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Microbial Ecology

, Volume 70, Issue 4, pp 948–960 | Cite as

Effect of the Organic Loading Rate Increase and the Presence of Zeolite on Microbial Community Composition and Process Stability During Anaerobic Digestion of Chicken Wastes

  • Elvira E. Ziganshina
  • Dmitry E. Belostotskiy
  • Olga N. Ilinskaya
  • Eugenia A. Boulygina
  • Tatiana V. Grigoryeva
  • Ayrat M. Ziganshin
Environmental Microbiology

Abstract

This study investigates the effect of the organic loading rate (OLR) increase from 1.0 to 3.5 g VS L−1 day−1 at constant hydraulic retention time (HRT) of 35 days on anaerobic reactors’ performance and microbial diversity during mesophilic anaerobic digestion of ammonium-rich chicken wastes in the absence/presence of zeolite. The effects of anaerobic process parameters on microbial community structure and dynamics were evaluated using a 16S ribosomal RNA gene-based pyrosequencing approach. Maximum 12 % of the total ammonia nitrogen (TAN) was efficiently removed by zeolite in the fixed zeolite reactor (day 87). In addition, volatile fatty acids (VFA) in the fixed zeolite reactor accumulated in lower concentrations at high OLR of 3.2–3.5 g VS L−1 day−1. Microbial communities in the fixed zeolite reactor and reactor without zeolite were dominated by various members of Bacteroidales and Methanobacterium sp. at moderate TAN and VFA levels. The increase of the OLR accompanied by TAN and VFA accumulation and increase in pH led to the predominance of representatives of the family Erysipelotrichaceae and genera Clostridium and Methanosarcina. Methanosarcina sp. reached relative abundances of 94 and 57 % in the fixed zeolite reactor and reactor without zeolite at the end of the experimental period, respectively. In addition, the diminution of Synergistaceae and Crenarchaeota and increase in the abundance of Acholeplasmataceae in parallel with the increase of TAN, VFA, and pH values were observed.

Keywords

Biogas Organic loading rate Zeolite Microbial diversity Ammonia inhibition Pyrosequencing 

Notes

Acknowledgments

The work is performed according to the Russian Government Program of Competitive Growth of Kazan Federal University. Financial support was also provided by the Russian Foundation for Basic Research, Grant No. 14-08-31768. 454 Pyrosequencing was performed in the Interdisciplinary Center for Collective Use of Kazan Federal University for cellular, genomic, and post-genomic research in Volga Region (Russia).

Conflict of Interest

The authors declare that they have no competing interests.

References

  1. 1.
    Abouelenien F, Fujiwara W, Namba Y, Kosseva M (2010) Improved methane fermentation of chicken manure via ammonia removal by biogas recycle. Bioresour Technol 101:6368–6373CrossRefPubMedGoogle Scholar
  2. 2.
    Bacenetti J, Negri M, Fiala M, González-García S (2013) Anaerobic digestion of different feedstocks: impact on energetic and environmental balances of biogas process. Sci Total Environ 463–464:541–551CrossRefPubMedGoogle Scholar
  3. 3.
    Chen Y, Cheng JJ, Creamer KS (2008) Inhibition of anaerobic digestion process: a review. Bioresour Technol 99:4044–4064CrossRefPubMedGoogle Scholar
  4. 4.
    Chen S, Dong X (2005) Proteiniphilum acetatigenes gen. nov., sp. nov., from a UASB reactor treating brewery wastewater. Int J Syst Evol Microbiol 55:2257–2261CrossRefPubMedGoogle Scholar
  5. 5.
    Cisar CR, Akiyama T, Hatley J, Arney L, Kezunovic N, Owen D (2010) PCR assay specific for chicken feces. Proc Okla Acad Sci 90:55–60PubMedCentralPubMedGoogle Scholar
  6. 6.
    Costa JC, Barbosa SG, Alves MM, Sousa DZ (2012) Thermochemical pre- and biological co-treatments to improve hydrolysis and methane production from poultry litter. Bioresour Technol 111:141–147CrossRefPubMedGoogle Scholar
  7. 7.
    Das D, Veziroglu TN (2001) Hydrogen production by biological processes: a survey of literature. Int J Hydrogen Energy 26:13–28CrossRefGoogle Scholar
  8. 8.
    Demirel B, Scherer P (2008) The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Rev Environ Sci Biotechnol 7:173–190CrossRefGoogle Scholar
  9. 9.
    Ezaki T, Kawamura Y, Li N, Li ZY, Zhao L, Shu S (2001) Proposal of the genera Anaerococcus gen. nov., Peptoniphilus gen. nov. and Gallicola gen. nov. for members of the genus Peptostreptococcus. Int J Syst Evol Microbiol 51:1521–1528CrossRefPubMedGoogle Scholar
  10. 10.
    Fontes CM, Gilbert HJ (2010) Cellulosomes: highly efficient nanomachines designed to deconstruct plant cell wall complex carbohydrates. Annu Rev Biochem 79:655–681CrossRefPubMedGoogle Scholar
  11. 11.
    Fotidis IA, Karakashev D, Kotsopoulos TA, Martzopoulos GG, Angelidaki I (2013) Effect of ammonium and acetate on methanogenic pathway and methanogenic community composition. FEMS Microbiol Ecol 83:38–48CrossRefPubMedGoogle Scholar
  12. 12.
    Fotidis IA, Karakashev D, Angelidaki I (2014) The dominant acetate degradation pathway/methanogenic composition in full-scale anaerobic digesters operating under different ammonia levels. Int J Environ Sci Technol 11:2087–2094CrossRefGoogle Scholar
  13. 13.
    Garcia ML, Angenent LT (2009) Interaction between temperature and ammonia in mesophilic digesters for animal waste treatment. Water Res 43:2373–2382CrossRefPubMedGoogle Scholar
  14. 14.
    Goberna M, Insam H, Franke-Whittle IH (2009) Effect of biowaste sludge maturation on the diversity of thermophilic bacteria and archaea in an anaerobic reactor. Appl Environ Microbiol 75:2566–2572PubMedCentralCrossRefPubMedGoogle Scholar
  15. 15.
    Hahnke S, Maus I, Wibberg D, Tomazetto G, Pühler A, Klocke M, Schlüter A (2015) Complete genome sequence of the novel Porphyromonadaceae bacterium strain ING2-E5B isolated from a mesophilic lab-scale biogas reactor. J Biotechnol 193:34–36CrossRefPubMedGoogle Scholar
  16. 16.
    Hansen KH, Angelidaki I, Ahring BK (1998) Anaerobic digestion of swine manure: inhibition by ammonia. Water Res 32:5–12CrossRefGoogle Scholar
  17. 17.
    Ho DP, Jensen PD, Batstone DJ (2013) Methanosarcinaceae and acetate-oxidizing pathways dominate in high-rate thermophilic anaerobic digestion of waste-activated sludge. Appl Environ Microbiol 79:6491–6500PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Karakashev D, Batstone DJ, Trably E, Angelidaki I (2006) Acetate oxidation is the dominant methanogenic pathway from acetate in the absence of Methanosaetaceae. Appl Environ Microbiol 72:5138–5141PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    Karlsson A, Einarsson P, Schnürer A, Sundberg C, Ejlertsson J, Svensson B (2012) Impact of trace element addition on degradation efficiency of volatile fatty acids, oleic acid and phenyl acetate and on microbial populations in a biogas digester. J Biosci Bioeng 114:446–452CrossRefPubMedGoogle Scholar
  20. 20.
    Kotsopoulos TA, Karamanlis X, Dotas D, Martzopoulos GG (2008) The impact of different natural zeolite concentrations on the methane production in thermophilic anaerobic digestion of pig waste. Biosystems Eng 99:105–111CrossRefGoogle Scholar
  21. 21.
    Kougias PG, Fotidis IA, Zaganas ID, Kotsopoulos TA, Martzopoulos GG (2013) Zeolite and swine inoculum effect on poultry manure biomethanation. Int Agrophys 27:169–173CrossRefGoogle Scholar
  22. 22.
    Krause L, Diaz NN, Edwards RA, Gartemann KH, Krömeke H, Neuweger H, Pühler A, Runte KJ, Schlüter A, Stoye J, Szczepanowski R, Tauch A, Goesmann A (2008) Taxonomic composition and gene content of a methane-producing microbial community isolated from a biogas reactor. J Biotechnol 136:91–101CrossRefPubMedGoogle Scholar
  23. 23.
    Kröber M, Bekel T, Diaz NN, Goesmann A, Jaenicke S, Krause L, Miller D, Runte KJ, Viehöver P, Pühler A, Schlüter A (2009) Phylogenetic characterization of a biogas plant microbial community integrating clone library 16S-rDNA sequences and metagenome sequence data obtained by 454-pyrosequencing. J Biotechnol 142:38–49CrossRefPubMedGoogle Scholar
  24. 24.
    Li A, Chu Y, Wang X, Ren L, Yu J, Liu X, Yan J, Zhang L, Wu S, Li S (2013) A pyrosequencing-based metagenomic study of methane-producing microbial community in solid-state biogas reactor. Biotechnol Biofuels 6:3PubMedCentralCrossRefPubMedGoogle Scholar
  25. 25.
    Li YF, Nelson MC, Chen PH, Graf J, Li Y, Yu Z (2014) Comparison of the microbial communities in solid-state anaerobic digestion (SS-AD) reactors operated at mesophilic and thermophilic temperatures. Appl Microbiol Biotechnol 99:969–980CrossRefPubMedGoogle Scholar
  26. 26.
    MacLean D, Jones JD, Studholme DJ (2009) Application of ‘next-generation’ sequencing technologies to microbial genetics. Nat Rev Microbiol 7:287–296PubMedGoogle Scholar
  27. 27.
    Milán Z, Montalvo S, Ruiz-Tagle N, Urrutia H, Chamy R, Sánchez E, Borja R (2010) Influence of heavy metal supplementation on specific methanogenic activity and microbial communities detected in batch anaerobic digesters. J Environ Sci Health A 45:1307–1314CrossRefGoogle Scholar
  28. 28.
    Milán Z, Sánchez E, Weiland P, Borja R, Martín A, Ilangovan K (2001) Influence of different natural zeolite concentrations on the anaerobic digestion of piggery waste. Bioresour Technol 80:37CrossRefPubMedGoogle Scholar
  29. 29.
    Montalvo S, Guerrero L, Borja R, Sánchez E, Milán Z, Cortés I, De la Rubia AM (2012) Application of natural zeolites in anaerobic digestion processes: a review. Appl Clay Sci 58:125–133CrossRefGoogle Scholar
  30. 30.
    Nikolaeva S, Sánchez E, Borja R, Raposo F, Colmenarejo MF, Montalvo S, Jiménez-Rodríguez AM (2009) Kinetics of anaerobic degradation of screened dairy manure by upflow fixed bed digesters: effect of natural zeolite addition. J Environ Sci Health A Tox Hazard Subst Environ Eng 44:146–154CrossRefPubMedGoogle Scholar
  31. 31.
    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 146:223–233CrossRefPubMedGoogle Scholar
  32. 32.
    Oksanen J (2011) Multivariate analysis of ecological communities in R: vegan tutorial. Publisher Univ Oulu Comput Serv Cent 83:1–43Google Scholar
  33. 33.
    Raes J, Foerstner KU, Bork P (2007) Get the most out of your metagenome: computational analysis of environmental sequence data. Curr Opin Microbiol 10:490–498CrossRefPubMedGoogle Scholar
  34. 34.
    Ramasamy D, Lagier JC, Nguyen TT, Raoult D, Fournier PE (2013) Non contiguous-finished genome sequence and description of Dielma fastidiosa gen. nov., sp. nov., a new member of the family Erysipelotrichaceae. Stand Genomic Sci 8:336–351PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Rao AG, Prakash SS, Joseph J, Reddy AR, Sarma PN (2011) Multi stage high biomethanation of poultry litter with self mixed anaerobic digester. Bioresour Technol 102:729–735CrossRefPubMedGoogle Scholar
  36. 36.
    Rivière D, Desvignes V, Pelletier E, Chaussonnerie S, Guermazi S, Weissenbach J, Li T, Camacho P, Sghir A (2009) Towards the definition of a core of microorganisms involved in anaerobic digestion of sludge. ISME J 3:700–714CrossRefPubMedGoogle Scholar
  37. 37.
    Schiefer-Ullrich H, Andreesen JR (1985) Peptostreptococcus barnesae sp. nov., a Gram-positive, anaerobic, obligately purine utilizing coccus from chicken feces. Arch Microbiol 143:26–31CrossRefGoogle Scholar
  38. 38.
    Schmidt T, Ziganshin AM, Nikolausz M, Scholwin F, Nelles M, Kleinsteuber S, Pröter J (2014) Effects of the reduction of the hydraulic retention time to 1.5 days at constant organic loading in CSTR, ASBR, and fixed-bed reactors—performance and methanogenic community composition. Biomass Bioenergy 69:241–248CrossRefGoogle Scholar
  39. 39.
    Schnürer A, Nordberg A (2008) Ammonia, a selective agent for methane production by syntrophic acetate oxidation at mesophilic temperature. Water Sci Technol 57:735–740CrossRefPubMedGoogle Scholar
  40. 40.
    Schnürer A, Schink B, Svensson BH (1996) Clostridium ultunense sp. nov., a mesophilic bacterium oxidizing acetate in syntrophic association with a hydrogenotrophic methanogenic bacterium. Int J Syst Bacteriol 46:1145–1152CrossRefPubMedGoogle Scholar
  41. 41.
    Schnürer A, Zellner G, Svensson BH (1999) Mesophilic syntrophic acetate oxidation during methane formation in biogas reactors. FEMS Microbiol Ecol 29:249–261CrossRefGoogle Scholar
  42. 42.
    Smith AM, Sharma D, Lappin-Scott H, Burton S, Huber DH (2013) Microbial community structure of a pilot-scale thermophilic anaerobic digester treating poultry litter. Appl Microbiol Biotechnol 98:2321–2334CrossRefPubMedGoogle Scholar
  43. 43.
    St-Pierre B, Wright AD (2014) Comparative metagenomic analysis of bacterial populations in three full-scale mesophilic anaerobic manure digesters. Appl Microbiol Biotechnol 98:2709–2717CrossRefPubMedGoogle Scholar
  44. 44.
    Sun L, Müller B, Westerholm M, Schnürer A (2014) Syntrophic acetate oxidation in industrial CSTR biogas digesters. J Biotechnol 171:39–44CrossRefPubMedGoogle Scholar
  45. 45.
    Sundberg C, Al-Soud WA, Larsson M, Alm E, Yekta SS, Svensson BH, Sørensen SJ, Karlsson A (2013) 454 pyrosequencing analyses of bacterial and archaeal richness in 21 full-scale biogas digesters. FEMS Microbiol Ecol 85:612–626CrossRefPubMedGoogle Scholar
  46. 46.
    Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072PubMedCentralCrossRefPubMedGoogle Scholar
  47. 47.
    Town J, Annand H, Pratt D, Dumonceaux T, Fonstad T (2014) Microbial community composition is consistent across anaerobic digesters processing wheat-based fuel ethanol waste streams. Bioresour Technol 157:127–133CrossRefPubMedGoogle Scholar
  48. 48.
    Ueki A, Akasaka H, Suzuki D, Ueki K (2006) Paludibacter propionicigenes gen. nov., sp. nov., a novel strictly anaerobic, Gram-negative, propionate-producing bacterium isolated from plant residue in irrigated rice-field soil in Japan. Int J Syst Evol Microbiol 56:39–44CrossRefPubMedGoogle Scholar
  49. 49.
    Vichuviwat R, Boonsombuti A, Luengnaruemitchai A, Wongkasemjit S (2014) Enhanced butanol production by immobilized Clostridium beijerinckii TISTR 1461 using zeolite 13× as a carrier. Bioresour Technol 172:76–82CrossRefPubMedGoogle Scholar
  50. 50.
    Wang Q, Yang Y, Yu C, Huang H, Kim M, Feng C, Zhang Z (2011) Study on a fixed zeolite bioreactor for anaerobic digestion of ammonium-rich swine wastes. Bioresour Technol 102:7064–7068CrossRefPubMedGoogle Scholar
  51. 51.
    Weiland P (2010) Biogas production: current state and perspectives. Appl Microbiol Biotechnol 85:849–860CrossRefPubMedGoogle Scholar
  52. 52.
    Weiß S, Lebuhn M, Andrade D, Zankel A, Cardinale M, Birner-Gruenberger R, Somitsch W, Ueberbacher BJ, Guebitz GM (2013) Activated zeolite-suitable carriers for microorganisms in anaerobic digestion processes? Appl Microbiol Biotechnol 97:3225–3238CrossRefPubMedGoogle Scholar
  53. 53.
    Weiss S, Zankel A, Lebuhn M, Petrak S, Somitsch W, Guebitz GM (2011) Investigation of microorganisms colonizing activated zeolites during anaerobic biogas production from grass silage. Bioresour Technol 102:4353–4359CrossRefPubMedGoogle Scholar
  54. 54.
    Westerholm M, Dolfing J, Sherry A, Gray ND, Head IM, Schnürer A (2011) Quantification of syntrophic acetate-oxidizing microbial communities in biogas processes. Environ Microbiol Rep 3:500–505PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    Wirth R, Kovács E, Maróti G, Bagi Z, Rákhely G, Kovács KL (2012) Characterization of a biogas-producing microbial community by short-read next generation DNA sequencing. Biotechnol Biofuels 5:41PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Wu S, Wang G, Angert ER, Wang W, Li W, Zou H (2012) Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS ONE 7:e30440PubMedCentralCrossRefPubMedGoogle Scholar
  57. 57.
    Xing J, Criddle C, Hickey R (1997) Effects of a long-term periodic substrate perturbation on an anaerobic community. Water Res 31:2195–2204CrossRefGoogle Scholar
  58. 58.
    Zakrzewski M, Goesmann A, Jaenicke S, Junemann S, Eikmeyer F, Szczepanowski R, Abu Al-Soud W, Sorensen S, Puhler A, Schluter A (2012) Profiling of the metabolically active community from a production-scale biogas plant by means of high throughput metatranscriptome sequencing. J Biotechnol 158:248–258CrossRefPubMedGoogle Scholar
  59. 59.
    Zhao C, Gao Z, Qin Q, Ruan L (2011) Mangroviflexus xiamenensis gen. nov., sp. nov., a member of the family Marinilabiaceae isolated from mangrove sediment. Int J Syst Evol Microbiol 62:1819–1824CrossRefPubMedGoogle Scholar
  60. 60.
    Zhilina TN, Appel R, Probian C, Brossa EL, Harder J, Widdel F, Zavarzin GA (2004) Alkaliflexus imshenetskii gen. nov. sp. nov., a new alkaliphilic gliding carbohydrate-fermenting bacterium with propionate formation from a soda lake. Arch Microbiol 182:244–253CrossRefPubMedGoogle Scholar
  61. 61.
    Ziganshin AM, Gerlach R, Naumenko EA, Naumova RP (2010) Aerobic degradation of 2,4,6-trinitrotoluene by the yeast strain Geotrichum candidum AN-Z4. Microbiology 79:178–183CrossRefGoogle Scholar
  62. 62.
    Ziganshin AM, Liebetrau J, Pröter J, Kleinsteuber S (2013) Microbial community structure and dynamics during anaerobic digestion of various agricultural waste materials. Appl Microbiol Biotechnol 97:5161–5174CrossRefPubMedGoogle Scholar
  63. 63.
    Ziganshin AM, Naumova RP, Pannier AJ, Gerlach R (2010) Influence of pH on 2,4,6-trinitrotoluene degradation by Yarrowia lipolytica. Chemosphere 79:426–433CrossRefPubMedGoogle Scholar
  64. 64.
    Ziganshin AM, Schmidt T, Scholwin F, Il’inskaya ON, Harms H, Kleinsteuber S (2011) Bacteria and archaea involved in anaerobic digestion of distillers grains with solubles. Appl Microbiol Biotechnol 89:2039–2052CrossRefPubMedGoogle Scholar
  65. 65.
    Ziganshin AM, Ziganshina EE, Pröter J, Kleinsteuber S, Il’inskaya ON (2012) Methanogenic community dynamics during anaerobic utilization of agricultural wastes. Acta Nat 4:91–97Google Scholar
  66. 66.
    Ziganshina EE, Bagmanova AR, Khilyas IV, Ziganshin AM (2014) Assessment of a biogas-generating microbial community diversity in a pilot-scale anaerobic reactor. J Biosci Bioeng 117:730–736CrossRefPubMedGoogle Scholar
  67. 67.
    Ziganshina EE, Belostotskiy DE, Shushlyaev RV, Miluykov VA, Vankov PY, Ziganshin AM (2014) Microbial community diversity in anaerobic reactors digesting turkey, chicken, and swine wastes. J Microbiol Biotechnol 24:1464–1472PubMedGoogle Scholar
  68. 68.
    Zverlov VV, Hiegl W, Köck DE, Kellermann J, Köllmeier T, Schwarz WH (2010) Hydrolytic bacteria in mesophilic and thermophilic degradation of plant biomass. Eng Life Sci 10:528–536CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Elvira E. Ziganshina
    • 1
  • Dmitry E. Belostotskiy
    • 2
  • Olga N. Ilinskaya
    • 1
  • Eugenia A. Boulygina
    • 3
  • Tatiana V. Grigoryeva
    • 3
  • Ayrat M. Ziganshin
    • 1
  1. 1.Department of MicrobiologyKazan (Volga Region) Federal UniversityKazanRussia
  2. 2.Department of Technologies, A. E. Arbuzov Institute of Organic and Physical ChemistryRussian Academy of SciencesKazanRussia
  3. 3.Laboratory of Omics TechnologiesKazan (Volga Region) Federal UniversityKazanRussia

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