Advertisement

Applied Microbiology and Biotechnology

, Volume 100, Issue 13, pp 6013–6033 | Cite as

Archaeal and bacterial community dynamics and bioprocess performance of a bench-scale two-stage anaerobic digester

  • Alejandro Gonzalez-Martinez
  • Maria Jesus Garcia-Ruiz
  • Alejandro Rodriguez-Sanchez
  • Francisco Osorio
  • Jesus Gonzalez-Lopez
Environmental biotechnology

Abstract

Two-stage technologies have been developed for anaerobic digestion of waste-activated sludge. In this study, the archaeal and bacterial community structure dynamics and bioprocess performance of a bench-scale two-stage anaerobic digester treating urban sewage sludge have been studied by the means of high-throughput sequencing techniques and physicochemical parameters such as pH, dried sludge, volatile dried sludge, acid concentration, alkalinity, and biogas generation. The coupled analyses of archaeal and bacterial communities and physicochemical parameters showed a direct relationship between archaeal and bacterial populations and bioprocess performance during start-up and working operation of a two-stage anaerobic digester. Moreover, results demonstrated that archaeal and bacterial community structure was affected by changes in the acid/alkalinity ratio in the bioprocess. Thus, a predominance of the acetoclastic methanogen Methanosaeta was observed in the methanogenic bioreactor at high-value acid/alkaline ratio, while a predominance of Methanomassilicoccaeceae archaea and Methanoculleus genus was observed in the methanogenic bioreactor at low-value acid/alkaline ratio. Biodiversity tag-iTag sequencing studies showed that methanogenic archaea can be also detected in the acidogenic bioreactor, although its biological activity was decreased after 4 months of operation as supported by physicochemical analyses. Also, studies of the VFA producers and VFA consumers microbial populations showed as these microbiota were directly affected by the physicochemical parameters generated in the bioreactors. We suggest that the results obtained in our study could be useful for future implementations of two-stage anaerobic digestion processes at both bench- and full-scale.

Keywords

Archaeal dynamics iTag sequencing Two-stage anaerobic digestion Wastewater treatment 

Notes

Acknowledgments

The authors would like to acknowledge the support given by Entidad Regional de Saneamiento y Depuración de Aguas Residuales de la Región de Murcia (ESAMUR) and Empresa Municipal de Aguas y Saneamiento de Murcia, S.A. (EMUASA).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

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

Supplementary material

253_2016_7393_MOESM1_ESM.pdf (1.5 mb)
ESM 1 (PDF 1539 kb)

References

  1. Abbasi T, Abbasi SA (2012) Formation and impact of granules in fostering clean energy production and wastewater treatment in upflow anaerobic sludge blanket (UASB) reactors. Renew Sust Energ Rev 16:1696–1708. doi: 10.1016/j.rser.2011.11.017 CrossRefGoogle Scholar
  2. Acharya BK, Pathak H, Mohana S, Shouche Y, Singh V, Madamwar D (2011) Kinetic modelling and microbial community assessment of anaerobic biphasic fixed film bioreactor treating distillery spent wash. Water Res 45:4248–4259. doi: 10.1016/j.watres.2011.05.048 CrossRefPubMedGoogle Scholar
  3. Aguilera M, Monteoliva-Sanchez M, Suarez A, Guerra V, Lizama C, Bennasar A, Ramos-Cormenzana A (2001) Panibacillus jamilae sp. nov., an exopolysaccharide-producing bacterium able to grow in olive-mill wastewater. Int J Syst Evol Microbiol 51:1687–1692CrossRefPubMedGoogle Scholar
  4. American Public Health Association (APHA) (2005) Standard methods for the examination of water and wastewater, 21st Edition.Google Scholar
  5. Anderson GK, Kasapgil B, Ince O (1994) Microbiological study of two-stage anaerobic digestion during start-up. Wat Res 28:2383–2392CrossRefGoogle Scholar
  6. Barret M, Gagnon N, Kalmokoff ML, Topp E, Verastegui Y, Brooks SPJ, Matias F, Neufeld JD, Talbot G (2013) Identification of Methanoculleus spp. as active methanogens during anoxic incubations of swine manure storage tank samples. Appl Environ Microbiol 79:424–433. doi: 10.1128/AEM.02268-12 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Barwell LJ, Isaac NJB, Kunin WE (2015) Measuring β-diversity with species abundance data. J Animal Ecol 84:1112–1122. doi: 10.1111/1365-2656.12362 CrossRefGoogle Scholar
  8. Beale DJ, Karpe AV, McLeod JD, Gondalia SV, Muster TH, Othman MZ, Palombo EA, Joshi D (2016) An ‘omics’ approach towards the characterization of laboratory scale anaerobic digesters treating municipal sewage sludge. Water Res 88:346–357. doi: 10.1016/j.watres.2015.10.029 CrossRefPubMedGoogle Scholar
  9. Biswas K, Taylor MW, Turner SJ (2014) Successional development of biofilms in moving bed biofilm reactor (MBBR) systems treating municipal wastewater. App Microbiol Biotechnol 98:1429–1440CrossRefGoogle Scholar
  10. Borrel G, Parisot N, Harris HM, Peyretaillade E, Gaci N, Tottey W, Bardot O, Raymann K, Gribaldo S, Peyret P, O’Toole PW, Brugère J-F (2014) Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine. BMC Genomics 15:679. doi: 10.1186/1471-2164-15-679 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bowman JP, Nichols CM, Gibson JAE (2003) Algoriphagus ratkowskyi gen.nov., sp. nov., Brumimicrobium glaciale gen. nov., sp. nov., Cryomorpha ignava gen. nov., sp. nov. and Crocinitomix catalasitica gen. nov., sp. nov., novel Flavobacteria isolated from various polar habitats. Int J Syst Evol Microbiol 53:1343–1355. doi: 10.1099/ijs.0.02553-0 CrossRefPubMedGoogle Scholar
  12. Cai J, Wang Y, Liu D, Zeng Y, Xue Y, Ma Y, Feng Y (2007) Fervidobacterium changbaicum sp. nov., a novel thermophilic anaerobic bacterium isolated from hot spring of the Changbai Mountains, China. Int J Syst Evol Microbiol 57:2333–2336. doi: 10.1099/ijs.0.64758-0 CrossRefPubMedGoogle Scholar
  13. Chaudhary PP, Gaci N, Borrel G, O’Toole PW, Brugère J-F (2015) Molecular methods for studying methanogens of the human gastrointestinal tract: current status and future directions. Appl Microbiol Biotechnol 99:5801–5815. doi: 10.1007/s00253-015-6739-2 CrossRefPubMedGoogle Scholar
  14. Criminger JD, Hazen TH, Sobecky PA, Lovell CR (2007) Nitrogen fixation by Vibrio parahaemolyticus and its implications for a new ecological niche. Appl Environ Microbiol 73:5959. doi: 10.1128/AEM.00981-07 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Del Nery V, Pozzi E, Damianovic MHRZ, Domingues MR, Zaiat M (2008) Granules characteristics in the vertical profile of a full-scale upflow anaerobic sludge blanket reactor treating poultry slaughterhouse wastewater. Bioresour Technol 99:2018–2024. doi: 10.1016/j.biortech.2007.03.019 CrossRefPubMedGoogle Scholar
  16. 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 7:173–190. doi: 10.1007/s11157-008-9131-1 CrossRefGoogle Scholar
  17. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon iTag sequencing (bTEFAP). BMC Microbiol 8:125. doi: 10.1186/1471-2180-8-125 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi: 10.1093/bioinformatics/btq461 CrossRefPubMedGoogle Scholar
  19. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi: 10.1093/bioinformatics/btr381 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Ganesh R, Torrijos M, Sousbie P, Lugardon A, Steyer JP, Delgenes JP (2014) Single-phase and two-phase anaerobic digestion of fruit and vegetable waste: comparison of start-up, reactor stability and process performance. Waste Manag 34:875–885CrossRefPubMedGoogle Scholar
  21. Goh F, Leuko S, Allen MA, Bowman JP, Kamekura M, Neilan BA, Burns BP (2006) Halococcus hamelinensis sp. nov., a novel halophilic archaeon isolated from stromatolites in Shark Bay, Australia. Int J Syst Evol Microbiol 56:1323–1329. doi: 10.1099/ijs.0.64180-0 CrossRefPubMedGoogle Scholar
  22. Gonzalez-Martinez A, Osorio F, Rodriguez-Sanchez A, Martinez-Toledo MV, Gonzalez-Lopez J, Lotti T, van Loosdrecht MCM (2014b) Bacterial community structure of a lab-scale anammox membrane bioreactor. Biotechnol Prog 31:186–193. doi: 10.1002/btpr.1995 CrossRefPubMedGoogle Scholar
  23. Gonzalez-Martinez A, Rodriguez-Sanchez A, Martinez-Toledo MV, Garcia-Ruiz M-J, Hontoria E, Osorio-Robles F, Gonzalez-Lopez J (2014a) Effect of ciprofloxacin antibiotic on the partial-nitritation process and bacterial community structure of a submerged biofilter. Sci Total Environ 476-477:276–287. doi: 10.1016/j.scitotenv.2014.01.012 CrossRefPubMedGoogle Scholar
  24. Gonzalez-Martinez A, Rodriguez-Sanchez A, Munoz-Palazon B, Osorio F, van Loosdrecht MCM, Gonzalez-Lopez J (2015a) Microbial Community Analysis of a Full-Scale DEMON Bioreactor. Bioprocess Biosyst Eng 38:499–508. doi: 10.1007/s00449-014-1289-z CrossRefPubMedGoogle Scholar
  25. Gray ND, Miskin IP, Kornilova O, Curtis TP, Head IM (2002) Occurrence and activity of archaea in aerated activated sludge wastewater treatment plants. Environ Microbiol 4:158–168. doi: 10.1046/j.1462-2920.2002.00280.x CrossRefPubMedGoogle Scholar
  26. Griffin ME, McMahon KD, Mackie RI, Raskin L (1998) Methanogenic population dynamics during start-up of anaerobic digesters. Biotechnol Bioeng 5:342–355CrossRefGoogle Scholar
  27. Guo H, Yu Z, Zhang H (2015) Phylogenetic diversity of microbial communities associated with coalbed methane gas from Eastern Ordos Basin, China. Int J Coal Geol 150-151:120–126. doi: 10.1016/j.coal.2015.08.012 CrossRefGoogle Scholar
  28. Haegeman B, Hamelin J, Moriarty J, Neal P, Dushoff J, Weitz JS (2013) Robust estimation of microbial diversity in theory and in practice. ISME J 7:1092–1101. doi: 10.1038/ismej.2013.10 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hagen LH, Vivekanand V, Pope PB, Eijsink VGH, Horn SJ (2015) The effect of storage conditions on microbial community composition and biomethane potential in a biogas starter culture. App Microbiol Biotechnol 99:5749–5761. doi: 10.1007/s00253-015-6623-0 CrossRefGoogle Scholar
  30. Heeg KPoh M, Sontag M, Mumme J, Klocke M, Nettmann E (2014) Microbial communities involved in biogas production from wheat straw as the sole substrate within a two-phase solid-state anaerobic digestion. System and Appl Microbiol 37(8):590–600Google Scholar
  31. Hegler F, Posth NR, Jiang J, Kappler A (2008) Physiology of phototrophic iron(II)-oxidizing bacteria: implications for modern and ancient environments. FEMS Microbiol Ecol 66:250–260CrossRefPubMedGoogle Scholar
  32. Im W-T, Bae H-S, Yokota A, Lee ST (2004) Herbaspirillum chlorophenolicum sp. nov., a 4-chlorophenol-degrading bacterium. Int J Syst Evol Microbiol 54:851–855. doi: 10.1099/ijs.0.02812-0 CrossRefPubMedGoogle Scholar
  33. Kant R, de Vos WM, Palva A, Satokari R (2014) Immunostimulatory CpG motifs in the genome of gut bacteria and their role in human health and disease. J Medical Microbiol 63:293–308. doi: 10.1099/jmm.0.064220-0 CrossRefGoogle Scholar
  34. Kindaichi T, Yuri S, Ozaki N, Ohashi A (2012) Ecophysiological role and function of uncultured Chloroflexi in an anammox reactor. Water Sci Technol 66:2556–2561. doi: 10.2166/wst.2012.479 CrossRefPubMedGoogle Scholar
  35. Lagier J-C, Gimenez G, Robert C, Raoult D, Fournier P-E (2012) Non-contiguous finished genome sequence and description of Herbaspirillum massiliense sp. nov. Stand Gen Sci 7:200–209Google Scholar
  36. Layton BA, Cao Y, Ebentier DL, Hanley K, Balleste E, Brandao J, Byappanahalli M, Converse R, Farnleitner AH, Gentry-Shielders J, Gidley ML, Gourmelon M, Lee CS, Lee J, Lozach S, Madi T, Meijer WG, Noble R, Peed L, Reischer GH, Rodrigues R, Rose JB, Schriewer A, Sinigalliano C, Srinivasan S, Stewart J, van de Werfhost LC, Wang D, Whitman R, Wuertz S, Jay J, Holden PA, Boehm AB, Shanks O, Griffith JF (2013) Performance of human fecal anaerobe-associated PCR-based assays in a multi-laboratory method evaluation study. Water Res 47:6897–6908CrossRefPubMedGoogle Scholar
  37. Li L, He Q, Ma Y, Wang X, Peng Y (2015) Dynamics of microbial community in a mesophilic anaerobic digester treating food waste: relationship between community structure and process stability. Biores Technol 189:113–120. doi: 10.1016/j.biortech.2015.4.015 CrossRefGoogle Scholar
  38. Li YF, Chen PH, Yu Z (2014) Spatial and temporal variations of microbial community in a mixed plug-flow loop reactor fed with dairy manure. Microb Biotechnol 7:332–346. doi: 10.1111/1751-7915.12125 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lin Y, Yin J, Wang J, Tian W (2012) Performance and microbial community in hybrid anaerobic baffled reactor-constructed wetland for nitrobenzene wastewater. Bioresour Technol 118:128–135. doi: 10.1016/j.biortech.2012.05.056 CrossRefPubMedGoogle Scholar
  40. Lv W, Zhang W, Yu Z (2016) Volume ratios between the thermophilic and the mesophilic digesters of a temperature-phased anaerobic digestion system affect their performance and microbial communities. New Biotechnol 33:245–254. doi: 10.1016/j.nbt.2015.07.001 CrossRefGoogle Scholar
  41. Madsen M, Holm-Nielsen JB, Esbensen KH (2011) Monitoring of anaerobic digestion process: a review perspective. Renew Sustain Energy Reviews 15:3141–3155. doi: 10.1016/j.rser.2011.04.026 CrossRefGoogle Scholar
  42. McInerney MJ, Struchtemeyer CG, Sieber J, Moutakki H, Stams AJM, Schink B, Rohlin L, Gunsalus RP (2008) Physiology, ecology, phylogeny and genomics of microorganisms capable of syntrophic metabolism. Ann N Y Acad Sci 1125:58–72. doi: 10.1196/annals.1419.005 CrossRefPubMedGoogle Scholar
  43. McLellan SL, Huse SM, Mueller-Spitz SR, Andreishcheva EN, Sogin ML (2010) Diversity and population structure sewage-derived microorganisms in wastewater treatment plant influent. Environ Microbiol 12:378–392. doi: 10.1111/j.1462-2920.2009.02075.x CrossRefPubMedGoogle Scholar
  44. Meehan C, Bjourson AJ, McMullan G (2001) Paenibacillus azoreducens sp. nov., a synthetic azo dye decoloring bacterium from industrial wastewater. Int J Syst Evol Microbiol 51:1681–1685CrossRefPubMedGoogle Scholar
  45. Meyer RL, Saunders AM, Zeng RJ, Keller J, Blackall LL (2003) Microscale structure and function of anaerobic-aerobic granules containing glycogen accumulating organisms. FEMS Microbiol Ecol 45:253–261. doi: 10.1016/S0168-6496(03)00159-4 CrossRefPubMedGoogle Scholar
  46. Meyer T, Edwards EA (2014) Anaerobic digestion of pulp and paper mill wastewater and sludge. Water Res 65:321–349. doi: 10.1016/j.watres.2014.07.022 CrossRefPubMedGoogle Scholar
  47. Monteiro RA, Balsanelli E, Wassem R, Marin AM, Brusamarello-Santos LCC, Schmidt MA, Tadra-Sfeir MZ, Pankievicz VCS, Cruz LM, Chubatsu LS, Pedrosa FO, Souza EM (2012) Harbaspirillum-plant interactions: microscopical, histological and molecular aspects. Plant Soil 356:175–196. doi: 10.1007/s11104-012-1125-7 CrossRefGoogle Scholar
  48. Mysak J, Podzimek S, Sommerova P, Lyuya-Mi Y, Bartova J, Janatova T, Prochazkova J, Duskova J (2014) Porphyromonas gingivalis: major periodontopathic pathogen overview. J Immunol Res 476068:1–8. doi: 10.1155/2014/476068 CrossRefGoogle Scholar
  49. Namwong S, Tanasupawat S, Visessanguan W, Kudo T, Itoh T (2007) Halococcus thailandensis sp. nov., from fish sauce in Thailand. Int J Syst Evol Microbiol 57:2199–2203. doi: 10.1099/ijs.0.65218-0 CrossRefPubMedGoogle Scholar
  50. Nelson MC, Morrison M, Schanbacher F, Yu Z (2012) Shifts in microbial community structure of granular and liquid biomass in response to changes to infeed and digester design in anaerobic digesters receiving food-processing wastes. Bioresour Technol 107:135–143. doi: 10.1016/j.biortech.2011.12.070 CrossRefPubMedGoogle Scholar
  51. Ott BM, Rickards A, Gerhke L, Rio RVM (2015) Characterization of shed medicinal leech mucus reveals a diverse microbiota. Front Microbiol 5:757. doi: 10.3389/fmicb.2010.00757 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Panichnumsim P, Ahring B, Nopharatana A, Chaiprasert P (2012) Microbial community structure of an anaerobic reactor digesting cassava pulp and pig manure. Water Sci Technol 66:1590–1600. doi: 10.2166/wst.2012.358 CrossRefGoogle Scholar
  53. Pelletier E, Kreimeyer A, Bocs S, Rouy Z, Gyapay G, Chouari R, Riviere D, Ganesan A, Daegelen P, Sghir A, Cohen GN, Medigue C, Weissenbach J, Le Paslier D (2008) Candidatus Cloacamonas acidaminivorans: genome sequence reconstruction provides a first glimpse of a new bacterial division. J Bacteriol 190:2572–2579. doi: 10.1128/JB.01248-07 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Pervin HM, Batstone DJ, Bond PL (2013) Previously unclassified bacteria dominate during thermophilic and mesophilic anaerobic pre-treatment of primary sludge. Syst App Microbiol 36:281–290. doi: 10.1016/j.syapm.2013.03.003 CrossRefGoogle Scholar
  55. Podosokorskaya OA, Merkel AY, Kolganova TV, Chernyh NA, Miroshnichenko ML, Bonch-Osmolovskaya EA, Kublanov IV (2011) Fervidobacterium riparium sp. nov., a thermophilic anaerobic cellulolytic bacterium isolated from a hot spring. Int J Syst Evol Microbiol 61:2697–2701. doi: 10.1099/ijs.0.026070-0 CrossRefPubMedGoogle Scholar
  56. Posmanik R, Gross A, Nejidat A (2014) Effect of ammonia loads emitted from poultry-manure digestion on nitrification activity and nitrifier-community structure in a compost biofilter. Ecol Eng 62:140–147. doi: 10.1016/j.ecoleng.2013.10.033 CrossRefGoogle Scholar
  57. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org.
  58. Raizada N, Sonakya V, Dalhoff R, Hausner M, Wilderer PA (2003) Population dynamics of rumen microbes using modern techniques in rumen enhanced solid incubation. Water Sci Technol 48:113–119PubMedGoogle Scholar
  59. Razaviriani V, Buchanan ID (2014) Reactor performance and microbial community dynamics during anaerobic-aerobic co-digestion of municipal wastewater sludge with restaurant grease waste at steady-state and overloading stages. Biores Technol 172:232–240. doi: 10.1016/j.biortech.2014.09.046 CrossRefGoogle Scholar
  60. Rincon B, Portillo MC, González JM, Borja R (2013) Microbial community dynamics in the two-stage anaerobic digestion process of two-stage olive mill residue. Int J Environ Sci Technol 10:635–644. doi: 10.1007/s13762-013-0290-4 CrossRefGoogle Scholar
  61. Rodriguez-R LM, Konstantinidis KT (2014a) Estimating coverage in metagenomic datasets and why it matters. ISME J 8:2349–2351. doi: 10.1038/ismej.2014.76 CrossRefPubMedGoogle Scholar
  62. Rodriguez-R LM, Konstantinidis KT (2014b) Nonpareil: a redundanc-based approach to asses the level of coverage in metagenomic datasets. Bioinformatics 30:629–635. doi: 10.1093/bioinformatics/btt584 CrossRefPubMedGoogle Scholar
  63. Rodriguez-Sanchez A, Gonzalez-Martinez A, Martinez-Toledo MV, Garcia-Ruiz MJ, Osorio F, Gonzalez-Lopez J (2014) The effect of influent characteristics and operational conditions over the Performance and Microbial Community structure of partial nitritation reactors. Water 6:1905–1924. doi: 10.3390/w6071905 CrossRefGoogle Scholar
  64. Rothballer M, Schmid M, Klein I, Gattinger A, Grundmann S, Hartmann A (2006) Herbaspirillum hiltneri sp. nov., isolated from surface-sterilized wheat roots. Int J Syst Evol Microbiol 56:1341–1358. doi: 10.1099/ijs.064031-0 CrossRefPubMedGoogle Scholar
  65. Schmid M, Baldani JI, Hartmann A (2006) The genus Herbaspilrillum. Prokaryotes 5:141–150. doi: 10.1007/0-387-30745-1_7
  66. Shah FA, Mahmood Q, Maroof Shah M, Pervez A, Ahmad Asad S (2014) Review article. Microbial ecology of anaerobic digesters: the key players of anaerobiosis. Sci World J 183752:1–21. doi: 10.1155/2014/183752 Google Scholar
  67. Siegrist H, Vogt D, Garcia-Heras JL, Gujer W (2002) Mathematical model for meso- and thermophilic anaerobic sewage sludge digestion. Environ Sci Technol 36:1113–1123. doi: 10.1021/es010139p CrossRefPubMedGoogle Scholar
  68. Smith AM, Sharma D, Lappin-Scott H, Burton S, Huber DH (2014) Microbial community structure of a pilot-scale thermophilic anaerobic digester treating poultry filter. App Microbiol Biotechnol 98:2321–2334. doi: 10.1007/s00253-013-5144-y CrossRefGoogle Scholar
  69. Tabatabaei M, Rahim RA, Abdullah N, Wright A-DG, Shirai Y, Sakai K, Sulaiman A, Hassan MA (2010) Importance of the methanogenic archaea populations in anaerobic wastewater treatments. Process Biochem 45:1214–1225. doi: 10.1016/j.procbio.2010.05.017 CrossRefGoogle Scholar
  70. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi: 10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil 108:1–6. doi:10.1073/pnas.1013488108/−/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1013488108
  72. Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249. doi: 10.1038/nature11552 CrossRefPubMedGoogle Scholar
  73. Ueki A, Akasaka H, Suzuki D, Hattori S, Ueki K (2006) Xylanibacter oryzae gen. nov., sp. nov., a novel strictly anaerobic, Gram-negative, xylanolytic bacterium isolated from rice-plant residue in flooded rice-field soil in Japan. Int J Syst Evol Microbiol 56:2215–2221. doi: 10.1099/ijs.0.64364-0 CrossRefPubMedGoogle Scholar
  74. Wang QF, Li W, Yang H, Liu YL, Cao HH, Dornmayr-Pfaffenhuemer M, Stan-Lotter H, Guo GQ (2007) Halococcus qingdaonensis sp. nov., a halophilic archaeon isolated from a crude sea-salt sample. Int J Syst Evol Microbiol 57:600–604. doi: 10.1099/ijs.0.64673-0 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Weiβ S, Zankel A, Lebhun M, Petrak S, Somitsch W, Guebitz GM (2011) Investigation of microorganisms colonising activated zeolites during anaerobic biogas production from grass silage. Biores Technol 102:4353–4359. doi: 10.1016/j.biortech.2010.12.076 CrossRefGoogle Scholar
  76. Wilkins D, Lu X-Y, Shen Z, Chen J, Lee PKH (2015) Pyrosequencing of mcrA and archaeal 16S rRNA genes reveals diversity and substrate preferences of methanogen communities in anaerobic digesters. Appl Env Microb 81:604–613. doi: 10.1128/AEM.02566-14 CrossRefGoogle Scholar
  77. Yi J, Dong B, Xue Y, Li N, Gao P, Zhao Y, Dai L, Dai X (2014) Microbial community dynamics in batch high-solids anaerobic digestion of food waste under mesophilic conditions. J Microbiol Biotechnol 24:270–279. doi: 10.4014/jmb.1306.06067 CrossRefPubMedGoogle Scholar
  78. Zhang C, Liu X, Dong X (2004) Syntrophomonas curvata sp. nov., an anaerobe that degrades fatty acids in co-culture with methanogens. Int J Syst Evol Microbiol 54:969–973. doi: 10.1099/ijs.0.02903-0 CrossRefPubMedGoogle Scholar
  79. Zhang C, Liu X, Dong X (2005) Syntrophomonas erecta sp. nov., a novel anaerobe that syntrophically degrades short-chain fatty acids. Int J Syst Evol Microbiol 55:799–803. doi: 10.1099/ijs.0.063372-0 CrossRefPubMedGoogle Scholar
  80. Zhang D, Zhu W, Tang C, Suo Y, Gao L, Yuan X, Wang X, Cui Z (2012a) Bioreactor performance and methanogenic population dynamics in a low-temperature (5-18 °C) anaerobic fixed-bed reactor. Bioresour Technol 104:136–143. doi: 10.1016/j.biortech.2011.10.086 CrossRefPubMedGoogle Scholar
  81. Zhang T, Shao M-F, Ye L (2012b) 454 pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants. ISME J 6:1137–1147. doi: 10.1038/ismej.2011.188 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Alejandro Gonzalez-Martinez
    • 1
  • Maria Jesus Garcia-Ruiz
    • 2
  • Alejandro Rodriguez-Sanchez
    • 3
  • Francisco Osorio
    • 2
  • Jesus Gonzalez-Lopez
    • 3
  1. 1.Department of Built Environment, School of engineeringAalto UniversityEspooFinland
  2. 2.Department of Civil Engineering, Campus of FuentenuevaUniversity of GranadaGranadaSpain
  3. 3.Institute of Water ResearchUniversity of GranadaGranadaSpain

Personalised recommendations