Advertisement

Extremophiles

, Volume 21, Issue 1, pp 15–26 | Cite as

“Hot” acetogenesis

  • Mirko Basen
  • Volker Müller
Special Feature: Review 11th International Congress on Extremophiles
Part of the following topical collections:
  1. 11th International Congress on Extremophiles

Abstract

Thermophilic microorganisms as well as acetogenic bacteria are both considered ancient. Interestingly, only a few species of bacteria, all belonging to the family Thermoanaerobacteraceae, are described to conserve energy from acetate formation with hydrogen as electron donor and carbon dioxide as electron acceptor. This review reflects the metabolic differences between Moorella spp., Thermoanaerobacter kivui and Thermacetogenium phaeum, with focus on the biochemistry of autotrophic growth and energy conservation. The potential of these thermophilic acetogens for biotechnological applications is discussed briefly.

Keywords

Acetogenesis Thermophiles Thermoanaerobacter kivui Moorella thermoacetica Thermacetogenium phaeum Wood-Ljungdahl pathway CODH/ACS 

Abbreviations

WLP

Wood-Ljungdahl pathway

CODH/ACS

CO dehydrogenase/acetyl-CoA synthase

Fd

Ferredoxin

Ech

Energy converting hydrogenase

Notes

Acknowledgments

We would like to thank the Deutsche Forschungsgemeinschaft (DFG) for generous support.

References

  1. Alves JI, van Gelder AH, Alves MM, Sousa DZ, Plugge CM (2013) Moorella stamsii sp nov., a new anaerobic thermophilic hydrogenogenic carboxydotroph isolated from digester sludge. Int J Syst Evol Microbiol 63:4072–4076CrossRefPubMedGoogle Scholar
  2. Amend JP, Shock EL (1998) Energetics of amino acid synthesis in hydrothermal ecosystems. Science 281:1659–1662CrossRefPubMedGoogle Scholar
  3. Amend JP, Shock EL (2001) Energetics of overall metabolic reactions of thermophilic and hyperthermophilic archaea and bacteria. FEMS Microbiol Rev 25:175–243CrossRefPubMedGoogle Scholar
  4. Amend JP, LaRowe DE, McCollom TM, Shock EL (2013) The energetics of organic synthesis inside and outside the cell. Phil Trans R Soc B 368:20120255CrossRefPubMedPubMedCentralGoogle Scholar
  5. Balk M, Weijma J, Friedrich MW, Stams AJM (2003) Methanol utilization by a novel thermophilic homoacetogenic bacterium, Moorella mulderi sp nov., isolated from a bioreactor. Arch Microbiol 179:315–320CrossRefPubMedGoogle Scholar
  6. Balk M, van Gelder T, Weelink SA, Stams AJA (2008) (Per)chlorate reduction by the thermophilic bacterium Moorella perchloratireducens sp. nov., isolated from underground gas storage. Appl Environ Microbiol 74:403–409CrossRefPubMedGoogle Scholar
  7. Basen M et al (2014) Single gene insertion drives bioalcohol production by a thermophilic archaeon. Proc Natl Acad Sci USA 111:17618–17623CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bender G, Ragsdale SW (2011) Evidence that ferredoxin interfaces with an internal redox shuttle in acetyl-CoA synthase during reductive activation and catalysis. Biochemistry 50:276–286CrossRefPubMedGoogle Scholar
  9. Bertsch J, Müller V (2015) Bioenergetic constraints for conversion of syngas to biofuels in acetogenic bacteria. Biotechnol Biofuels 8:210CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bertsch J, Öppinger C, Hess V, Langer JD, Müller V (2015) Heterotrimeric NADH-oxidizing methylenetetrahydrofolate reductase from the acetogenic bacterium Acetobacterium woodii. J Bacteriol 197:1681–1689CrossRefPubMedPubMedCentralGoogle Scholar
  11. Biegel E, Müller V (2010) Bacterial Na+-translocating ferredoxin: NAD+ oxidoreductase. Proc Natl Acad Sci USA 107:18138–18142CrossRefPubMedPubMedCentralGoogle Scholar
  12. Biegel E, Schmidt S, Müller V (2009) Genetic, immunological and biochemical evidence for a Rnf complex in the acetogen Acetobacterium woodii. Environ Microbiol 11:1438–1443CrossRefPubMedGoogle Scholar
  13. Brandt K, Müller DB, Hoffmann J, Langer JD, Brutschy B, Morgner N, Müller V (2016) Stoichiometry and deletion analyses of subunits in the heterotrimeric F-ATP synthase c ring from the acetogenic bacterium Acetobacterium woodii. FEBS J 283:510–520CrossRefPubMedGoogle Scholar
  14. Daniel SL, Hsu T, Dean SI, Drake HL (1990) Characterization of the H2− and CO-dependent chemolithotrophic potentials of the acetogens Clostridium thermoaceticum and Acetogenium kivui. J Bacteriol 172:4464–4471CrossRefPubMedPubMedCentralGoogle Scholar
  15. Drake HL (1994) Acetogenesis. Chapman & Hall, New YorkGoogle Scholar
  16. Fontaine FE, Peterson WH, McCoy E, Johnson MJ, Ritter GJ (1942) A new type of glucose fermentation by Clostridium thermoaceticum n. sp. J Bacteriol 43:701–715PubMedPubMedCentralGoogle Scholar
  17. Gildemyn S, Verbeeck K, Slabbinck R, Andersen SJ, Prevoteau A, Rabaey K (2015) Integrated production, extraction, and concentration of acetic acid from CO2 through microbial electrosynthesis. Environ Sci Technol Lett 2:325–328CrossRefGoogle Scholar
  18. Gottschal JC, Prins RA (1991) Thermophiles—a life at elevated temperatures. Trends Ecol Evol 6:157–162CrossRefPubMedGoogle Scholar
  19. Grüber G, Manimekalai MSS, Mayer F, Müller V (2014) ATP synthases from archaea: the beauty of a molecular motor. Biochim Biophys Acta (BBA)-Bioenergetics 1837:940–952CrossRefGoogle Scholar
  20. Hattori S, Kamagata Y, Hanada S, Shoun H (2000) Thermacetogenium phaeum gen. nov., sp nov., a strictly anaerobic, thermophilic, syntrophic acetate-oxidizing bacterium. Int J Syst Evol Microbiol 50:1601–1609CrossRefPubMedGoogle Scholar
  21. He Y et al (2016) Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol 1:16035CrossRefPubMedGoogle Scholar
  22. Heise R, Reidlinger J, Müller V, Gottschalk G (1991) A sodium-stimulated ATP synthase in the acetogenic bacterium Acetobacterium woodii. FEBS Lett 295:119–122CrossRefPubMedGoogle Scholar
  23. Hess V, Poehlein A, Weghoff MC, Daniel R, Müller V (2014) A genome-guided analysis of energy conservation in the thermophilic, cytochrome-free acetogenic bacterium Thermoanaerobacter kivui. BMC Genom 15:1139CrossRefGoogle Scholar
  24. Hu P, Rismani-Yazdi H, Stephanopoulos G (2013) Anaerobic CO2 fixation by the acetogenic bacterium Moorella thermoacetica. AlChE J 59:3176–3183CrossRefGoogle Scholar
  25. Huang HY, Wang SN, Moll J, Thauer RK (2012) Electron bifurcation involved in the energy metabolism of the acetogenic bacterium Moorella thermoacetica growing on glucose or H2 plus CO2. J Bacteriol 194:3689–3699CrossRefPubMedPubMedCentralGoogle Scholar
  26. Huber C, Wächtershauser G (1997) Activated acetic acid by carbon fixation on (Fe, Ni)S under primordial conditions. Science 276:245–247CrossRefPubMedGoogle Scholar
  27. Inokuma K, Nakashimada Y, Akahoshi T, Nishio N (2007) Characterization of enzymes involved in the ethanol production of Moorella sp. HUC22-1. Arch Microbiol 188:37–45CrossRefPubMedGoogle Scholar
  28. Jouanneau Y, Jeong HS, Hugo N, Meyer C, Willison JC (1998) Overexpression in Escherichia coli of the rnf genes from Rhodobacter capsulatus—characterization of two membrane-bound iron-sulfur proteins. Eur J Biochem 251:54–64CrossRefPubMedGoogle Scholar
  29. Kasting JF, Howard MT (2006) Atmospheric composition and climate on the early Earth. Philos T R Soc B 361:1733–1741CrossRefGoogle Scholar
  30. Kelley DS et al (2005) A serpentinite-hosted ecosystem: the lost city hydrothermal field. Science 307:1428–1434CrossRefPubMedGoogle Scholar
  31. Kita A et al (2013) Development of genetic transformation and heterologous expression system in carboxydotrophic thermophilic acetogen Moorella thermoacetica. J Biosci Bioeng 115:347–352CrossRefPubMedGoogle Scholar
  32. Klemps R, Schoberth SM, Sahm H (1987) Production of acetic acid by Acetogenium kivui. Appl Microbiol Biotechnol 27:229–234CrossRefGoogle Scholar
  33. Köpke M et al (2010) Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc Natl Acad Sci USA 107:13087–13092CrossRefPubMedPubMedCentralGoogle Scholar
  34. Le Ruyet P, Dubourguier HC, Albagnac G (1984) Homoacetogenic fermentation of cellulose by a coculture of Clostridium thermocellum and Acetogenium kivui. Appl Environ Microbiol 48:893–894PubMedPubMedCentralGoogle Scholar
  35. Leigh JA, Wolfe RS (1983) Acetogenium kivui gen. nov., sp. nov., a thermophilic acetogenic bacterium. Int J Syst Bacteriol 33:886CrossRefGoogle Scholar
  36. Leigh JA, Mayer F, Wolfe RS (1981) Acetogenium kivui, a new thermophilic hydrogen-oxidizing, acetogenic bacterium. Arch Microbiol 129:275–280CrossRefGoogle Scholar
  37. Lindahl PA, Chang B (2001) The evolution of acetyl-CoA synthase. Orig Life Evol B 31:403–434CrossRefGoogle Scholar
  38. Ljungdahl LG (2009) A life with acetogens, thermophiles, and cellulolytic anaerobes. Annu Rev Microbiol 63:1–25CrossRefPubMedGoogle Scholar
  39. Lunine JI (2006) Physical conditions on the early Earth. Philos T R Soc B 361:1721–1731CrossRefGoogle Scholar
  40. Martin W, Russell MJ (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos T Roy Soc B 358:59–83CrossRefGoogle Scholar
  41. Martin WF, Sousa FL (2016) Early microbial evolution: the age of anaerobes. Cold Spring Harbor Perspect Biol 8:18CrossRefGoogle Scholar
  42. Mayer F, Müller V (2014) Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiol Rev 38:449–472CrossRefPubMedGoogle Scholar
  43. Mock J, Wang SN, Huang HY, Kahnt J, Thauer RK (2014) Evidence for a hexaheteromeric methylenetetrahydrofolate reductase in Moorella thermoacetica. J Bacteriol 196:3303–3314CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mock J et al (2015) Energy conservation associated with ethanol formation from H2 and CO2 in Clostridium autoethanogenum involving electron bifurcation. J Bacteriol 197:2965–2980CrossRefPubMedPubMedCentralGoogle Scholar
  45. Nevin KP et al (2011) Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl Environ Microbiol 77:2882–2886CrossRefPubMedPubMedCentralGoogle Scholar
  46. Oehler D, Poehlein A, Leimbach A, Müller N, Daniel R, Gottschalk G, Schink B (2012) Genome-guided analysis of physiological and morphological traits of the fermentative acetate oxidizer Thermacetogenium phaeum. BMC Genomics 13:723CrossRefPubMedPubMedCentralGoogle Scholar
  47. Olson DG, Sparling R, Lynd LR (2015) Ethanol production by engineered thermophiles. Curr Opin Biotechnol 33:130–141CrossRefPubMedGoogle Scholar
  48. Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740CrossRefPubMedGoogle Scholar
  49. Pierce E et al (2008) The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum). Environ Microbiol 10:2550–2573CrossRefPubMedPubMedCentralGoogle Scholar
  50. Ragsdale SW (2004) Life with carbon monoxide. Crit Rev Biochem Mol 39:165–195CrossRefGoogle Scholar
  51. Ragsdale SW, Ljungdahl LG (1984) Purification and properties of NAD-dependent 5,10-methylenetetrahydrolate dehydrogenase from Acetobacterium woodii. J Biol Chem 259:3499–3503PubMedGoogle Scholar
  52. Rosenbaum MA, Henrich AW (2014) Engineering microbial electrocatalysis for chemical and fuel production. Curr Opin Biotechnol 29:93–98CrossRefPubMedGoogle Scholar
  53. Russell MJ, Hall AJ, Martin W (2010) Serpentinization as a source of energy at the origin of life. Geobiology 8:355–371CrossRefPubMedGoogle Scholar
  54. Sakimoto KK, Wong AB, Yang P (2016) Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351:74–77CrossRefPubMedGoogle Scholar
  55. Schmehl M et al (1993) Identification of a new class of nitrogen fixation genes in Rhodobacter capsulatus—a putative membrane complex involved in electron transport to nitrogenase. Mol Gen Genet 241:602–615CrossRefPubMedGoogle Scholar
  56. Schönheit P, Buckel W, Martin WF (2016) On the origin of heterotrophy. Trends Microbiol 24:12–25CrossRefPubMedGoogle Scholar
  57. Schuchmann K, Müller V (2012) A bacterial electron-bifurcating hydrogenase. J Biol Chem 287:31165–31171CrossRefPubMedPubMedCentralGoogle Scholar
  58. Schuchmann K, Müller V (2013) Direct and reversible hydrogenation of CO2 to formate by a bacterial carbon dioxide reductase. Science 342:1382–1385CrossRefPubMedGoogle Scholar
  59. Schuchmann K, Müller V (2014) Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12:809–821CrossRefPubMedGoogle Scholar
  60. Schuchmann K, Müller V (2016) Energetics and application of heterotrophy in acetogenic bacteria. Appl Environ Microbiol 82:4056–4069CrossRefPubMedPubMedCentralGoogle Scholar
  61. Schuchmann K, Vonck J, Müller V (2016) A bacterial hydrogen-dependent CO2 reductase forms filamentous structures. FEBS J 283:1311–1322CrossRefPubMedGoogle Scholar
  62. Schut GJ, Adams MWW (2009) The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191:4451–4457CrossRefPubMedPubMedCentralGoogle Scholar
  63. Shao X, Zhou J, Olson DG, Lynd LR (2016) A markerless gene deletion and integration system for Thermoanaerobacter ethanolicus. Biotechnol Biofuels 9:1–8CrossRefGoogle Scholar
  64. Shaw AJ, Hogsett DA, Lynd LR (2010) Natural Competence in Thermoanaerobacter and Thermoanaerobacterium Species. Appl Environ Microbiol 76:4713–4719CrossRefPubMedPubMedCentralGoogle Scholar
  65. Simon H, White H, Lebertz H, Thanos I (1987) Reduction of 2-enoates and alkanoates with carbon monoxide or formate, viologens, and Clostridium thermoaceticum to saturated acids and unsaturated and saturated alcohols. Angew Chem Int Edit 26:785–787CrossRefGoogle Scholar
  66. Sousa FL et al (2013) Early bioenergetic evolution. Philos T R Soc B 368:20130088CrossRefGoogle Scholar
  67. Stetter KO (2006) History of discovery of the first hyperthermophiles. Extremophiles 10:357–362CrossRefPubMedGoogle Scholar
  68. Takami H et al (2012) A deeply branching thermophilic bacterium with an ancient acetyl-CoA pathway dominates a subsurface ecosystem. PLoS One 7:e30559CrossRefPubMedPubMedCentralGoogle Scholar
  69. Tamimi A, Rinker EB, Sandall OC (1994) Diffusion coefficients for hydrogen sulfide, carbon dioxide, and nitrous oxide in water over the temperature range 293–368 K. J Chem Eng Data 39:330–332CrossRefGoogle Scholar
  70. Taylor MP, Eley KL, Martin S, Tuffin MI, Burton SG, Cowan DA (2009) Thermophilic ethanologenesis: future prospects for second-generation bioethanol production. Trends Biotechnol 27:398–405CrossRefPubMedGoogle Scholar
  71. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotropic anaerobic bacteria. Bacteriol Rev 41:100–180PubMedPubMedCentralGoogle Scholar
  72. Tremblay P-L, Zhang T, Dar SA, Leang C, Lovley DR (2013) The Rnf complex of Clostridium ljungdahlii is a proton-translocating ferredoxin:NAD+ oxidoreductase essential for autotrophic growth. Mbio 4:e00406–e00412Google Scholar
  73. Tschech A, Pfennig N (1984) Growth yield increase linked to caffeate reduction in Acetobacterium woodii. Arch Microbiol 137:163–167CrossRefGoogle Scholar
  74. Verbeke TJ et al (2013) Genomic evaluation of Thermoanaerobacter spp. for the construction of designer co-cultures to improve lignocellulosic biofuel production. PLoS One 8:e59362CrossRefPubMedPubMedCentralGoogle Scholar
  75. Wang SN, Huang HY, Kahnt J, Müller AP, Köpke M, Thauer RK (2013) NADP-specific electron-bifurcating [FeFe]-hydrogenase in a functional complex with formate dehydrogenase in Clostridium autoethanogenum grown on CO. J Bacteriol 195:4373–4386CrossRefPubMedPubMedCentralGoogle Scholar
  76. Weghoff MC, Müller V (2016) CO metabolism in the thermophilic acetogen Thermoanaerobacter kivui. Appl Environ Microbiol 82:2312–2319CrossRefPubMedPubMedCentralGoogle Scholar
  77. Westall F et al (2015) Archean (3.33 Ga) microbe-sediment systems were diverse and flourished in a hydrothermal context. Geology 43:615–618CrossRefGoogle Scholar
  78. Wiegel J (1998) Anaerobic alkalithermophiles, a novel group of extremophiles. Extremophiles 2:257–267CrossRefPubMedGoogle Scholar
  79. Wiegel J (2009) Genus Moorella. In: De Vos P et al (eds) Bergey’s manual of systematic bacteriology, vol 3: the firmicutes, 2nd edn. Springer, New York, pp 1247–1253Google Scholar
  80. Yamamoto I, Saiki T, Liu SM, Ljungdahl LG (1983) Purification and properties of NADP-dependent formate dehydrogenase from Clostridium thermoaceticum, a tungsten-selenium-iron protein. J Biol Chem 258:1826–1832PubMedGoogle Scholar
  81. Yao S, Mikkelsen MJ (2010) Metabolic engineering to improve ethanol production in Thermoanaerobacter mathranii. Appl Microbiol Biotechnol 88:199–208CrossRefPubMedGoogle Scholar
  82. Zheng YN, Kahnt J, Kwon IH, Mackie RI, Thauer RK (2014) Hydrogen formation and its regulation in Ruminococcus albus: involvement of an electron-bifurcating [FeFe]-hydrogenase, of a non-electron-bifurcating [FeFe]-hydrogenase, and of a putative hydrogen-sensing [FeFe]-hydrogenase. J Bacteriol 196:3840–3852CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  1. 1.Department of Molecular Microbiology and Bioenergetics, Institute of Molecular BiosciencesJohann Wolfgang Goethe UniversityFrankfurt Am MainGermany

Personalised recommendations