123-33.

  22. Yang ZY, Xu J, Fu Q, Fu XL, Shu T, Bi YP, Song B. Antitumor activity of a polysaccharide from Pleurotus eryngii on mice bearing renal cancer. Carbohydr Polym. 2013;95:615-20.

  23. Xue Z, Li J, Cheng A, Yu W, Zhang Z, Kou X, Zhou F. Structure identification of triterpene from the mushroom Pleurotus eryngii with inhibitory effects against breast cancer. Plant Foods Hum Nutr. 2015;70:291-6.

  24. Kim SW, Kim HG, Lee BE, Hwang HH, Baek DH, Ko SY. Effects of mushroom, Pleurotus eryngii, extracts on bone metabolism. Clin Nutr. 2006;25:166-70.

  25. Shimizu K, Yamanaka M, Gyokusen M, Kaneko S, Tsutsui M, Sato J, Sato I, Sato M, Kondo R. Estrogen-like activity and prevention effect of bone loss in calcium deficient ovariectomized rats by the extract of Pleurotus eryngii. Phytother Res. 2006;20:659-64.

  26. Nelson N. A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem. 1944;153: 375-80.

  27. Somogyi M. Notes on sugar determination. J Biol Chem. 1952;195:19-23.

  28. Bourbonnais R, Paice MG. Veratryl alcohol oxidase from the lignin-degrading basidiomycete Pleurotus sajor-caju. Biochem J. 1988;255:445-50.

  29. Aitken MD, Irvine RL. Characterization of reactions catalyzed by manganese peroxidase from Phanerochaete chrysosporium. Arch Biochem Biophys. 1990;276:405-14.

  30. Bradford MM. A rapid and sensitive method for detecting microgram amounts of protein utilizing the principle of proteindye binding. Anal Biochem. 1976;72:248-54.

  31. Wood DA, Claydon N, Dudley KJ, Stephens SK, Allan M. Cellulase production in the life cycle of the cultivated mushroom Agaricus bisporus. In: Aubert JP, Begum P, Millet J, editors. Biochemistry and genetics of cellulose degradation. London: Academic Press; 1988. p. 53-70.

  32. Cai YJ, Chapman SJ, Buswell JA, Chang ST. Production and distribution of endoglucanase, cellobiohydrolase, and P-glucosidase components of the cellulolytic system of Volvariella volvacea, the edible straw mushroom. Appl Environ Microbiol. 1999;65:553-9.

  33. Ding SJ, Ge W, Buswell JA. Cloning of multiple cellulase cDNAs from Volvariella volvacea and their differential expression during substrate colonization and fruiting. FEMS Microbiol Lett. 2006;263:207-13.

  34. Elisashvili V, Kachlishvili E, Penninckx MJ. Lignocellulolytic enzymes profile during growth and fruiting of Pleurotus ostreatus on wheat straw and tree leaves. Acta Microbiol Immunol Hung. 2008;55:157-68.

  35. Bonnen L, Anton LH, Orth AB. Lignin-degrading enzymes of the commercial button mushroom, Agaricus bisporus. Appl Environ Microbiol. 1994;60:960-5.

  36. Ohga S, Royse DJ. Transcriptional regulation of laccase and cellulase genes during growth and fruiting of Lentinula edodes on supplemented sawdust. FEMS Microbiol Lett. 2001;201:111-5.

  37. Chen S, Ge W, Buswell JA. Molecular cloning of a new laccase from the edible straw mushroom Volvariella volvacea: Possible involvement in fruit body development. FEMS Microbiol Lett. 2004;230:171-6.

  38. Xie CL, Luo W, Li ZM, Yan L, Zhu ZH, Wang J, Hu ZX, Peng YD. Secretome analysis of Pleurotus eryngii reveals enzymatic composition for ramie stalk degradation. Electrophoresis. 2016;37:310-20.

  39. Xie CL, Xie LY, Gong WB, Zhu ZH, Tan, SW, Chen D, Hu ZX, Peng YD. Effects of different substrates on lignocellulosic enzyme expression, enzyme activity, substrate utilization and biological efficiency of Pleurotus eryngii. Cell Physiol Biochem. 2016;39:1479-94.

  40. Chen S, Ma DB, Ge W, Buswell JA. Induction of laccase activity in the edible straw mushroom, Volvariella volvacea. FEMS Microbiol Lett. 2003;218:143-8.

  41. De Vries OMH, Koolstra WHCF, Wessels GH. Formation of an extracellular laccase by Schizophyllum commune dikaryon. J Gen Microbiol. 1986;132:2817-26.


Articles with similar content:

Effect of the Carbon Source and Inoculum Preparation Method on Laccase and Manganese Peroxidase Production in Submerged Cultivation by the Medicinal Mushroom Ganoderma lucidum (W. Curt.: Fr.) P. Karst. (Aphyllophoromycetideae)
International Journal of Medicinal Mushrooms, Vol.10, 2008, issue 1
George G. Songulashvili, Yitzhak Hadar, Vladimir I. Elisashvili, Eviatar D. Nevo
Shiitake Medicinal Mushroom, Lentinus edodes (Higher Basidiomycetes) Productivity and Lignocellulolytic Enzyme Profiles during Wheat Straw and Tree Leaf Bioconversion
International Journal of Medicinal Mushrooms, Vol.17, 2015, issue 1
Eva Kachlishvili, Mikheil D. Asatiani, Vladimir I. Elisashvili
Bioconversion of Plant Raw Materials in Value-Added Products by Lentinus edodes (Berk.) Singer and Pleurotus spp.
International Journal of Medicinal Mushrooms, Vol.7, 2005, issue 3
George G. Songulashvili, Nana Aladashvili, Yitzhak Hadar, Michel Penninckx, Mikheil D. Asatiani, Eka Metreveli, Vladimir I. Elisashvili
Vineyard Pruning Waste Improves Bioconversion and Chemical Composition of Native Ganoderma spp. (Agaricomycetes) Strains from Mexico
International Journal of Medicinal Mushrooms, Vol.20, 2018, issue 8
Idaly Morales-Estrada, Aldo Gutiérrez, Georgina Vargas, Rigoberto Gaitán-Hernández, Alberto Jiménez, Agustin Rascón, Martín Esqueda
Purification and Particular Characterization of Laccase from the Ling Zhi or Reishi Medicinal Mushroom Ganoderma lucidum (W. Curt.: Fr.) P. Karst. 447 (Aphyllophoromycetideae)
International Journal of Medicinal Mushrooms, Vol.10, 2008, issue 4
George G. Songulashvili, Yitzhak Hadar, Vladimir I. Elisashvili, Eviatar D. Nevo