View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by PubMed Central GENERAL COMMENTARY published: 31 January 2012 doi: 10.3389/fmicb.2012.00022 There must be an acetogen somewhere Aharon Oren* Department of Plant and Environmental Sciences, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel *Correspondence: [email protected] A commentary on −+ available on (growth parameters) μ, K , 43HH23++CO HC→+HH42O s K , Y, and q of these organisms, prefer- ∆=Gk′ −135.6 J m Acetogenesis in the energy-starved deep o ably obtained in chemostat experiments.” biosphere – a paradox? To my knowledge no such experiments 42HH++CO−−HC+ →+HCOO 4HO by Mark Alexander Lever (2012). Front. 223 3 have yet been performed. ′ Microbiol. 2:284. doi: 10.3389/fmicb.2011.00284 ∆=Gko −104.6 J The question therefore remains where in nature the acetogens can out-compete In the beginning of 1983, when I was a As long as sulfate is available, sul- the methanogens. In recent years evidence post-doctoral student at the University of fate reducers will consume most of the is accumulating that, unexpectedly, aceto- Illinois, Ralph Wolfe handed me an offprint hydrogen. They obtain more energy from gens may represent a quantitatively impor- of a long article and said: “Read this!” That hydrogen oxidation, and their affinity for tant component of the microbial ecosystem paper was the review by Thauer et al. (1977) hydrogen is much higher than that of the in the oligotrophic marine and terrestrial on “Energy conservation in chemotrophic methanogenic Archaea, explaining why deep biosphere. The paper by Lever pro- anaerobic bacteria.” I have read it many the methanogens are out-competed when vides an in-depth analysis of the possible times. I remember that the first and second the energy source is limiting (Kristjansson factors that give the acetogens advantages time I understood very little. During the et al., 1982). When sulfate is limiting, in this vast, but largely unexplored niche. third and fourth reading I started to grasp methanogens will take over. No similar Lever argues that under conditions encoun- the ideas expressed and to appreciate them. competition studies between methano- tered in the subseafloor, the energy yields And after having read the paper for the fifth gens and acetogens were ever reported, of most acetogenesis reactions are sufficient and sixth time I had become convinced that but based on the lower energy yield of the to support growth. Furthermore, aceto- microbial metabolism and metabolic diver- acetogenic reaction it is highly probably gens have a remarkable metabolic flexibil- sity can only be properly understood using that the acetogens will lose the competi- ity compared to methanogens and sulfate the kind of thermodynamic analyses on tion. Recent calculations confirm this: reducers, and can use more substrates or which Thauer and his colleagues based their assuming a “biological energy quantum” substrate combinations as energy source. review. Until this day I use this thermody- (the minimum amount of free energy Moreover, the fact that they use the energy- namic approach to explain the functioning change of a reaction that can drive the efficient reductive acetyl-CoA pathway (also of the microbial world in the basic and more formation of ATP) of −10 kJ, the ther- known as the Wood–Ljungdahl pathway) advanced microbiology courses I teach. modynamic threshold concentrations of both for autotrophic carbon fixation and At the same time Ralph Wolfe also intro- H2 calculated for chemolithoautotrophic for energy production makes their metabo- duced me to the world of the acetogens. I still sulfate reducers, methanogens, and aceto- lism highly efficient, enabling them to save remember how excited he was that the culture gens are ∼0.6, 11, and 410 nM, respectively precious energy for survival when stressed of Clostridium aceticum, isolated in the 1930s (Lever, 2011). These numbers clearly show (Lever, 2011). (Wieringa, 1936) but subsequently consid- that the “homoacetogenic” reaction from The title of this commentary – “There ered as lost, had been revived from a prepara- H2–CO2 is thermodynamically unfavora- must be an acetogen somewhere” para- tion of endospores of the original strain and ble. The advantage of the methanogens phrases Woese’s (1994) “There must be a thus became again available for study (Braun over the acetogens is also demonstrated prokaryote somewhere.” Nobody can have et al., 1981). The place of the acetogens in in the following calculation: at partial any doubt that prokaryotes play a central nature, and especially those species that live pressures for hydrogen and for methane function in nature, but the role of the aceto- as autotrophs on hydrogen as their energy of 10−4 and 0.5 atm, respectively, and bicar- gens was never really clear. Therefore Lever’s source, has always been enigmatic. The reason bonate, and acetate concentrations of 100 paper contributes much toward a proper becomes immediately obvious when calculat- and 10 mM, the Gibbs free energy is −40 kJ assessment of the place of this intriguing ing the thermodynamics of the process, com- per reaction for the formation of methane group of prokaryotes in anaerobic ecosys- paring the Gibbs free energy change under from bicarbonate and hydrogen, but only tems worldwide. standard conditions of three competing −13 kJ for the formation of acetate. Dolfing processes: sulfate reduction, methanogenesis, (1988) wrote: “A meaningful evaluation of REFERENCES and homoacetogenic metabolism: the energy conservation and the selection Braun, M., Mayer, F., and Gottschalk, G. (1981). Clostridium aceticum (Wieringa), a microorgan- mechanism that govern the outcome of 44HS++OH2−+→+HS− HO ism producing acetic acid from molecular hydro- 24 2 competition between methanogens and gen and carbon dioxide. Arch. Microbiol. 128, ′ ∆=Gko −152.2 J acetogens has to wait until more data are 188–293. www.frontiersin.org January 2012 | Volume 3 | Article 22 | 1 Oren Acetogens and anaerobic ecosystems Dolfing, J. (1988). “Acetogenesis,” in Environmental Thauer, R. K., Jungermann, K., and Decker, K. (1977). Citation: Oren A (2012) There must be an aceto- Microbiology of Anaerobes, ed. A. J. B. Zehnder (New Energy conservation in chemotrophic anaerobic bac- gen somewhere. Front. Microbiol. 3:22. doi: 10.3389/ York: John Wiley & Sons), 417–468. teria. Bacteriol. Rev. 41, 100–180. fmicb.2012.00022 Kristjansson, J. K., Schönheit, P., and Thauer, R. K. (1982). Wieringa, K. T. (1936). Over het verdwijnen van waterstof This article was submitted to Frontiers in Extreme Different Ks values for hydrogen of methanogenic en koolzuur onder anaerobe voorwaarden. Antonie Microbiology, a specialty of Frontiers in Microbiology. bacteria and sulfate reducing bacteria: an explana- van Leeuwenhoek 3, 263–273. Copyright © 2012 Oren. This is an open-access article tion for the apparent inhibition of methanogenesis Woese, C. R. (1994). There must be a prokaryote somewhere: distributed under the terms of the Creative Commons by sulfate. Arch. Microbiol. 131, 278–283. microbiology’s search for itself. Microbiol. Rev. 58, 1–9. Attribution Non Commercial License, which permits Lever, M. A. (2011). Acetogenesis in the energy-starved non-commercial use, distribution, and reproduction in deep biosphere – a paradox? Front. Microbiol. 2, 284. Received: 12 January 2012; accepted: 13 January 2012; other forums, provided the original authors and source doi: 10.3389/fmicb.2011.00284 published online: 31 January 2012. are credited. Frontiers in Microbiology | Extreme Microbiology January 2012 | Volume 3 | Article 22 | 2.