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“Hot” acetogenesis

  • Special Feature: Review
  • 11th International Congress on Extremophiles
  • Published:
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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.

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Abbreviations

WLP:

Wood-Ljungdahl pathway

CODH/ACS:

CO dehydrogenase/acetyl-CoA synthase

Fd:

Ferredoxin

Ech:

Energy converting hydrogenase

References

  • 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 63:4072–4076

    Article  CAS  PubMed  Google Scholar 

  • Amend JP, Shock EL (1998) Energetics of amino acid synthesis in hydrothermal ecosystems. Science 281:1659–1662

    Article  CAS  PubMed  Google Scholar 

  • Amend JP, Shock EL (2001) Energetics of overall metabolic reactions of thermophilic and hyperthermophilic archaea and bacteria. FEMS Microbiol Rev 25:175–243

    Article  CAS  PubMed  Google Scholar 

  • Amend JP, LaRowe DE, McCollom TM, Shock EL (2013) The energetics of organic synthesis inside and outside the cell. Phil Trans R Soc B 368:20120255

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 179:315–320

    Article  CAS  PubMed  Google Scholar 

  • 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 74:403–409

    Article  CAS  PubMed  Google Scholar 

  • Basen M et al (2014) Single gene insertion drives bioalcohol production by a thermophilic archaeon. Proc Natl Acad Sci USA 111:17618–17623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bender G, Ragsdale SW (2011) Evidence that ferredoxin interfaces with an internal redox shuttle in acetyl-CoA synthase during reductive activation and catalysis. Biochemistry 50:276–286

    Article  CAS  PubMed  Google Scholar 

  • Bertsch J, Müller V (2015) Bioenergetic constraints for conversion of syngas to biofuels in acetogenic bacteria. Biotechnol Biofuels 8:210

    Article  PubMed  PubMed Central  Google Scholar 

  • Bertsch J, Öppinger C, Hess V, Langer JD, Müller V (2015) Heterotrimeric NADH-oxidizing methylenetetrahydrofolate reductase from the acetogenic bacterium Acetobacterium woodii. J Bacteriol 197:1681–1689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biegel E, Müller V (2010) Bacterial Na+-translocating ferredoxin: NAD+ oxidoreductase. Proc Natl Acad Sci USA 107:18138–18142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biegel E, Schmidt S, Müller V (2009) Genetic, immunological and biochemical evidence for a Rnf complex in the acetogen Acetobacterium woodii. Environ Microbiol 11:1438–1443

    Article  CAS  PubMed  Google Scholar 

  • 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 283:510–520

    Article  CAS  PubMed  Google Scholar 

  • 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 172:4464–4471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drake HL (1994) Acetogenesis. Chapman & Hall, New York

    Google Scholar 

  • Fontaine FE, Peterson WH, McCoy E, Johnson MJ, Ritter GJ (1942) A new type of glucose fermentation by Clostridium thermoaceticum n. sp. J Bacteriol 43:701–715

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 2:325–328

    Article  CAS  Google Scholar 

  • Gottschal JC, Prins RA (1991) Thermophiles—a life at elevated temperatures. Trends Ecol Evol 6:157–162

    Article  CAS  PubMed  Google Scholar 

  • Grüber G, Manimekalai MSS, Mayer F, Müller V (2014) ATP synthases from archaea: the beauty of a molecular motor. Biochim Biophys Acta (BBA)-Bioenergetics 1837:940–952

    Article  Google Scholar 

  • 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 50:1601–1609

    Article  CAS  PubMed  Google Scholar 

  • 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 1:16035

    Article  CAS  PubMed  Google Scholar 

  • Heise R, Reidlinger J, Müller V, Gottschalk G (1991) A sodium-stimulated ATP synthase in the acetogenic bacterium Acetobacterium woodii. FEBS Lett 295:119–122

    Article  CAS  PubMed  Google Scholar 

  • 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 15:1139

    Article  Google Scholar 

  • Hu P, Rismani-Yazdi H, Stephanopoulos G (2013) Anaerobic CO2 fixation by the acetogenic bacterium Moorella thermoacetica. AlChE J 59:3176–3183

    Article  CAS  Google Scholar 

  • 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 194:3689–3699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huber C, Wächtershauser G (1997) Activated acetic acid by carbon fixation on (Fe, Ni)S under primordial conditions. Science 276:245–247

    Article  CAS  PubMed  Google Scholar 

  • Inokuma K, Nakashimada Y, Akahoshi T, Nishio N (2007) Characterization of enzymes involved in the ethanol production of Moorella sp. HUC22-1. Arch Microbiol 188:37–45

    Article  CAS  PubMed  Google Scholar 

  • 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 251:54–64

    Article  CAS  PubMed  Google Scholar 

  • Kasting JF, Howard MT (2006) Atmospheric composition and climate on the early Earth. Philos T R Soc B 361:1733–1741

    Article  CAS  Google Scholar 

  • Kelley DS et al (2005) A serpentinite-hosted ecosystem: the lost city hydrothermal field. Science 307:1428–1434

    Article  CAS  PubMed  Google Scholar 

  • Kita A et al (2013) Development of genetic transformation and heterologous expression system in carboxydotrophic thermophilic acetogen Moorella thermoacetica. J Biosci Bioeng 115:347–352

    Article  CAS  PubMed  Google Scholar 

  • Klemps R, Schoberth SM, Sahm H (1987) Production of acetic acid by Acetogenium kivui. Appl Microbiol Biotechnol 27:229–234

    Article  CAS  Google Scholar 

  • Köpke M et al (2010) Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc Natl Acad Sci USA 107:13087–13092

    Article  PubMed  PubMed Central  Google Scholar 

  • Le Ruyet P, Dubourguier HC, Albagnac G (1984) Homoacetogenic fermentation of cellulose by a coculture of Clostridium thermocellum and Acetogenium kivui. Appl Environ Microbiol 48:893–894

    PubMed  PubMed Central  Google Scholar 

  • Leigh JA, Wolfe RS (1983) Acetogenium kivui gen. nov., sp. nov., a thermophilic acetogenic bacterium. Int J Syst Bacteriol 33:886

    Article  Google Scholar 

  • Leigh JA, Mayer F, Wolfe RS (1981) Acetogenium kivui, a new thermophilic hydrogen-oxidizing, acetogenic bacterium. Arch Microbiol 129:275–280

    Article  CAS  Google Scholar 

  • Lindahl PA, Chang B (2001) The evolution of acetyl-CoA synthase. Orig Life Evol B 31:403–434

    Article  CAS  Google Scholar 

  • Ljungdahl LG (2009) A life with acetogens, thermophiles, and cellulolytic anaerobes. Annu Rev Microbiol 63:1–25

    Article  CAS  PubMed  Google Scholar 

  • Lunine JI (2006) Physical conditions on the early Earth. Philos T R Soc B 361:1721–1731

    Article  CAS  Google Scholar 

  • 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 358:59–83

    Article  CAS  Google Scholar 

  • Martin WF, Sousa FL (2016) Early microbial evolution: the age of anaerobes. Cold Spring Harbor Perspect Biol 8:18

    Article  Google Scholar 

  • Mayer F, Müller V (2014) Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiol Rev 38:449–472

    Article  CAS  PubMed  Google Scholar 

  • Mock J, Wang SN, Huang HY, Kahnt J, Thauer RK (2014) Evidence for a hexaheteromeric methylenetetrahydrofolate reductase in Moorella thermoacetica. J Bacteriol 196:3303–3314

    Article  PubMed  PubMed Central  Google Scholar 

  • Mock J et al (2015) Energy conservation associated with ethanol formation from H2 and CO2 in Clostridium autoethanogenum involving electron bifurcation. J Bacteriol 197:2965–2980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nevin KP et al (2011) Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl Environ Microbiol 77:2882–2886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 13:723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olson DG, Sparling R, Lynd LR (2015) Ethanol production by engineered thermophiles. Curr Opin Biotechnol 33:130–141

    Article  CAS  PubMed  Google Scholar 

  • Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740

    Article  CAS  PubMed  Google Scholar 

  • Pierce E et al (2008) The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum). Environ Microbiol 10:2550–2573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ragsdale SW (2004) Life with carbon monoxide. Crit Rev Biochem Mol 39:165–195

    Article  CAS  Google Scholar 

  • Ragsdale SW, Ljungdahl LG (1984) Purification and properties of NAD-dependent 5,10-methylenetetrahydrolate dehydrogenase from Acetobacterium woodii. J Biol Chem 259:3499–3503

    CAS  PubMed  Google Scholar 

  • Rosenbaum MA, Henrich AW (2014) Engineering microbial electrocatalysis for chemical and fuel production. Curr Opin Biotechnol 29:93–98

    Article  CAS  PubMed  Google Scholar 

  • Russell MJ, Hall AJ, Martin W (2010) Serpentinization as a source of energy at the origin of life. Geobiology 8:355–371

    Article  CAS  PubMed  Google Scholar 

  • Sakimoto KK, Wong AB, Yang P (2016) Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351:74–77

    Article  CAS  PubMed  Google Scholar 

  • 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 241:602–615

    Article  CAS  PubMed  Google Scholar 

  • Schönheit P, Buckel W, Martin WF (2016) On the origin of heterotrophy. Trends Microbiol 24:12–25

    Article  PubMed  Google Scholar 

  • Schuchmann K, Müller V (2012) A bacterial electron-bifurcating hydrogenase. J Biol Chem 287:31165–31171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuchmann K, Müller V (2013) Direct and reversible hydrogenation of CO2 to formate by a bacterial carbon dioxide reductase. Science 342:1382–1385

    Article  CAS  PubMed  Google Scholar 

  • Schuchmann K, Müller V (2014) Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12:809–821

    Article  CAS  PubMed  Google Scholar 

  • Schuchmann K, Müller V (2016) Energetics and application of heterotrophy in acetogenic bacteria. Appl Environ Microbiol 82:4056–4069

    Article  PubMed  PubMed Central  Google Scholar 

  • Schuchmann K, Vonck J, Müller V (2016) A bacterial hydrogen-dependent CO2 reductase forms filamentous structures. FEBS J 283:1311–1322

    Article  CAS  PubMed  Google Scholar 

  • 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 191:4451–4457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao X, Zhou J, Olson DG, Lynd LR (2016) A markerless gene deletion and integration system for Thermoanaerobacter ethanolicus. Biotechnol Biofuels 9:1–8

    Article  Google Scholar 

  • Shaw AJ, Hogsett DA, Lynd LR (2010) Natural Competence in Thermoanaerobacter and Thermoanaerobacterium Species. Appl Environ Microbiol 76:4713–4719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 26:785–787

    Article  Google Scholar 

  • Sousa FL et al (2013) Early bioenergetic evolution. Philos T R Soc B 368:20130088

    Article  Google Scholar 

  • Stetter KO (2006) History of discovery of the first hyperthermophiles. Extremophiles 10:357–362

    Article  PubMed  Google Scholar 

  • Takami H et al (2012) A deeply branching thermophilic bacterium with an ancient acetyl-CoA pathway dominates a subsurface ecosystem. PLoS One 7:e30559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 39:330–332

    Article  CAS  Google Scholar 

  • Taylor MP, Eley KL, Martin S, Tuffin MI, Burton SG, Cowan DA (2009) Thermophilic ethanologenesis: future prospects for second-generation bioethanol production. Trends Biotechnol 27:398–405

    Article  CAS  PubMed  Google Scholar 

  • Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotropic anaerobic bacteria. Bacteriol Rev 41:100–180

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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–e00412

    CAS  Google Scholar 

  • Tschech A, Pfennig N (1984) Growth yield increase linked to caffeate reduction in Acetobacterium woodii. Arch Microbiol 137:163–167

    Article  CAS  Google Scholar 

  • 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:e59362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 195:4373–4386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weghoff MC, Müller V (2016) CO metabolism in the thermophilic acetogen Thermoanaerobacter kivui. Appl Environ Microbiol 82:2312–2319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westall F et al (2015) Archean (3.33 Ga) microbe-sediment systems were diverse and flourished in a hydrothermal context. Geology 43:615–618

    Article  CAS  Google Scholar 

  • Wiegel J (1998) Anaerobic alkalithermophiles, a novel group of extremophiles. Extremophiles 2:257–267

    Article  CAS  PubMed  Google Scholar 

  • 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 1247–1253

    Google Scholar 

  • 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 258:1826–1832

    CAS  PubMed  Google Scholar 

  • Yao S, Mikkelsen MJ (2010) Metabolic engineering to improve ethanol production in Thermoanaerobacter mathranii. Appl Microbiol Biotechnol 88:199–208

    Article  CAS  PubMed  Google Scholar 

  • 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 196:3840–3852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

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

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  1. Department of Molecular Microbiology and Bioenergetics, Institute of Molecular Biosciences, Johann Wolfgang Goethe University, Frankfurt Am Main, Germany

    Mirko Basen & Volker Müller

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  1. Mirko Basen
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  2. Volker Müller
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Correspondence to Volker Müller.

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Communicated by H. Atomi.

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Basen, M., Müller, V. “Hot” acetogenesis. Extremophiles 21, 15–26 (2017). https://doi.org/10.1007/s00792-016-0873-3

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