Applied Microbiology and Biotechnology

, Volume 102, Issue 12, pp 5323–5334 | Cite as

Seeking key microorganisms for enhancing methane production in anaerobic digestion of waste sewage sludge

  • Nurul Asyifah Mustapha
  • Anyi Hu
  • Chang-Ping Yu
  • Siti Suhailah Sharuddin
  • Norhayati Ramli
  • Yoshihito Shirai
  • Toshinari Maeda
Environmental biotechnology
  • 63 Downloads

Abstract

Efficient approaches for the utilization of waste sewage sludge have been widely studied. One of them is to use it for the bioenergy production, specifically methane gas which is well-known to be driven by complex bacterial interactions during the anaerobic digestion process. Therefore, it is important to understand not only microorganisms for producing methane but also those for controlling or regulating the process. In this study, azithromycin analogs belonging to macrolide, ketolide, and lincosamide groups were applied to investigate the mechanisms and dynamics of bacterial community in waste sewage sludge for methane production. The stages of anaerobic digestion process were evaluated by measuring the production of intermediate substrates, such as protease activity, organic acids, the quantification of bacteria and archaea, and its community dynamics. All azithromycin analogs used in this study achieved a high methane production compared to the control sample without any antibiotic due to the efficient hydrolysis process and the presence of important fermentative bacteria and archaea responsible in the methanogenesis stage. The key microorganisms contributing to the methane production may be Clostridia, Cladilinea, Planctomycetes, and Alphaproteobacteria as an accelerator whereas Nitrosomonadaceae and Nitrospiraceae may be suppressors for methane production. In conclusion, the utilization of antibiotic analogs of macrolide, ketolide, and lincosamide groups has a promising ability in finding the essential microorganisms and improving the methane production using waste sewage sludge.

Keywords

Macrolide Ketolide Lincosamide Sewage sludge Methane Microbial community 

Notes

Funding information

The authors wish to thank the Japanese Government Scholarship (MEXT), Kitakyushu City, and Science & Technology Research Partnership for Sustainable Development Program (SATREPS) for the support of this study.

Compliance with ethical standards

Ethical approval

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

Conflict of interest

The authors declare that there are no conflicts of interest.

Supplementary material

253_2018_9003_MOESM1_ESM.pdf (230 kb)
ESM 1 (PDF 230 kb)

References

  1. Amin MM, Zilles JL, Greiner J, Charbonneau S, Raskin L, Morgenroth E (2006) Influence of the antibiotic erythromycin on anaerobic treatment of a pharmaceutical wastewater. Environ Sci Technol 40:3971–3977CrossRefPubMedGoogle Scholar
  2. Amsden GW (1996) Erythromycin, clarithromycin, and azithromycin: are the differences real? Clin Ther 18:56–72CrossRefPubMedGoogle Scholar
  3. Appels L, Baeyens J, Degrève J, Dewil R (2008) Principles and potential of the anaerobic digestion of waste-activated sludge. Prog Energy Combust Sci 34:755–781CrossRefGoogle Scholar
  4. Ariesyady HD, Ito T, Okabe S (2007) Functional bacterial and archaeal community structures of major trophic groups in a full-scale anaerobic sludge digester. Water Res 41:1554–1568CrossRefPubMedGoogle Scholar
  5. Bryskier A (1998) Roxithromycin: review of its antimicrobial activity. J Antimicrob Chemother 41:1–21CrossRefPubMedGoogle Scholar
  6. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cetecioglu Z, Ince B, Ince O, Orhon D (2015) Acute effect of erythromycin on metabolic transformations of volatile fatty acid mixture under anaerobic conditions. Chemosphere 124:129–135CrossRefPubMedGoogle Scholar
  8. Chantot JF, Bryskier A, Gasc JC (1986) Antibacterial activity of roxithromycin: a laboratory evaluation. J Antibiot 39:660–668CrossRefPubMedGoogle Scholar
  9. Chen Q (2010) Kinetics of anaerobic digestion of selected C1 to C4 organic acids. Dissertation, University of Missouri—ColumbiaGoogle Scholar
  10. 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 72:5069–5072CrossRefPubMedPubMedCentralGoogle Scholar
  11. Doons-Goossens A, Bedert R, Degreef H, Vandele M (1990) Airborne allergic contact dermatitis from kitasamycin and midecamycin. Contact Dermatitis 23:118–119CrossRefGoogle Scholar
  12. Dunfield P, Knowles R (1995) Kinetics of inhibition of methane oxidation by nitrate, nitrite, and ammonium in a humisol. Appl Environ Microbiol 61:3129–3135PubMedPubMedCentralGoogle Scholar
  13. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998CrossRefPubMedGoogle Scholar
  14. Elshahed MS, Youssef NH, Luo Q, Najar FZ, Roe BA, Sisk TM, Bühring SI, Hinrichs KU, Krumholz LR (2007) Phylogenetic and metabolic diversity of Planctomycetes from anaerobic, sulfide- and sulfur-rich Zodletone Spring, Oklahoma. Appl Environ Microbiol 73:4707–4716CrossRefPubMedPubMedCentralGoogle Scholar
  15. Ettwig KF, Speth DR, Reimann J, Wu ML, Jetten MS, Keltjens JT (2012) Bacterial oxygen production in the dark. Front Microbiol 3:273Google Scholar
  16. Fan C, Lee PKH, Ng WJ, Alvarez-Cohen L, Brodie EL, Andersen GL, He J (2009) Influence of trace erythromycin and erythromycin-H2O on carbon and nutrients removal and on resistance selection in sequencing batch reactors (SBRs). Appl Microbiol Biotechnol 85:185–195CrossRefPubMedPubMedCentralGoogle Scholar
  17. Felmingham D (2001) Microbiological profile of telithromycin, the first ketolide antimicrobial. Clin Microbiol Infect 7:2–10CrossRefPubMedGoogle Scholar
  18. Goldstein EJC, Citron DM, Merriam CV, Warren Y, Tyrrel KL, Fernandez H (2003) In vitro activities of telithromycin and 10 oral agents against aerobic and anaerobic pathogens isolated from antral puncture specimens from patients with sinusitis. Antimicrob Agents Chemother 47:1963–1967CrossRefPubMedPubMedCentralGoogle Scholar
  19. Guo J, Peng Y, Ni B-J, Han X, Fan L, Yuan Z (2015) Dissecting microbial community structure and methane-producing pathways of a full-scale anaerobic reactor digesting activated sludge from wastewater treatment by metagenomic sequencing. Microb Cell Factories 14:33CrossRefGoogle Scholar
  20. Hammer Ø, Harper DAT, Ryan PD (2001) Paleontological statistics software: package for education and data analysis. Palaeontol Electron 4Google Scholar
  21. Hildebrand F, Tadeo R, Voigt AY, Bork P, Raes J (2014) LotuS: an efficient and user-friendly OTU processing pipeline. Microbiome 2:30CrossRefPubMedPubMedCentralGoogle Scholar
  22. Huser BA, Wuhrmann K, Zehnder AJB (1982) Methanothrix soehngenii gen. nov. sp. nov., a new acetotrophic non-hydrogen-oxidizing methane bacterium. Arch Microbiol 132:1–9CrossRefGoogle Scholar
  23. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:1–11CrossRefGoogle Scholar
  24. Lee C, Kim J, Shin SG, Hwang S (2008) Monitoring bacterial and archaeal community shifts in a mesophilic anaerobic batch reactor treating a high-strength organic wastewater. FEMS Microbiol Ecol 65:544–554CrossRefPubMedGoogle Scholar
  25. Leigh DA (1981) Antibacterial activity and pharmacokinetics of clindamycin. J Antimicrob Chemother 7:3–9CrossRefPubMedGoogle Scholar
  26. Liu L, Xu X, Cao Y, Cai C, Cui H, Yao J (2017) Nitrate decreases methane production also by increasing methane oxidation through stimulating NC10 population in ruminal culture. AMB Express 7:76CrossRefPubMedPubMedCentralGoogle Scholar
  27. Liu PY, Chen JR, Shao L, Tan J, Chen DJ (2018) Responses of flocculent and granular sludge in anaerobic sequencing batch reactor (ASBR) to azithromycin wastewater and its impact on microbial communities. J Chem Technol Biotechnol.  https://doi.org/10.1002/jctb.5578
  28. Lu X, Zhen G, Liu Y, Hojo T, Estrada AL, Li Y-Y (2014) Long-term effect of the antibiotic cefalexin on methane production during waste activated sludge anaerobic digestion. Bioresour Technol 169:644–651CrossRefPubMedGoogle Scholar
  29. Maeda T, Yoshimura T, García-Contreras R, Ogawa HI (2011) Purification and characterization of a serine protease secreted by Brevibacillus sp. KH3 for reducing waste activated sludge and biofilm formation. Bioresour Technol 102:10650–10656CrossRefPubMedGoogle Scholar
  30. Maeda T, Yoshimura T, Shimazu T, Shirai Y, Ogawa HI (2009) Enhanced production of lactic acid with reducing excess sludge by lactate fermentation. J Hazard Mater 168:656–663CrossRefPubMedGoogle Scholar
  31. Manyi-Loh CE, Mamphweli SN, Meyer EL, Okoh AI, Makaka G, Simon M (2013) Microbial anaerobic digestion (bio-digesters) as an approach to the decontamination of animal wastes in pollution control and the generation of renewable energy. Int J Environ Res Public Health 10:4390–4417CrossRefPubMedPubMedCentralGoogle Scholar
  32. Mohd Yasin NH, Maeda T, Hu A, Yu C-P, Wood TK (2015) CO2 sequestration by methanogens in activated sludge for methane production. Appl Energy 142:426–434CrossRefGoogle Scholar
  33. Mohd Yusoff MZ, Maeda T, Sanchez-Torres V, Ogawa HI, Shirai Y, Hassan MA, Wood TK (2012) Uncharacterized Escherichia coli proteins YdjA and YhjY are related to biohydrogen production. Int J Hydrog Energy 37:17778–17787CrossRefGoogle Scholar
  34. Mustapha NA, Sakai K, Shirai Y, Maeda T (2016) Impact of different antibiotics on methane production using waste-activated sludge: mechanisms and microbial community dynamics. Appl Microbiol Biotechnol 100:9355–9364CrossRefPubMedGoogle Scholar
  35. Ng KK, Shi X, Ng HY (2015) Evaluation of system performance and microbial communities of a bioaugmented anaerobic membrane bioreactor treating pharmaceutical wastewater. Water Res 81:311–324CrossRefPubMedGoogle Scholar
  36. Nguyen MT, Maeda T, Mohd Yusoff MZ, Ogawa HI (2014) Effect of azithromycin on enhancement of methane production from waste activated sludge. J Ind Microbiol Biotechnol 41:1051–1059CrossRefPubMedGoogle Scholar
  37. Osaka T, Ebie Y, Tsuneda S, Inamori Y (2008) Identification of the bacterial community involved in methane-dependent denitrification in activated sludge using DNA stable-isotope probing. FEMS Microbiol Ecol 64:494–506CrossRefPubMedGoogle Scholar
  38. Peters DH, Clissold SP (1992) Clarithromycin. Drugs 44:117–164CrossRefPubMedGoogle Scholar
  39. Rakhit S, Singh K (1974) Structure activity relationship in sixteen membered macrolide antibiotics. J Antibiot 27:221–224CrossRefPubMedGoogle Scholar
  40. Roberts MC (2004) Resistance to macrolide, lincosamide, streptogramin, ketolide, and oxazolidinone antibiotics. Mol Biotechnol 28:47–62CrossRefPubMedGoogle Scholar
  41. Roberts MC (2008) Update on macrolide–lincosamide–streptogramin, ketolide, and oxazolidinone resistance genes. FEMS Microbiol Lett 282:147–159CrossRefPubMedGoogle Scholar
  42. Sanz JL, Rodriguez N, Amils ÁR (1996) The action of antibiotics on the anaerobic digestion process. Appl Microbiol Biotechnol 46:587–592CrossRefPubMedGoogle Scholar
  43. Scheinfeld N (2004) Telithromycin: a brief review of a new ketolide antibiotic. J Drugs Dermatol 3:409–413PubMedGoogle Scholar
  44. Schlüsener MP, Bester K (2006) Persistence of antibiotics such as macrolides, tiamulin and salinomycin in soil. Environ Pollut 143:565–571CrossRefPubMedGoogle Scholar
  45. Senta I, Krizman-Matasic I, Terzic S, Ahel M (2017) Comprehensive determination of macrolide antibiotics, their synthesis intermediates and transformation products in wastewater effluents and ambient waters by liquid chromatography–tandem mass spectrometry. J Chromatogr A 1509:60–68CrossRefPubMedGoogle Scholar
  46. Shi JC, Liao XD, Wu YB, Liang JB (2011) Effect of antibiotics on methane arising from anaerobic digestion of pig manure. Anim Feed Sci Technol 166:457–463CrossRefGoogle Scholar
  47. Shimada T, Li X, Zilles JL, Morgenroth E, Raskin L (2011) Effects of the antimicrobial tylosin on the microbial community structure of an anaerobic sequencing batch reactor. Biotechnol Bioeng 108:296–305CrossRefPubMedGoogle Scholar
  48. Shimada T, Zilles JL, Morgenroth E, Raskin L (2008) Inhibitory effects of the macrolide antimicrobial tylosin on anaerobic treatment. Biotechnol Bioeng 101:73–82CrossRefPubMedGoogle Scholar
  49. Skindersoe ME, Alhede M, Phipps R, Yang L, Jensen PO, Rasmussen TB, Bjarnsholt T, Tolker-Nielsen T, Høiby N, Givskov M (2008) Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 52:3648–3663CrossRefPubMedPubMedCentralGoogle Scholar
  50. Smieja M (1998) Current indications for the use of clindamycin: a critical review. Can J Infect Dis Med Microbiol 9:22–28Google Scholar
  51. Steinhaus B, Garcia ML, Shen AQ, Angenent LT (2007) A portable anaerobic microbioreactor reveals optimum growth conditions for the methanogen Methanosaeta concilii. Appl Environ Microbiol 73:1653–1658CrossRefPubMedPubMedCentralGoogle Scholar
  52. Straneo G, Scarpazza G (1990) Efficacy and safety of clarithromycin versus josamycin in the treatment of hospitalized patients with bacterial pneumonia. J Int Med Res 18:164–170CrossRefPubMedGoogle Scholar
  53. Terzic S, Udikovic-Kolic N, Jurina T, Krizman-Matasic I, Senta I, Mihaljevic I, Loncar J, Smital T, Ahel M (2018) Biotransformation of macrolide antibiotics using enriched activated sludge culture: kinetics, transformation routes and ecotoxicological evaluation. J Hazard Mater 349:143–152CrossRefPubMedGoogle Scholar
  54. Venkiteshwaran K, Bocher B, Maki J, Zitomer D (2015) Relating anaerobic digestion microbial community and process function. Microbiol Insights 8:MBI-S33593CrossRefGoogle Scholar
  55. Wei R, Ge F, Huang S, Chen M, Wang R (2011) Occurrence of veterinary antibiotics in animal wastewater and surface water around farms in Jiangsu Province, China. Chemosphere 82:1408–1414CrossRefPubMedGoogle Scholar
  56. Weiland P (2010) Biogas production: current state and perspectives. Appl Microbiol Biotechnol 85:849–860CrossRefPubMedGoogle Scholar
  57. Williams JD (1991) Spectrum of activity of azithromycin. Eur J Clin Microbiol Infect Dis 10:813–820 ratioCrossRefPubMedGoogle Scholar
  58. Wu D, Lü F, Gao H, Shao L, He P (2011) Mesophilic bio-liquefaction of lincomycin manufacturing biowaste: the influence of total solid content and inoculum to substrate. Bioresour Technol 102:5855–5862CrossRefPubMedGoogle Scholar
  59. Xu R, Peng Y, Wang M, Fan L, Li X (2014) Effects of broad-spectrum antibiotics on the metabolism and pharmacokinetics of ginsenoside Rb1: a study on rats’ gut microflora influenced by lincomycin. J Ethnopharmacol 158:338–344CrossRefPubMedGoogle Scholar
  60. Zhao Z, Jin L, Xu Y, Zhu D, Liu Y, Liu C, Lei P (2014) Synthesis and antibacterial activity of a series of novel 9-O-acetyl-4′-substituted 16-membered macrolides derived from josamycin. Bioorg Med Chem Lett 24:480–484CrossRefPubMedGoogle Scholar
  61. 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

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological Functions Engineering, Graduate School of Life Science and Systems EngineeringKyushu Institute of TechnologyKitakyushuJapan
  2. 2.CAS Key Laboratory of Urban Pollutant Conversion, Institute of Urban EnvironmentChinese Academy of SciencesXiamenChina
  3. 3.Department of Bioprocess Technology, Faculty of Biotechnology and Biomolecular SciencesUniversiti Putra MalaysiaSerdangMalaysia

Personalised recommendations