Skip to main content
SpringerLink
Log in

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

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 51:1687–1692

    Article  CAS  PubMed  Google Scholar 

  • American Public Health Association (APHA) (2005) Standard methods for the examination of water and wastewater, 21st Edition.

  • Anderson GK, Kasapgil B, Ince O (1994) Microbiological study of two-stage anaerobic digestion during start-up. Wat Res 28:2383–2392

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Biswas K, Taylor MW, Turner SJ (2014) Successional development of biofilms in moving bed biofilm reactor (MBBR) systems treating municipal wastewater. App Microbiol Biotechnol 98:1429–1440

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 34:875–885

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Griffin ME, McMahon KD, Mackie RI, Raskin L (1998) Methanogenic population dynamics during start-up of anaerobic digesters. Biotechnol Bioeng 5:342–355

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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):590–600

  • 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 66:250–260

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 7:200–209

    CAS  Google Scholar 

  • 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 47:6897–6908

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 51:1681–1685

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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.

  • 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 48:113–119

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Schmid M, Baldani JI, Hartmann A (2006) The genus Herbaspilrillum. Prokaryotes 5:141–150. doi:10.1007/0-387-30745-1_7

  • 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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

  • Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249. doi:10.1038/nature11552

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Department of Built Environment, School of engineering, Aalto University, P.O. Box 15200, Aalto, 00076, Espoo, FI, Finland

    Alejandro Gonzalez-Martinez

  2. Department of Civil Engineering, Campus of Fuentenueva, University of Granada, 18071, Granada, Spain

    Maria Jesus Garcia-Ruiz & Francisco Osorio

  3. Institute of Water Research, University of Granada, C/Ramon y Cajal, 4, 18071, Granada, Spain

    Alejandro Rodriguez-Sanchez & Jesus Gonzalez-Lopez

Authors
  1. Alejandro Gonzalez-Martinez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Jesus Garcia-Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alejandro Rodriguez-Sanchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francisco Osorio
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jesus Gonzalez-Lopez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alejandro Gonzalez-Martinez.

Ethics declarations

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.

Electronic supplementary material

ESM 1

(PDF 1539 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gonzalez-Martinez, A., Garcia-Ruiz, M.J., Rodriguez-Sanchez, A. et al. Archaeal and bacterial community dynamics and bioprocess performance of a bench-scale two-stage anaerobic digester. Appl Microbiol Biotechnol 100, 6013–6033 (2016). https://doi.org/10.1007/s00253-016-7393-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-016-7393-z

Keywords

Search

Navigation