Advertisement

Applied Microbiology and Biotechnology

, Volume 102, Issue 1, pp 499–507 | Cite as

Anaerobic digestion of spent mushroom substrate under thermophilic conditions: performance and microbial community analysis

  • Zheng Xiao
  • Manhong Lin
  • Jinlin Fan
  • Yixuan Chen
  • Chao Zhao
  • Bin LiuEmail author
Bioenergy and Biofuels

Abstract

Spent mushroom substrate (SMS) is the residue of edible mushroom production occurring in huge amounts. The SMS residue can be digested for biogas production in the mesophilic anaerobic digestion. In the present study, performance of batch thermophilic anaerobic digestion (TAD) of SMS was investigated as well as the interconnected microbial population structure changes. The analyzed batch TAD process lasted for 12 days with the cumulative methane yields of 177.69 mL/g volatile solid (VS). Hydrolytic activities of soluble sugar, crude protein, and crude fat in SMS were conducted mainly in the initial phase, accompanied by the excessive accumulation of volatile fatty acids and low methane yield. Biogas production increased dramatically from days 4 to 6. The degradation rates of cellulose and hemicellulose were 47.53 and 55.08%, respectively. The high-throughput sequencing of 16S rRNA gene amplicons revealed that Proteobacteria (56.7%–62.8%) was the dominant phylum in different fermentative stages, which was highly specific compared with other anaerobic processes of lignocellulosic materials reported in the literature. Crenarchaeota was abundant in the archaea. The most dominant genera of archaea were retrieved as Methanothermobacter and Methanobacterium, but the latter decreased sharply with time. This study shows that TAD is a feasible method to handle the waste SMS.

Keywords

Biogas Lignocellulosic biomass Proteobacteria Crenarchaeota Methanothermobacter 

Notes

Funding information

This study was funded by Natural Science Foundation of China (31370146), Collaborative Innovation for Juncao Ecology Industry (JCZXGGKT-2015001), Fujian Province Science and Technology Major Projects (2014NZ2002-1), Sub Project of National Science and Technology Support Program (2014BAD15B01-6).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

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

References

  1. APHA (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, New York,USAGoogle Scholar
  2. Bhattacharya M, Biswas D, Sana S, Datta S (2015) Biodegradation of waste lubricants by a newly isolated Ochrobactrum sp. C1. 3 Biotech 5(5):807–817.  https://doi.org/10.1007/s13205-015-0282-9 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bisaria R, Madan M, Mukhopadhyay SN (1983) Production of biogas from residues from mushroom cultivation. Biotechnol Lett 5(12):811–812.  https://doi.org/10.1007/BF01386653 CrossRefGoogle Scholar
  4. Bisaria R, Vasudevan P, Bisaria VS (1990) Utilization of spent agro-residues from mushroom cultivation for biogas production. Appl Microbiol Biotechnol 33(5):607–609.  https://doi.org/10.1007/BF00172560 CrossRefGoogle Scholar
  5. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chaturvedi V, Verma P (2015) Biodegradation of malachite green by a novel copper-tolerant Ochrobactrum pseudogrignonense strain GGUPV1 isolated from copper mine waste water. Bioresour Bioprocess 2(1).  https://doi.org/10.1186/s40643-015-0070-8
  7. Chen CL, JH W, Liu WT (2008) Identification of important microbial populations in the mesophilic and thermophilic phenol-degrading methanogenic consortia. Water Res 42(8–9):1963–1976.  https://doi.org/10.1016/j.watres.2007.11.037 CrossRefPubMedGoogle Scholar
  8. Chen X, Wang Y, Yang F, Qu Y, Li X (2015) Isolation and characterization of Achromobacter sp. CX2 from symbiotic Cytophagales, a non-cellulolytic bacterium showing synergism with cellulolytic microbes by producing β-glucosidase. Ann Microbiol 65(3):1699–1707.  https://doi.org/10.1007/s13213-014-1009-6 CrossRefGoogle Scholar
  9. CNBS (1986) Determination of soluble sugar in vegetable and fruit. China National Bureau of Standards. Beijing, ChinaGoogle Scholar
  10. Coats ER, Ibrahim I, Briones A, Brinkman CK (2012) Methane production on thickened, pre-fermented manure. Bioresour Technol 107(2):205–212.  https://doi.org/10.1016/j.biortech.2011.12.077 CrossRefPubMedGoogle Scholar
  11. Desantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072.  https://doi.org/10.1128/AEM.03006-05 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998.  https://doi.org/10.1038/nmeth.2604 CrossRefPubMedGoogle Scholar
  13. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200.  https://doi.org/10.1093/bioinformatics/btr381 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Finney KN, Ryu C, Sharifi VN, Swithenbank J (2009) The reuse of spent mushroom compost and coal tailings for energy recovery: comparison of thermal treatment technologies. Bioresour Technol 100(1):310–315.  https://doi.org/10.1016/j.biortech.2008.05.054 CrossRefPubMedGoogle Scholar
  15. Guo X, Wang C, Sun F, Zhu W, Wu W (2014) A comparison of microbial characteristics between the thermophilic and mesophilic anaerobic digesters exposed to elevated food waste loadings. Bioresour Technol 152:420–428.  https://doi.org/10.1016/j.biortech.2013.11.012 CrossRefPubMedGoogle Scholar
  16. Jang HM, Kim M-S, Ha JH, Park JM (2015) Reactor performance and methanogenic archaea species in thermophilic anaerobic co-digestion of waste activated sludge mixed with food wastewater. Chem Eng J 276:20–28.  https://doi.org/10.1016/j.cej.2015.04.072 CrossRefGoogle Scholar
  17. Kowalczyk A, Chyc M, Ryszka P, Latowski D (2016) Achromobacter xylosoxidans as a new microorganism strain colonizing high-density polyethylene as a key step to its biodegradation. Environ Sci Pollut Res Int 23(11):11349–11356.  https://doi.org/10.1007/s11356-016-6563-y CrossRefPubMedPubMedCentralGoogle Scholar
  18. Lü F, Bize A, Guillot A, Monnet V, Madigou C, Chapleur O, Mazéas L, He P, Bouchez T (2014) Metaproteomics of cellulose methanisation under thermophilic conditions reveals a surprisingly high proteolytic activity. ISME J 8(1):88–102.  https://doi.org/10.1038/ismej.2013.120 CrossRefPubMedGoogle Scholar
  19. Lin Y, Ge X, Li Y (2014) Solid-state anaerobic co-digestion of spent mushroom substrate with yard trimmings and wheat straw for biogas production. Bioresour Technol 169:468–474.  https://doi.org/10.1016/j.biortech.2014.07.020 CrossRefPubMedGoogle Scholar
  20. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963.  https://doi.org/10.1093/bioinformatics/btr507 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Mikiciński A, Sobiczewski P, Puławska J, Maciorowski R (2016) Control of fire blight (Erwinia amylovora) by a novel strain 49M of Pseudomonas graminis from the phyllosphere of apple (Malus spp.) Eur J Plant Pathol 145(2):265–276.  https://doi.org/10.1007/s10658-015-0837-y CrossRefGoogle Scholar
  22. Niu Q, Qiao W, Qiang H, Li YY (2013) Microbial community shifts and biogas conversion computation during steady, inhibited and recovered stages of thermophilic methane fermentation on chicken manure with a wide variation of ammonia. Bioresour Technol 146:223–233.  https://doi.org/10.1016/j.biortech.2013.07.038 CrossRefPubMedGoogle Scholar
  23. Niu Q, Takemura Y, Kubota K, Li YY (2015) Comparing mesophilic and thermophilic anaerobic digestion of chicken manure: microbial community dynamics and process resilience. Waste Manag 43:114–122.  https://doi.org/10.1016/j.wasman.2015.05.012 CrossRefPubMedGoogle Scholar
  24. Nordell E, Nilsson B, Nilsson Paledal S, Karisalmi K, Moestedt J (2016) Co-digestion of manure and industrial waste—the effects of trace element addition. Waste Manag 47(Pt A):21–27.  https://doi.org/10.1016/j.wasman.2015.02.032
  25. Phan CW, Sabaratnam V (2012) Potential uses of spent mushroom substrate and its associated lignocellulosic enzymes. Appl Microbiol Biotechnol 96(4):863–873.  https://doi.org/10.1007/s00253-012-4446-9 CrossRefPubMedGoogle Scholar
  26. Pivato A, Vanin S, Raga R, Lavagnolo MC, Barausse A, Rieple A, Laurent A, Cossu R (2016) Use of digestate from a decentralized on-farm biogas plant as fertilizer in soils: an ecotoxicological study for future indicators in risk and life cycle assessment. Waste Manag 49:378–389.  https://doi.org/10.1016/j.wasman.2015.12.009 CrossRefPubMedGoogle Scholar
  27. SAC (1994) Method for the determination of crude protein in feedstuffs. Standardization Administration of China, Beijing, ChinaGoogle Scholar
  28. SAC (2006) Determination of crude fat in feeds. Standardization Administration of China, Beijing, ChinaGoogle Scholar
  29. Schlüter A, Bekel T, Diaz NN, Dondrup M, Eichenlaub R, Gartemann K-H, Krahn I, Krause L, Krömeke H, Kruse O, Mussgnug JH, Neuweger H, Niehaus K, Pühler A, Runte KJ, Szczepanowski R, Tauch A, Tilker A, Viehöver P, Goesmann A (2008) The metagenome of a biogas-producing microbial community of a production-scale biogas plant fermenter analysed by the 454-pyrosequencing technology. J Biotechnol 136(1–2):77–90.  https://doi.org/10.1016/j.jbiotec.2008.05.008 CrossRefPubMedGoogle Scholar
  30. Sharma S, Madan M, Vasudevan P (1989) Biomethane production from fermented substrates. J Ferment Bioeng 68(4):296–297.  https://doi.org/10.1016/0922-338X(89)90034-2 CrossRefGoogle Scholar
  31. Shi X-S, Yuan X-Z, Wang Y-P, Zeng S-J, Qiu Y-L, Guo R-B, Wang L-S (2014) Modeling of the methane production and pH value during the anaerobic co-digestion of dairy manure and spent mushroom substrate. Chem Eng J 244:258–263.  https://doi.org/10.1016/j.cej.2014.02.007 CrossRefGoogle Scholar
  32. Singh NS, Singh DK (2011) Biodegradation of endosulfan and endosulfan sulfate by Achromobacter xylosoxidans strain C8B in broth medium. Biodegradation 22(5):845–857.  https://doi.org/10.1007/s10532-010-9442-0 CrossRefPubMedGoogle Scholar
  33. Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D (2008) Determination of structural carbohydrates and lignin in biomass. National Renewable Energy Laboratory Technical Report NREL/TP-510-42618, GoldenGoogle Scholar
  34. Stefaniuk M, Bartminski P, Rozylo K, Debicki R, Oleszczuk P (2015) Ecotoxicological assessment of residues from different biogas production plants used as fertilizer for soil. J Hazard Mater 298:195–202.  https://doi.org/10.1016/j.jhazmat.2015.05.026 CrossRefPubMedGoogle Scholar
  35. Stolze Y, Zakrzewski M, Maus I, Eikmeyer F, Jaenicke S, Rottmann N, Siebner C, Pühler A, Schlüter A (2015) Comparative metagenomics of biogas-producing microbial communities from production-scale biogas plants operating under wet or dry fermentation conditions. Biotechnol Biofuels 8:14.  https://doi.org/10.1186/s13068-014-0193-8 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Subba Reddy GV, Rafi MM, Rubesh Kumar S, Khayalethu N, Muralidhara Rao D, Manjunatha B, Philip GH, Reddy BR (2016) Optimization study of 2-hydroxyquinoxaline (2-HQ) biodegradation by Ochrobactrum sp. HQ1. 3 Biotech 6(1).  https://doi.org/10.1007/s13205-015-0358-6
  37. Sundberg C, Al-Soud WA, Larsson M, Alm E, Yekta SS, Svensson BH, Sorensen SJ, Karlsson A (2013) 454 pyrosequencing analyses of bacterial and archaeal richness in 21 full-scale biogas digesters. FEMS Microbiol Ecol 85(3):612–626.  https://doi.org/10.1111/1574-6941.12148 CrossRefPubMedGoogle Scholar
  38. Synytsya A, Míčková K, Synytsya A, Jablonský I, Spěváček J, Erban V, Kováříková E, Čopíková J (2009) Glucans from fruit bodies of cultivated mushrooms Pleurotus ostreatus and Pleurotus eryngii: structure and potential prebiotic activity. Carbohydr Polym 76(4):548–556.  https://doi.org/10.1016/j.carbpol.2008.11.021 CrossRefGoogle Scholar
  39. Tian Z, Chauliac D, Pullammanappallil P (2013) Comparison of non-agitated and agitated batch, thermophilic anaerobic digestion of sugarbeet tailings. Bioresour Technol 129:411–420.  https://doi.org/10.1016/j.biortech.2012.11.056 CrossRefPubMedGoogle Scholar
  40. Wan S, Sun L, Sun J, Luo W (2013) Biogas production and microbial community change during the co-digestion of food waste with chinese silver grass in a single-stage anaerobic reactor. Biotechnol Bioproc E 18(5):1022–1030.  https://doi.org/10.1007/s12257-013-0128-4 CrossRefGoogle Scholar
  41. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267.  https://doi.org/10.1128/AEM.00062-07 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Xu F, Li Y (2012) Solid-state co-digestion of expired dog food and corn stover for methane production. Bioresour Technol 118:219–226.  https://doi.org/10.1016/j.biortech.2012.04.102 CrossRefPubMedGoogle Scholar
  43. Yang ZH, Xu R, Zheng Y, Chen T, Zhao LJ, Li M (2016) Characterization of extracellular polymeric substances and microbial diversity in anaerobic co-digestion reactor treated sewage sludge with fat, oil, grease. Bioresour Technol 212:164–173.  https://doi.org/10.1016/j.biortech.2016.04.046 CrossRefPubMedGoogle Scholar
  44. Zakrzewski M, Goesmann A, Jaenicke S, Jünemann S, Eikmeyer F, Szczepanowski R, Al-Soud WA, Sørensen S, Pühler A, Schlüter A (2012) Profiling of the metabolically active community from a production-scale biogas plant by means of high-throughput metatranscriptome sequencing. J Biotechnol 158(4):248–258.  https://doi.org/10.1016/j.jbiotec.2012.01.020 CrossRefPubMedGoogle Scholar
  45. Zhang Z, Nan Z (2014) Erwinia persicina, a possible new necrosis and wilt threat to forage or grain legumes production. Eur J Plant Pathol 139(2):349–358.  https://doi.org/10.1007/s10658-014-0390-0 CrossRefGoogle Scholar
  46. Zheng Y, Zhao J, Xu F, Li Y (2014) Pretreatment of lignocellulosic biomass for enhanced biogas production. Prog Energ Combust 42:35–53.  https://doi.org/10.1016/j.pecs.2014.01.001 CrossRefGoogle Scholar
  47. Zhu H, Sheng K, Yan E, Qiao J, Lv F (2012) Extraction, purification and antibacterial activities of a polysaccharide from spent mushroom substrate. Int J Biol Macromol 50(3):840–843.  https://doi.org/10.1016/j.ijbiomac.2011.11.016 CrossRefPubMedGoogle Scholar
  48. Zhu J, Han M, Zhang G, Yang L (2015) Co-digestion of spent mushroom substrate and corn stover for methane production via solid-state anaerobic digestion. J Renew Sustain Ener 7(2):023135.  https://doi.org/10.1063/1.4919404 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.College of Life ScienceFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.National Engineering Research Center of JUNCAO TechnologyFuzhouChina
  3. 3.Institute of BioenergyFujian Agriculture and Forestry UniversityFuzhouChina
  4. 4.College of Food ScienceFujian Agriculture and Forestry UniversityFuzhouChina

Personalised recommendations