Skip to main content
SpringerLink
Log in

From mesophilic to thermophilic digestion: the transitions of anaerobic bacterial, archaeal, and fungal community structures in sludge and manure samples

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

Abstract

The shift of microbial communities during a transition from mesophilic anaerobic digestion (MAD) to thermophilic anaerobic digestion (TAD) was characterized in two treatments. One treatment was inoculated with sludge and the other was inoculated with manure. In this study, methane was produced both in MAD and TAD, but TAD has slightly more methane produced than MAD. A broad phylogenetic spectrum of bacterial, archaeal, and fungal taxa at thermophilic conditions was detected. Coprothermobacter, Bacillus, Haloplasma, Clostridiisalibacter, Methanobacterium, Methanothermobacter, Saccharomycetales, Candida, Alternaria, Cladosporium, and Penicillium were found almost exclusively in TAD, suggesting their adaptation to thermophilic conditions and ecological roles in digesting the organic compounds. The characterization of the lesser-known fungal community revealed that fungi probably constituted an important portion of the overall community within TAD and contributed to this process by degrading complex organic compounds. The shift of the microbial communities between MAD and TAD implied that temperature drastically affected the microbial diversity in anaerobic digestion. In addition, the difference in microbial communities between sludge and manure indicated that different source of inoculum also affected the microbial diversity and community.

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.

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

Similar content being viewed by others

References

  • APHA, AWWA, WEF (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, Washington,D.C.

    Google Scholar 

  • Blotevogel K-H, Fischer U, Mocha M, Jannsen S (1985) Methanobacteriumthermoalcaliphilum spec. nov., a new moderately alkaliphilic and thermophilic autotrophic methanogen. Arch Microbiol 142(3):211–217

    Article  CAS  Google Scholar 

  • Bond PL, Smriga SP, Banfield JF (2000) Phylogeny of microorganisms populating a thick, subaerial, predominantly lithotrophic biofilm at an extreme acid mine drainage site. Appl Environ Microb 66(9):3842–3849

    Article  CAS  Google Scholar 

  • Boone DR, Liu Y, Zhao Z-J, Balkwill DL, Drake GR, Stevens TO, Aldrich HC (1995) Bacillusinfernus sp. nov., an Fe (III)-and Mn (IV)-reducing anaerobe from the deep terrestrial subsurface. Int J Syst Bacteriol 45(3):441–448

    Article  CAS  PubMed  Google Scholar 

  • Bouanane-Darenfed A, Fardeau M-L, Grégoire P, Joseph M, Kebbouche-Gana S, Benayad T, Hacene H, Cayol J-L, Ollivier B (2011) Caldicoprobacteralgeriensis sp. nov. A new thermophilic anaerobic, xylanolytic bacterium isolated from an Algerian hot spring. Curr Microbiol 62(3):826–832

    Article  CAS  PubMed  Google Scholar 

  • Bouanane-Darenfed A, Hania WB, Hacene H, Cayol J-L, Ollivier B, Fardeau M-L (2013) Caldicoprobacterguelmensis sp. nov., a thermophilic, anaerobic, xylanolytic bacterium isolated from a hot spring. Int J Syst Evol Micr 63(Pt 6):2049–2053

    Article  CAS  Google Scholar 

  • Brock TD, Freeze H (1969) Thermusaquaticus gen. n. and sp. n., a nonsporulating extreme thermophile. J Bacteriol 98(1):289–297

    PubMed Central  CAS  PubMed  Google Scholar 

  • Buchan A, Newell SY, Butler M, Biers EJ, Hollibaugh JT, Moran MA (2003) Dynamics of bacterial and fungal communities on decaying salt marsh grass. Appl Environ Microb 69(11):6676–6687

    Article  CAS  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108(Supplement 1):4516–4522

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheon J, Hong F, Hidaka T, Koshikawa H, Tsuno H (2007) Microbial population dynamics in a thermophilic methane digester fed with garbage. Water Sci Technol 55(10):175–182

    Article  CAS  PubMed  Google Scholar 

  • Craveri R, Manachini P, Aragozzini F (1972) Thermozymocidin new antifungal antibiotic from a thermophilic eumycete. Experientia 28(7):867–868

    Article  CAS  PubMed  Google Scholar 

  • Darland G, Brock T (1971) Bacillusacidocaldarius sp. nov., an acidophilic thermophilic spore-forming bacterium. J Gen Microbiol 67(1):9–15

    Article  Google Scholar 

  • de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29(4):795–811

    Article  PubMed  Google Scholar 

  • De la Rubia M, Riau V, Raposo F, Borja R (2013) Thermophilic anaerobic digestion of sewage sludge: focus on the influence of the start-up. A Rev Crit Rev Biotechnol 33(4):448–460

    Article  PubMed  Google Scholar 

  • 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 Microb 72(7):5069–5072

    Article  CAS  Google Scholar 

  • Emmerich M, Bhansali A, Lösekann-Behrens T, Schröder C, Kappler A, Behrens S (2012) Abundance, distribution, and activity of Fe (II)-oxidizing and Fe (III)-reducing microorganisms in hypersaline sediments of Lake Kasin, southern Russia. Appl Environ Microb 78(12):4386–4399

    Article  CAS  Google Scholar 

  • Etchebehere C, Pavan M, Zorzopulos J, Soubes M, Muxi L (1998) Coprothermobacterplatensis sp. nov., a new anaerobic proteolytic thermophilic bacterium isolated from an anaerobic mesophilic sludge. Int J Syst Bacteriol 48(4):1297–1304

    Article  CAS  PubMed  Google Scholar 

  • Ghazifard A, Kasra-Kermanshahi R, Far ZE (2001) Identification of thermophilic and mesophilic bacteria and fungi in Esfahan (Iran) municipal solid waste compost. Waste Manag Res 19(3):257–261

    Article  CAS  PubMed  Google Scholar 

  • Gujer W, Zehnder A (1983) Conversion processes in anaerobic digestion. Water Sci Technol 15(8–9):127–167

    CAS  Google Scholar 

  • Hori T, Haruta S, Sasaki D, Hanajima D, Ueno Y, Ogata A, Ishii M, Igarashi Y (2014) Reorganization of the bacterial and archaeal populations associated with organic loading conditions in a thermophilic anaerobic digester. J Biosci Bioeng

  • Hultman J, Vasara T, Partanen P, Kurola J, Kontro M, Paulin L, Auvinen P, Romantschuk M (2010) Determination of fungal succession during municipal solid waste composting using a cloning-based analysis. J Appl Microbiol 108(2):472–487

    Article  CAS  PubMed  Google Scholar 

  • Jiang L, Xu H, Zeng X, Wu X, Long M, Shao Z (2015) Thermophilic hydrogen-producing bacteria inhabiting deep-sea hydrothermal environments represented by Caloranaerobacter. Res Microbiol

  • Kamagata Y, Kawasaki H, Oyaizu H, Nakamura K, Mikami E, Endo G, Koga Y, Yamasato K (1992) Characterization of three thermophilic strains of Methanothrix (“Methanosaeta”) thermophila sp. nov. and rejection of Methanothrix (“Methanosaeta”) thermoacetophila. Int J Syst Bacteriol 42(3):463–468

    Article  CAS  PubMed  Google Scholar 

  • Kersters I, Maestrojuan GM, Torck U, Vancanneyt M, Kersters K, Verstraete W (1994) Isolation of Coprothermobacterproteolyticus from an anaerobic digest and further characterization of the species. Syst Appl Microbiol 17(2):289–295

    Article  CAS  Google Scholar 

  • Khemkhao M, Nuntakumjorn B, Techkarnjanaruk S, Phalakornkule C (2012) UASB performance and microbial adaptation during a transition from mesophilic to thermophilic treatment of palm oil mill effluent. J Environ Manag 103:74–82

    Article  CAS  Google Scholar 

  • Kirk TK, Farrell RL (1987) Enzymatic “combustion”: the microbial degradation of lignin. Annu Rev Microbiol 41(1):465–501

    Article  CAS  PubMed  Google Scholar 

  • Kotelnikova S, Macario AJ, Pedersen K (1998) Methanobacteriumsubterraneum sp. nov., a new alkaliphilic, eurythermic and halotolerant methanogen isolated from deep granitic groundwater. Int J Syst Bacteriol 48(2):357–367

    Article  PubMed  Google Scholar 

  • Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG, Knight R (2012) Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protoc Microbiol:1E. 5.1-1E. 5.20

  • Kuhar S, Nair LM, Kuhad RC (2008) Pretreatment of lignocellulosic material with fungi capable of higher lignin degradation and lower carbohydrate degradation improves substrate acid hydrolysis and the eventual conversion to ethanol. Can J Microbiol 54(4):305–313

    Article  CAS  PubMed  Google Scholar 

  • Levén L, Eriksson AR, Schnürer A (2007) Effect of process temperature on bacterial and archaeal communities in two methanogenic bioreactors treating organic household waste. FEMS Microbiol Ecol 59(3):683–693

    Article  PubMed  Google Scholar 

  • Luo G, Angelidaki I (2013) Co-digestion of manure and whey for in situ biogas upgrading by the addition of H2: process performance and microbial insights. Appl Microbiol Biot 97(3):1373–1381

    Article  CAS  Google Scholar 

  • Maeda K, Hanajima D, Morioka R, Osada T (2010) Characterization and spatial distribution of bacterial communities within passively aerated cattle manure composting piles. Bioresource Technol 101(24):9631–9637

    Article  CAS  Google Scholar 

  • Margesin R, Fonteyne P-A, Redl B (2005) Low-temperature biodegradation of high amounts of phenol by Rhodococcus spp. and basidiomycetous yeasts. Res Microbiol 156(1):68–75

    Article  CAS  PubMed  Google Scholar 

  • Menes RJ, Fernández A, Muxí LA (2001) Physiological and molecular characterisation of an anaerobic thermophilic oleate-degrading enrichment culture. Anaerobe 7(1):17–24

    Article  CAS  Google Scholar 

  • Merlino G, Rizzi A, Schievano A, Tenca A, Scaglia B, Oberti R, Adani F, Daffonchio D (2013) Microbial community structure and dynamics in two-stage vs single-stage thermophilic anaerobic digestion of mixed swine slurry and market bio-waste. Water Res 47(6):1983–1995

    Article  CAS  PubMed  Google Scholar 

  • Nallathambi Gunaseelan V (1997) Anaerobic digestion of biomass for methane production: a review. Biomass Bioenerg 13(1):83–114

    Article  Google Scholar 

  • Orcutt BN, Bach W, Becker K, Fisher AT, Hentscher M, Toner BM, Wheat CG, Edwards KJ (2010) Colonization of subsurface microbial observatories deployed in young ocean crust. ISME J 5(4):692–703

    Article  PubMed Central  PubMed  Google Scholar 

  • Osono T (2003) Effects of prior decomposition of beech leaf litter by phyllosphere fungi on substrate utilization by fungal decomposers. Mycoscience 44(1):41–45

    Article  Google Scholar 

  • Panswad T, Doungchai A, Anotai J (2003) Temperature effect on microbial community of enhanced biological phosphorus removal system. Water Res 37(2):409–415

    Article  CAS  PubMed  Google Scholar 

  • Park Y, Hong F, Cheon J, Hidaka T, Tsuno H (2008) Comparison of thermophilic anaerobic digestion characteristics between single-phase and two-phase systems for kitchen garbage treatment. J Biosci Bioeng 105(1):48–54

    Article  CAS  PubMed  Google Scholar 

  • Parkin GF, Owen WF (1986) Fundamentals of anaerobic digestion of wastewater sludges. J Environ Eng 112(5):867–920

    Article  CAS  Google Scholar 

  • Rademacher A, Nolte C, Schönberg M, Klocke M (2012) Temperature increases from 55 to 75 °C in a two-phase biogas reactor result in fundamental alterations within the bacterial and archaeal community structure. Appl Microbiol Biot 96(2):565–576

    Article  CAS  Google Scholar 

  • Ritari J, Koskinen K, Hultman J, Kurola JM, Kymäläinen M, Romantschuk M, Paulin L, Auvinen P (2012) Molecular analysis of meso- and thermophilic microbiota associated with anaerobic biowaste degradation. BMC Microbiol 12(1):121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sasaki K, Morita M, Sasaki D, Nagaoka J, Matsumoto N, Ohmura N, Shinozaki H (2011) Syntrophic degradation of proteinaceous materials by the thermophilic strains Coprothermobacter proteolyticus and Methanothermobacterthermautotrophicus. J Biosci Bioeng 112(5):469–472

    Article  CAS  PubMed  Google Scholar 

  • Shin K-S, Shin YK, Yoon J-H, Park Y-H (2001) Candidathermophila sp. nov., a novel thermophilic yeast isolated from soil. Int J Syst Evol Micr 51(6):2167–2170

    Article  CAS  Google Scholar 

  • Skirnisdottir S, Hreggvidsson GO, Hjörleifsdottir S, Marteinsson VT, Petursdottir SK, Holst O, Kristjansson JK (2000) Influence of sulfide and temperature on species composition and community structure of hot spring microbial mats. Appl Environ Microb 66(7):2835–2841

    Article  CAS  Google Scholar 

  • Štursová M, Žifčáková L, Leigh MB, Burgess R, Baldrian P (2012) Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol 80(3):735–746

    Article  PubMed  Google Scholar 

  • Sun W, Xiao T, Sun M, Dong Y, Ning Z, Xiao E, Tang S, Li J (2015) Diversity of the sediment microbial community in the Aha watershed (Southwest China) in response to acid mine drainage pollution gradients. Appl Environ Microb 81(15):4874–4884

    Article  CAS  Google Scholar 

  • Tada C, Tsukahara K, Sawayama S (2006) Illumination enhances methane production from thermophilic anaerobic digestion. Appl Microbiol Biot 71(3):363–368

    Article  CAS  Google Scholar 

  • Ueno Y, Tatara M (2008) Microbial population in a thermophilic packed-bed reactor for methanogenesis from volatile fatty acids. Enzyme Microb Tech 43(3):302–308

    Article  CAS  Google Scholar 

  • Walters WA, Caporaso JG, Lauber CL, Berg-Lyons D, Fierer N, Knight R (2011) PrimerProspector: de novo design and taxonomic analysis of barcoded polymerase chain reaction primers. Bioinformatics 27(8):1159–1161

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang X, Hu M, Xia Y, Wen X, Ding K (2012) Pyrosequencing analysis of bacterial diversity in 14 wastewater treatment systems in China. Appl Environ Microb 78(19):7042–7047

    Article  CAS  Google Scholar 

  • Wasserfallen A, Nölling J, Pfister P, Reeve J, De Macario EC (2000) Phylogenetic analysis of 18 thermophilic Methanobacterium isolates supports the proposals to create a new genus, Methanothermobacter gen. nov., and to reclassify several isolates in three species, Methanothermobacter thermautotrophicus comb. nov., Methanothermobacter wolfeii comb. nov., and Methanothermobacter marburgensis sp. nov. Int J Syst Evol Micr 50(1):43–53

    Article  CAS  Google Scholar 

  • Winter J, Lerp C, Zabel H-P, Wildenauer F, König H, Schindler F (1984) Methanobacterium wolfei, sp. nov., a new tungsten-requiring, thermophilic, autotrophic methanogen. Syst Appl Microbiol 5(4):457–466

    Article  CAS  Google Scholar 

  • Wood TM, Garcia-Campayo V (1991) Enzymology of cellulose degradation physiology of biodegradative microorganisms. Springer, pp 147–161

  • Wrighton KC, Agbo P, Warnecke F, Weber KA, Brodie EL, DeSantis TZ, Hugenholtz P, Andersen GL, Coates JD (2008) A novel ecological role of the Firmicutes identified in thermophilic microbial fuel cells. ISME J 2(11):1146–1156

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama H, Wagner ID, Wiegel J (2010) Caldicoprobacteroshimai gen. nov., sp. nov., an anaerobic, xylanolytic, extremely thermophilic bacterium isolated from sheep faeces, and proposal of Caldicoprobacteraceae fam. nov. Int J Syst Evol Micr 60(1):67–71

    Article  CAS  Google Scholar 

  • Zbransk J, Wachtl R, Jenek P, Dohnyos M (2000) The activity of anaerobic biomass in thermophilic andmesophilic digesters at different loading rates. Water Sci Technol 42(9):49–56

    Google Scholar 

  • Zeikus J, Wolee R (1972) Methanobacterium thermoautotrophicus sp. n., an anaerobic, autotrophic, extreme thermophile. J Bacteriol 109(2):707–713

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ziganshin AM, Liebetrau J, Pröter J, Kleinsteuber S (2013) Microbial community structure and dynamics during anaerobic digestion of various agricultural waste materials. Appl Microbiol Biot 97(11):5161–5174

    Article  CAS  Google Scholar 

  • Zinder SH, Mah RA (1979) Isolation and characterization of a thermophilic strain of Methanosarcina unable to use H2-CO2 for methanogenesis. Appl Environ Microb 38(5):996–1008

    CAS  Google Scholar 

Download references

Compliance with ethical standards

ᅟ

Funding

This study was funded by the National Natural Science Foundation of China (51178093, 51208086), the Shanghai Pujiang Program (13PJ1400100), the DHU Distinguished Young Professor Program, and the Fundamental Research Funds for the Central Universities.

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

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

Author information

Authors and Affiliations

  1. Departmentof Biochemistry and Microbiology, Rutgers, the State University of New Jersey, New Brunswick, NJ, 08901, USA

    Weimin Sun, Tiffany Louie, Tong Liu & Chengsheng Zhu

  2. Department of Environmental Science and Engineering, College of Natural Resource and Environment, South China Agricultural University, Guangzhou, 510642, China

    Guangwei Yu

  3. College of Environmental Science and Engineering, State Environmental Protection Engineering Center for Pollution Treatment and Control in Textile Industry, Donghua University, 2999 North Renmin Road, Songjiang District, Shanghai, 201620, China

    Gang Xue & Pin Gao

Authors
  1. Weimin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guangwei Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tiffany Louie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chengsheng Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gang Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pin Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pin Gao.

Electronic supplementary material

ESM 1

(PDF 213 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, W., Yu, G., Louie, T. et al. From mesophilic to thermophilic digestion: the transitions of anaerobic bacterial, archaeal, and fungal community structures in sludge and manure samples. Appl Microbiol Biotechnol 99, 10271–10282 (2015). https://doi.org/10.1007/s00253-015-6866-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-015-6866-9

Keywords

Search

Navigation