Abstract
In coffee-producing countries, waste products from coffee production are useful substrates for cultivation of Pleurotus ostreatus. This species is relatively easy to grow, coffee waste substrates are readily available and the mushroom fruiting bodies are a valuable source of nutrition and income. In developed countries, cultivation of P. ostreatus on spent coffee grounds (SCG) from coffee consumption is a novel way to recycle this urban waste product. Here, we studied the effect of SCG and caffeine on growth of a commercial strain of P. ostreatus in liquid and solid cultures, and on a commercial scale. The presence of caffeine inhibited mycelial growth on agar and in liquid culture in the laboratory. Increased levels of SCG in an SCG/sawdust substrate also delayed mycelial growth and delayed or prevented fruiting during commercial cultivation. Despite growth inhibition, partial degradation of caffeine to xanthine by P. ostreatus mycelium was observed in all SCG-containing substrate mixtures. Degradation of caffeine proceeded mainly via sequential N-demethylation to theophylline (1,3-dimethylxanthine) and 3-methylxanthine, although both paraxanthine and theobromine also accumulated in the substrate. Caffeine and its demethylated metabolites were also detected in fruiting bodies, but it was not clear whether caffeine metabolism occurred in the fruiting bodies themselves or whether caffeine metabolites were translocated there from the mycelium. Based on the caffeine concentrations measured in fruiting bodies after growth with SCG, it would be necessary to consume ~ 250 kg of fresh oyster mushrooms to obtain the amount of caffeine equivalent to one cup of espresso coffee, suggesting that the health impact of caffeine in these mushrooms is low. However, the ability of P. ostreatus to degrade caffeine indicates that this and other species in this genus may have potential applications in detoxification of coffee production wastes.








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References
Bermúdez RC, García N, Gross P, Serrano M (2001) Cultivation of Pleurotus on agricultural substrates in Cuba. Micol Apl Int 13:25–29
Brand D, Pandey A, Roussos S, Soccol CR (2000) Biological detoxification of coffee husk by filamentous fungi using a solid state fermentation system. Enzym Microb Technol 27:127–133. https://doi.org/10.1016/s0141-0229(00)00186-1
Campos-Vega R, Loarca-Pina G, Vergara-Castaneda HA, Oomah BD (2015) Spent coffee grounds: a review on current research and future prospects. Trends Food Sci Technol 45:24–36. https://doi.org/10.1016/j.tifs.2015.04.012
Castanera R, Perez G, Omarini A, Alfaro M, Pisabarro AG, Faraco V, Amore A, Ramirez L (2012) Transcriptional and enzymatic profiling of Pleurotus ostreatus laccase genes in submerged and solid-state fermentation cultures. Appl Environ Microbiol 78:4037–4045. https://doi.org/10.1128/aem.07880-11
Chandravanshi MK, Sairkar PK, Chouhan S, Shukla NP, Gautam SP (2012) A comparative study of mycoprotein conversion potency of seven different species of Pleurotus from various agro-wastes. Int J Agri Sci 2:149–160
Cheung PCK (2010) Nutritional value and health benefits of mushrooms Nutr Bull 35:292–299
Cohen R, Persky L, Hadar Y (2002) Biotechnological applications and potential of wood-degrading mushrooms of the genus Pleurotus. Appl Microbiol Biotechnol 58:582–594. https://doi.org/10.1007/s00253-002-0930-y
Dash SS, Gummadi SN (2006) Catabolic pathways and biotechnological applications of microbial caffeine degradation. Biotechnol Lett 28:1993–2002. https://doi.org/10.1007/s10529-006-9196-2
Espresso Mushroom Company (2018) Grow your own mushrooms. https://espressomushroom.co.uk/ Accessed 11 Feb 2019
Fan L, Pandey A, Mohan R, Soccol CR (2000) Use of various coffee industry residues for the cultivation of Pleurotus ostreatus in solid state fermentation. Acta Biotechnol 20:41–52. https://doi.org/10.1002/abio.370200108
Fan L, Soccol AT, Pandey A, Vandenberghe LPD, Soccol CR (2006) Effect of caffeine and tannins on cultivation and fructification of Pleurotus on coffee husks. Braz J Microbiol 37:420–424. https://doi.org/10.1590/s1517-83822006000400003
Freitas AC, Antunes MB, Rodrigues D, Sousa S, Amorim M, Barroso MF, Carvalho A, Ferrador SM, Gomes AM (2018) Use of coffee by-products for the cultivation of Pleurotus citrinopileatus and Pleurotus salmoneo-stramineus and its impact on biological properties of extracts thereof. Int J Food Sci Technol 53:1914–1924. https://doi.org/10.1111/ijfs.13778
Gutierrez-Sanchez G, Roussos S, Augur C (2013) Effect of caffeine concentration on biomass production, caffeine degradation, and morphology of Aspergillus tamarii. Folia Microbiol 58:195–200. https://doi.org/10.1007/s12223-012-0197-3
Hakil M, Denis S, Viniegra-Gonzalez G, Augur C (1998) Degradation and product analysis of caffeine and related dimethylxanthines by filamentous fungi. Enzym Microb Technol 22:355–359. https://doi.org/10.1016/s0141-0229(97)00205-6
Hakil M, Voisinet F, Viniegra-Gonzalez G, Augur C (1999) Caffeine degradation in solid state fermentation by Aspergillus tamarii: effects of additional nitrogen sources. Process Biochem 35:103–109. https://doi.org/10.1016/s0032-9592(99)00039-4
Hernandez-Bautista J, Rodriguez-Magadan HM, Villegas-Sanchez JA, Salinas-Rios T, Ortiz-Munoz IY, Aquino-Cleto M, Lozano-Trejo S (2018) Health status and productivity of sheep fed coffee pulp during fattening. Austral J Vet Sci 50:95–99
Hernandez D, Sanchez JE, Yamasaki K (2003) A simple procedure for preparing substrate for Pleurotus ostreatus cultivation. Bioresour Technol 90:145–150. https://doi.org/10.1016/s0960-8524(03)00118-4
Janissen B, Huynh T (2018) Chemical composition and value-adding applications of coffee industry by-products: a review. Resour Conserv Recycl 128:110–117. https://doi.org/10.1016/j.resconrec.2017.10.001
Jaramillo C, Rodríguez N, Chang ST (2010) Simple methodology for the cultivation of the medicinal mushroom Ganoderma lucidum in Colombian coffee farms. In: Martinez-Carrera D, Curvetto N, Sobal M, Morales P, Mora VM (eds) Hacia un desarrollo sostenible del sistema de producción-consumo de los hongos comestibles y medicinales en Llatinoamérica: avances y perspectivas en el Siglo XXI Red Latinoamericana de Hongos Comestibles y Medicinales, Puebla, Mexico, pp 397–405
Karmee SK (2018) A spent coffee grounds based biorefinery for the production of biofuels, biopolymers, antioxidants and biocomposites. Waste Manag 72:240–254. https://doi.org/10.1016/j.wasman.2017.10.042
Kovalcik A, Obruca S, Marova N (2018) Valorization of spent coffee grounds: a review. Food Bioprod Process 110:104–119. https://doi.org/10.1016/j.fbp.2018.05.002
Lopez-Barrera DM, Vazquez-Sanchez K, Loarca-Pina MGF, Campos-Vega R (2016) Spent coffee grounds, an innovative source of colonic fermentable compounds, inhibit inflammatory mediators in vitro. Food Chem 212:282–290. https://doi.org/10.1016/j.foodchem.2016.05.175
Ma YX, Wu XH, Wu HS, Dong ZB, Ye JH, Zheng XQ, Liang YR, Lu JL (2018) Different catabolism pathways triggered by various methylxanthines in caffeine-tolerant bacterium Pseudomonas putida CT25 isolated from tea garden soil. J Microbiol Biotechnol 28:1147–1155. https://doi.org/10.4014/jmb.1801.01043
Machado EMS, Rodriguez-Jasso RM, Teixeira JA, Mussatto SI (2012) Growth of fungal strains on coffee industry residues with removal of polyphenolic compounds. Biochem Eng J 60:87–90. https://doi.org/10.1016/j.bej.2011.10.007
Martínez-Carrera D, Aguilar A, Martínez W, Bonilla M, Morales P, Sobal M (2000) Commercial production and marketing of edible mushrooms cultivated on coffee pulp in Mexico. In: Sera T, Soccol CR, Pandey A, Roussos S (eds) Coffee biotechnology and quality. Kluwer Academic Publishers, Dordrecht, pp 471–488
Mata G, Salmones D, Perez-Merlo R (2016) Hydrolytic enzyme activities in shiitake mushroom (Lentinula edodes) strains cultivated on coffee pulp. Rev Argent Microbiol 48:191–195. https://doi.org/10.1016/j.ram.2016.05.008
Mazzafera P (2004) Catabolism of caffeine in plants and microorganisms. Front Biosci 9:1348–1359. https://doi.org/10.2741/1339
Membrillo I, Sanchez C, Meneses M, Favela E, Loera O (2011) Particle geometry affects differentially substrate composition and enzyme profiles by Pleurotus ostreatus growing on sugar cane bagasse. Bioresour Technol 102:1581–1586. https://doi.org/10.1016/j.biortech.2010.08.091
Monteiro JP, Alves MG, Oliveira PF, Silva BM (2016) Structure-bioactivity relationships of methylxanthines: trying to make sense of all the promises and the drawbacks. Molecules 21:32. https://doi.org/10.3390/molecules21080974
Montoya S, Orrego CE, Levin L (2012) Growth, fruiting and lignocellulolytic enzyme production by the edible mushroom Grifola frondosa (maitake). World J Microbiol Biotechnol 28:1533–1541. https://doi.org/10.1007/s11274-011-0957-2
Mussatto SI, Machado EMS, Martins S, Teixeira JA (2011) Production, composition, and application of coffee and its industrial residues. Food Bioprocess Technol 4:661–672. https://doi.org/10.1007/s11947-011-0565-z
Nanjundaiah S, Bhatt P, Rastogi NK, Thakur MS (2016) Response surface optimization for decaffeination and theophylline production by Fusarium solani. Appl Biochem Biotechnol 178:58–75. https://doi.org/10.1007/s12010-015-1858-x
Park J, Kim B, Lee JW (2016) In-situ transesterification of wet spent coffee grounds for sustainable biodiesel production. Bioresour Technol 221:55–60. https://doi.org/10.1016/j.biortech.2016.09.001
Petrik S, Obruca S, Benesova P, Marova I (2014) Bioconversion of spent coffee grounds into carotenoids and other valuable metabolites by selected red yeast strains. Biochem Eng J 90:307–315. https://doi.org/10.1016/j.bej.2014.06.025
Philippoussis AN (2009) Production of mushrooms using agroindustrial residues as substrates. In: Nigam PS-N, Pandey A (eds) Biotechnology for agro-industrial residues utilisation. Springer, Dordrecht, pp 163–196
Ramalho AN, Kultz TW, Byczkovski GM, Groff DB, Dalla Santa HS, Torres YR (2018) Content of caffeine in the edible mushroom Pleurotus ostreatus grown in coffee residues. Orbital 10:174–182. https://doi.org/10.17807/orbital.v10i3.1096
Roussos S, Aquiahuatl MD, Trejohernandez MD, Perraud IG, Favela E, Ramakrishna M, Raimbault M, Viniegragonzalez G (1995) Biotechnological management of coffee pulp - isolation, screening, characterization, selection of caffeine degrading fungi and natural microflora in coffee pulp and husk. Appl Microbiol Biotechnol 42:756–762. https://doi.org/10.1007/bf00171958
Salinas-Rios T, Ortega-Cerrilla ME, Sanchez-Torres-Esqueda MT, Hernandez-Bautista J, Diaz-Cruz A, Figueroa-Velasco JL, Guinzberg-Perrusquia R, Cordero-Mora JL (2015) Productive performance and oxidative status of sheep fed diets supplemented with coffee pulp. Small Ruminant Res 123:17–21. https://doi.org/10.1016/j.smallrumres.2014.09.008
Salmones D, Mata G, Ramos LM, Waliszewski KN (1999) Cultivation of shiitake mushroom, Lentinula edodes, in several lignocellulosic materials originating from the subtropics. Agronomie 19:13–19. https://doi.org/10.1051/agro:19990102
Salmones D, Mata G, Waliszewski KN (2005) Comparative culturing of Pleurotus spp. on coffee pulp and wheat straw: biomass production and substrate biodegradation. Bioresour Technol 96:537–544. https://doi.org/10.1016/j.biortech.2004.06.019
Sánchez C (2010) Cultivation of Pleurotus ostreatus and other edible mushrooms. Appl Microbiol Biotechnol 85:1321–1337. https://doi.org/10.1007/s00253-009-2343-7
Stamets P (2000) Growing gourmet and medicinal mushrooms, 2 edn. Ten Speed Press, Berkeley
Stamets P, Chilton JS (1983) The mushroom cultivator. A practical guide to growing mushrooms at home. Agarikon Press, Washington
Sugiyama A, Sano CM, Yazaki K, Sano H (2016) Caffeine fostering of mycoparasitic fungi against phytopathogens. Plant Signal Behav 11:e1113362. https://doi.org/10.1080/15592324.2015.1113362
Summers RM, Mohanty SK, Gopishetty S, Subramanian M (2015) Genetic characterization of caffeine degradation by bacteria and its potential applications. Microb Biotechnol 8:369–378. https://doi.org/10.1111/1751-7915.12262
Tagliari CV, Sanson RK, Zanette A, Franco TT, Soccol CR (2003) Caffeine degradation by Rhizopus delemar in packed bed column bioreactors using coffee husk as substrate. Braz J Microbiol 34:102–104. https://doi.org/10.1590/s1517-83822003000500035
Vajna B, Nagy A, Sajben E, Manczinger L, Szijarto N, Kadar Z, Bordas D, Marialigeti K (2010) Microbial community structure changes during oyster mushroom substrate preparation. Appl Microbiol Biotechnol 86:367–375. https://doi.org/10.1007/s00253-009-2371-3
Vajna B, Szili D, Nagy A, Marialigeti K (2012) An improved sequence-aided T-RFLP analysis of bacterial succession during oyster mushroom substrate preparation. Microb Ecol 64:702–713. https://doi.org/10.1007/s00248-012-0063-5
Vieira FR, de Andrade MCN (2016) Optimization of substrate preparation for oyster mushroom (Pleurotus ostreatus) cultivation by studying different raw materials and substrate preparation conditions (composting: phases I and II). World J Microbiol Biotechnol 32:9. https://doi.org/10.1007/s11274-016-2152-y
Woldesenbet AG, Woldeyes B, Chandravanshi BS (2016) Bio-ethanol production from wet coffee processing waste in Ethiopia. SpringerPlus 5:1903. https://doi.org/10.1186/s40064-016-3600-8
Zheng YB, Xu XP, Zou XW (2016) Biotransformation of caffeine in oolong tea by Paecilomyces gunnii. Int Biodeterior Biodegrad 114:141–144. https://doi.org/10.1016/j.ibiod.2016.04.013
Acknowledgements
We are indebted to Dr. Noel Arrold of Li Sun Exotic Mushrooms, Mittagong, NSW, for providing assistance and resources for the commercial-scale experiments, detailed advice with sampling and processing and for his helpful discussions on many aspects of oyster mushroom production. We thank Charlotte’s Little Sister for providing spent coffee grounds.
Funding
CCC was supported by a scholarship from Becas Chile and by a Thomas Pawlett scholarship from the University of Sydney.
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Carrasco-Cabrera, C.P., Bell, T.L. & Kertesz, M.A. Caffeine metabolism during cultivation of oyster mushroom (Pleurotus ostreatus) with spent coffee grounds. Appl Microbiol Biotechnol 103, 5831–5841 (2019). https://doi.org/10.1007/s00253-019-09883-z
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DOI: https://doi.org/10.1007/s00253-019-09883-z



