Conductive iron oxides accelerate thermophilic methanogenesis from acetate and propionate

Journal of Bioscience and Bioengineering

Volumn 119, Issue 6, 2015, Pages 678-682

  Yamada, Chihaya ^a   Kato, Souichiro ^b,c,d   Ueno, Yoshiyuki ^e   Ishii, Masaharu ^a   Igarashi, Yasuo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e KAJIMA TECHNICAL RESEARCH INSTITUTE   (Japan)

Author keywords

CH4; Conductive iron oxides; Degradation of organic acid; Magnetite; Methane production; Methanogenic degradation; Syntrophic relationship; Thermophilic anaerobic digestion; Thermophilic methane fermentation

Indexed keywords

IRON OXIDES; MAGNETITE; METHANE; MICROORGANISMS; VOLATILE FATTY ACIDS; WASTEWATER TREATMENT;

CONTINUOUS DEVELOPMENT; METHANE FERMENTATION; METHANE PRODUCTION; MICROBIAL COMMUNITY ANALYSIS; SYNTROPHIC RELATIONSHIP; THERMOPHILIC ANAEROBIC DIGESTER; THERMOPHILIC ANAEROBIC DIGESTION; THERMOPHILIC CONDITIONS;

ANAEROBIC DIGESTION;

ACETIC ACID; FERRIC HYDROXIDE; IRON OXIDE; PROPIONIC ACID; FERRIC ION; MAGNETITE; METHANE; PROPIONIC ACID DERIVATIVE;

ANAEROBIC DIGESTION; ARTICLE; BACTERIUM CULTURE; COPROTHERMOBACTER PROTEOLYTICUS; GEOBACTER SULFURREDUCENS; METHANOGENESIS; METHANOGENIC BACTERIUM; METHANOSARCINA THERMOPHILA; MICROBIAL COMMUNITY; MICROBIAL DEGRADATION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; TEPIDOANAEROBACTER ACETOOXIDANS; TEPIDOANAEROBACTER SYNTROPHICUS; THERMOPHILIC BACTERIUM; ANAEROBIC GROWTH; ARCHAEON; BACTERIUM; ELECTRON TRANSPORT; FERMENTATION; METABOLISM; TEMPERATURE;

BACTERIA (MICROORGANISMS); COPROTHERMOBACTER;

ACETIC ACID; ANAEROBIOSIS; ARCHAEA; BACTERIA; ELECTRON TRANSPORT; FERMENTATION; FERRIC COMPOUNDS; FERROSOFERRIC OXIDE; METHANE; PROPIONATES; TEMPERATURE;

EID: 84928978320     PISSN: 13891723     EISSN: 13474421     Source Type: Journal    
DOI: 10.1016/j.jbiosc.2014.11.001     Document Type: Article

References (58)

1. Speece R.E. Anaerobic biotechnology for industrial wastewater-treatment. Environ. Sci. Technol. 1983, 17:A416-A427.
2. Mata-Alvarez J., Mace S., Llabres P. Anaerobic digestion of organic solid wastes. An overview of research achievements and perspectives. Bioresour. Technol. 2000, 74:3-16.
3. Kim J.K., Oh B.R., Chun Y.N., Kim S.W. Effects of temperature and hydraulic retention time on anaerobic digestion of food waste. J.Biosci. Bioeng. 2006, 102:328-332.
4. Sasaki D., Hori T., Haruta S., Ueno Y., Ishii M., Igarashi Y. Methanogenic pathway and community structure in a thermophilic anaerobic digestion process of organic solid waste. J.Biosci. Bioeng. 2011, 111:41-46.
5. Suryawanshi P.C., Chaudhari A.B., Kothari R.M. Thermophilic anaerobic digestion: the best option for waste treatment. Crit. Rev. Biotechnol. 2010, 30:31-40.
6. van Lier J.B., Groeneveld N., Lettinga G. Development of thermophilic methanogenic sludge in compartmentalized upflow reactors. Biotechnol. Bioeng. 1996, 50:115-124.
7. Shigematsu T., Tang Y., Mizuno Y., Kawaguchi H., Morimura S., Kida K. Microbial diversity of mesophilic methanogenic consortium that can degrade long-chain fatty acids in chemostat cultivation. J.Biosci. Bioeng. 2006, 102:535-544.
8. Shigematsu T., Tang Y.Q., Kobayashi T., Kawaguchi H., Morimura S., Kida K. Effect of dilution rate on metabolic pathway shift between aceticlastic and nonaceticlastic methanogenesis in chemostat cultivation. Appl. Environ. Microbiol. 2004, 70:4048-4052.
9. Labatut R.A., Angenent L.T., Scott N.R. Conventional mesophilic vs. thermophilic anaerobic digestion: a trade-off between performance and stability?. Water Res. 2014, 53:249-258.
10. Leven L., Eriksson A.R.B., Schnurer A. Effect of process temperature on bacterial and archaeal communities in two methanogenic bioreactors treating organic household waste. FEMS Microbiol. Ecol. 2007, 59:683-693.
11. Raskin L., Poulsen L.K., Noguera D.R., Rittmann B.E., Stahl D.A. Quantification of methanogenic groups in anaerobic biological reactors by oligonucleotide probe hybridization. Appl. Environ. Microbiol. 1994, 60:1241-1248.
12. Amani T., Nosrati M., Mousavi S.M., Kermanshahi R.K. Study of syntrophic anaerobic digestion of volatile fatty acids using enriched cultures at mesophilic conditions. Int. J. Environ. Sci. Tech. 2011, 8:83-96.
13. Kida K., Morimura S., Sonoda Y. Accumulation of propionic acid during anaerobic treatment of distillery wastewater from barley-shochu making. J.Ferment. Bioeng. 1993, 75:213-216.
14. de Bok F.A., Plugge C.M., Stams A.J. Interspecies electron transfer in methanogenic propionate degrading consortia. Water Res. 2004, 38:1368-1375.
15. Imachi H., Sakai S., Ohashi A., Harada H., Hanada S., Kamagata Y., Sekiguchi Y. Pelotomaculum propionicicum sp. nov., an anaerobic, mesophilic, obligately syntrophic propionate-oxidizing bacterium. Int. J. Syst. Evol. Microbiol. 2007, 57:1487-1492.
16. Stams A.J., Plugge C.M. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 2009, 7:568-577.
17. Ishii S., Kosaka T., Hori K., Hotta Y., Watanabe K. Coaggregation facilitates interspecies hydrogen transfer between Pelotomaculum thermopropionicum and Methanothermobacter thermautotrophicus. Appl. Environ. Microbiol. 2005, 71:7838-7845.
18. Schink B., Stams A.J.M. Syntrophism among prokaryotes, p. 309-335. Ecophysiology and biochemistry 2006, vol. 2. Springer, New York. 3rd ed. M. Dworkin, S. Falkow, E. Rosenberg, K.H. Schleifer, E. Stackebrandt (Eds.).
19. Jetten M.S.M., Stams A.J.M., Zehnder A.J.B. Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiol. Lett. 1992, 88:181-197.
20. Thauer R.K., Kaster A.K., Seedorf H., Buckel W., Hedderich R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 2008, 6:579-591.
21. Zinder S.H., Koch M. Non-aceticlastic methanogenesis from acetate: acetate oxidation by a thermophilic syntrophic coculture. Arch. Microbiol. 1984, 138:263-272.
22. Hattori S. Syntrophic acetate-oxidizing microbes in methanogenic environments. Microbes Environ. 2008, 23:118-127.
23. Lu F., Hao L., Guan D., Qi Y., Shao L., He P. Synergetic stress of acids and ammonium on the shift in the methanogenic pathways during thermophilic anaerobic digestion of organics. Water Res. 2013, 47:2297-2306.
24. Angelidaki I., Ahring B.K. Anaerobic thermophilic digestion of manure at different ammonia loads: effect of temperature. Water Res. 1994, 28:727-731.
25. Kato S., Sasaki K., Watanabe K., Yumoto I., Kamagata Y. Physiological and transcriptomic analyses of the thermophilic, aceticlastic methanogen methanosaeta thermophila responding to ammonia stress. Microbes Environ. 2014, 29:162-167.
26. Qu X., Vavilin V.A., Mazeas L., Lemunier M., Duquennoi C., He P.J., Bouchez T. Anaerobic biodegradation of cellulosic material: batch experiments and modelling based on isotopic data and focusing on aceticlastic and non-aceticlastic methanogenesis. Waste Manag. 2009, 29:1828-1837.
27. Schink B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 1997, 61:262-280.
28. Stams A.J., de Bok F.A., Plugge C.M., van Eekert M.H., Dolfing J., Schraa G. Exocellular electron transfer in anaerobic microbial communities. Environ. Microbiol. 2006, 8:371-382.
29. Summers Z.M., Fogarty H.E., Leang C., Franks A.E., Malvankar N.S., Lovley D.R. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 2010, 330:1413-1415.
30. Kato S., Hashimoto K., Watanabe K. Microbial interspecies electron transfer via electric currents through conductive minerals. Proc. Natl. Acad. Sci. USA 2012, 109:10042-10046.
31. Kato S., Hashimoto K., Watanabe K. Methanogenesis facilitated by electric syntrophy via (semi)conductive iron-oxide minerals. Environ. Microbiol. 2012, 14:1646-1654.
32. Morita M., Malvankar N.S., Franks A.E., Summers Z.M., Giloteaux L., Rotaru A.E., Rotaru C., Lovley D.R. Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. MBio 2011, 2. e00159-e00111.
33. Zhou S., Xu J., Yang G., Zhuang L. Methanogenesis affected by the co-occurrence of iron(III) oxides and humic substances. FEMS Microbiol. Ecol. 2014, 88:107-120.
34. Liu F., Rotaru A.-E., Shrestha P.M., Malvankar N.S., Nevin K.P., Lovley D.R. Promoting direct interspecies electron transfer with activated carbon. Energy Environ. Sci. 2012, 5:8982-8989.
35. Cruz Viggi C., Rossetti S., Fazi S., Paiano P., Majone M., Aulenta F. Magnetite particles triggering a faster and more robust syntrophic pathway of methanogenic propionate degradation. Environ. Sci. Technol. 2014, 48:7536-7543.
36. Rotaru A.E., Shrestha P.M., Liu F., Shrestha M., Shrestha D., Embree M., Zengler K., Wardman C., Nevin K.P., Lovley D.R. Anew model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ. Sci. 2014, 7:408-415.
37. Tatara M., Yamazawa A., Ueno Y., Fukui H., Goto M., Sode K. High-rate thermophilic methane fermentation on short-chain fatty acids in a down-flow anaerobic packed-bed reactor. Bioprocess Biosyst. Eng. 2005, 27:105-113.
38. Lovley D.R., Phillips E.J.P. Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl. Environ. Microbiol. 1986, 51:683-689.
39. 3 particles. Chem. Mater. 1996, 8:2209-2211.
40. Lovley D. Dissimilatory Fe(III)- and Mn(IV)-reducing prokaryotes. Ecophysiology and biochemistry 2006, vol. 2:635-658. Springer, New York. 3rd ed. M. Dworkin, S. Falkow, E. Rosenberg, K.H. Schleifer, E. Stackebrandt (Eds.).
41. Noll M., Matthies D., Frenzel P., Derakshani M., Liesack W. Succession of bacterial community structure and diversity in a paddy soil oxygen gradient. Environ. Microbiol. 2005, 7:382-395.
42. Akuzawa M., Hori T., Haruta S., Ueno Y., Ishii M., Igarashi Y. Distinctive responses of metabolically active microbiota to acidification in a thermophilic anaerobic digester. Microb. Ecol. 2011, 61:595-605.
43. Lueders T., Friedrich M.W. Effects of amendment with ferrihydrite and gypsum on the structure and activity of methanogenic populations in rice field soil. Appl. Environ. Microbiol. 2002, 68:2484-2494.
44. 13C-acetate probing. ISME J. 2010, 4:267-278.
45. Reiche M., Torburg G., Kusel K. Competition of Fe(III) reduction and methanogenesis in an acidic fen. FEMS Microbiol. Ecol. 2008, 65:88-101.
46. Yamada C., Kato S., Ueno Y., Ishii M., Igarashi Y. Inhibitory effects of ferrihydrite on a thermophilic methanogenic community. Microbes Environ. 2014, 29:227-230.
47. Lovley D.R., Stolz J.F., Nord G.L., Phillips E.J.P. Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism. Nature 1987, 330:252-254.
48. Liu S.V., Zhou J.Z., Zhang C.L., Cole D.R., GajdarziskaJosifovska M., Phelps T.J. Thermophilic Fe(III)-reducing bacteria from the deep subsurface: the evolutionary implications. Science 1997, 277:1106-1109.
49. Vargas M., Kashefi K., Blunt-Harris E.L., Lovley D.R. Microbiological evidence for Fe(III) reduction on early Earth. Nature 1998, 395:65-67.
50. Vali H., Weiss B., Li Y.L., Sears S.K., Kim S.S., Kirschvink J.L., Zhang L. Formation of tabular single-domain magnetite induced by Geobacter metallireducens GS-15. Proc. Natl. Acad. Sci. USA 2004, 101:16121-16126.
51. Wu W.F., Li B., Hu J., Li J.H., Wang F.P., Pan Y.X. Iron reduction and magnetite biomineralization mediated by a deep-sea iron-reducing bacterium Shewanella piezotolerans WP3. J.Geophys. Res. 2011, 116. G04034.
52. Kato S., Nakamura R., Kai F., Watanabe K., Hashimoto K. Respiratory interactions of soil bacteria with (semi)conductive iron-oxide minerals. Environ. Microbiol. 2010, 12:3114-3123.
53. Yamada C., Kato S., Kimura S., Ishii M., Igarashi Y. Reduction of Fe(III) oxides by phylogenetically and physiologically diverse thermophilic methanogens. FEMS Microbiol. Ecol. 2014, 89:637-645.
54. Sekiguchi Y., Imachi H., Susilorukmi A., Muramatsu M., Ohashi A., Harada H., Hanada S., Kamagata Y. Tepidanaerobacter syntrophicus gen. nov., sp. nov., an anaerobic, moderately thermophilic, syntrophic alcohol- and lactate-degrading bacterium isolated from thermophilic digested sludges. Int. J. Syst. Evol. Microbiol. 2006, 56:1621-1629.
55. Westerholm M., Roos S., Schnurer A. Tepidanaerobacter acetatoxydans sp. nov., an anaerobic, syntrophic acetate-oxidizing bacterium isolated from two ammonium-enriched mesophilic methanogenic processes. Syst. Appl. Microbiol. 2011, 34:260-266.
56. Ollivier B.M., Mah R.A., Ferguson T.J., Boone D.R., Garcia J.L., Robinson R. Emendation of the genus Thermobacteroides: Thermobacteroides proteolyticus sp. nov., a proteolytic acetogen from a methanogenic enrichment. Int. J. Syst. Bacteriol. 1985, 35:425-428.
57. Wrighton K.C., Agbo P., Warnecke F., Weber K.A., Brodie E.L., DeSantis T.Z., Hugenholtz P., Andersen G.L., Coates J.D. Anovel ecological role of the Firmicutes identified in thermophilic microbial fuel cells. ISME J. 2008, 2:1146-1156.
58. 2 for methanogenesis. Appl. Environ. Microbiol. 1979, 38:996-1008.