Environmental Microbiology Reports (2015) 7(1), 31–32


Microbial life at the thermodynamic limit: how much energy is required to sustain life?

Volker Müller, Molecular Microbiology and Bioenergetics, Goethe University Frankfurt, Germany. We all know that Adenosine triphosphate (ATP) is the central energy currency of a living cell and we all know that it is the exclusive task of catabolism to provide cells with ATP and precursors for biosynthetic reaction. ATP can be synthesized by two mechanisms: by a direct coupling to an exergonic reaction (such as in glycolysis, for example pyruvate kinase) or by an indirect coupling. In the latter, an exergonic reaction is used to energize the cytoplasmic membrane by ion export (H+, Na+) and the electrochemical ion gradient then drives the synthesis of ATP via a membrane-bound ATP synthase. This is called the chemiosmotic mechanism of ATP synthesis. Very often, chemiosmosis is used synonymously with ‘aerobic respiration’, and we all know that aerobic respiration provided the energetic boost for evolution. However, respiration was evolved very early in life history and enabled first creatures to make a living from gaseous compounds or simple organic molecules (Mayer and Müller, 2014). Compare chemiosmosis to using a battery: it is charged by current and discharged by the consumer (the ATP synthase). In principle, the loading current can be indefinetely slow, it just takes longer to load the batterie so that it can finally be used to drive the consuming reaction. What does that mean for biological systems? The minimal energy required for ATP synthesis is not what it takes to make one ATP but that required to pump out one ion. Consider four ions to be pumped through the ATP synthase; the enzymatic reaction may proceed four times to pump out the four ions required for the synthesis of one ATP. In other words, the minimal energy required to make one ATP is only 25% compared with a direct coupling (Mayer and Müller, 2014). Mechanistically, a given membrane protein cannot pump less than one ion; half an ion is hard to make and even harder to pump! Therefore, the minimum biological energy quantum was regarded to be around −20 kJ mol−1 (Schink, 1997), the amount of energy required to pump one ion at an electrochemical membrane potential of around −200 mV. Recently, this was challenged with the discovery of a lifestyle that was exluded before to be able to sustain the life of a pure culture, the oxidation of formate to hydrogen and carbon © 2015 Society for Applied Microbiology and John Wiley & Sons Ltd

dioxide which is endergonic at room temperature and only slightly exergonic at 80°C, the optimum temperature of the Thermococcus strain that lives from this reaction (Kim et al., 2010; Lim et al., 2014). This reaction would only allow for the net transport of a fraction of an ion! But how can this be achieved? Six years after my last crystal ball article, the enyzmes used by these anaerobes to couple exergonic membrane reactions to the generation of a transmembrane ion gradient have been identified: membrane-bound ferredoxin:H+ oxidoreductases (hydrogenases) (Schut et al., 2013) and ferredoxin:NADH oxidoreductases (Rnf complex) (Biegel and Müller, 2010; Biegel et al., 2011). We still don’t know how these enzymes function on a molecular level and how they couple the enzymatic reaction to the export of ions into the periplasm. The first hurdle is to get these membrane protein complexes purified, and molecular methods to overproduce these heterologously must be established. The choice of the host will be the key to success: The enterobacterium Escherichia coli is easy to work with but for many of our interesting proteins, E. coli is too stupid to deal with, cannot handle them and does not know how to insert the metal centres often encountered in these proteins. But I do see diffuse homologous expression systems at the bottom of the crystal ball. Analysis of these proteins will bring many surprises. For me, the most important is: How can they pump out ions with less than 20 kJ mol−1 available? Maybe by an energetic coupling two or more ion-translocating modules in one protein. For example, the membrane-bound hydrogenase gene cluster of Thermoccoccus and Pyrococcus both have genes encoding Na+/H+ antiporter (Schut et al., 2013; Lim et al., 2014). In theory, it would be possible to export one ion by the hydrogenase module and if the Na+/H+ antiporter is electrogenic with a Na+:H+ stoichiometry > 1, the overall ion stoichiometry would be < 1. Most exciting, by varying the stoichiometry of the Na+/H+ antiporter, any net stoichiometry of < 1 ion pumped per mole of substrate oxidized can be achieved, even close to zero, or, as in the case of anaerobic formate oxidation, even around zero. Having said this brings me to another fascinating point. If a reaction proceeds close to equlibrium and if it is possible to make ATP from that, can we reverse the reaction and


Crystal ball

also make ATP from it? Examples are the ‘reverse’ types of metabolism such as reverse methanogenesis or acetogenesis. Truly fascinating examples in which microbes can make a living from by a reaction running from A to B but also the same way backwards from B to A. Consider this for human beings: breakfast in Bavaria, bavarian beer and sausage is slowly oxidized to carbon dioxide, and, if we could turn it around, carbon dioxide transformed to beer and sausage, and we could live from both it, what a wonderfull imagination. Anyway, we will see in the future how these novel ‘respiratory’ enzymes in anaerobic microbes work, and this will certainly be an enlightning for biochemists, bioenergeticists and also ecophysiologists.

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

Biegel, E., Schmidt, S., Gonzalez, J.M., and Müller, V. (2011) Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes. Cell Mol Life Sci 68: 613–634. Kim, Y.E., Lee, H.S., Kim, E.S., Bae, S.S., Lim, J.K., Matsumi, R., et al. (2010) Formate-driven growth coupled with H2 production. Nature 467: 352–355. Lim, J.K., Mayer, F., Kang, S.G., and Müller, V. (2014) Energy conservation by oxidation of formate to carbon dioxide and hydrogen via sodium ion current in a hyperthermophilic archaeon. Proc Natl Acad Sci USA 111: 11497–11502. doi:10.1073/pnas.1407056111. Mayer, F., and Müller, V. (2014) Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiol Rev 38: 449–472. Schink, B. (1997) Energetics of synthrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61: 262–280. Schut, G.J., Boyd, E.S., Peters, J.W., and Adams, M.W. (2013) The modular respiratory complexes involved in hydrogen and sulfur metabolism by heterotrophic hyperthermophilic archaea and their evolutionary implications. FEMS Microbiol Rev 37: 182–203.

© 2015 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 7, 31–32

Microbial life at the thermodynamic limit: how much energy is required to sustain life?

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