In search of a thermodynamic description of biomass yields for the chemotrophic growth of microorganisms

Abstract

Correlations for the prediction of biomass yields are valuable, and many proposals based on a number of parameters (Y(ATP), Y(Ave), eta(o), Y(c), Gibbs energy efficiencies, and enthalpy efficiencies) have been published. This article critically examines the properties of the proposed parameters with respect to the general applicability to chemotrophic growth systems, a clear relation to the Second Law of Thermodynamics, the absence of intrinsic problems, and a requirement of only black box information. It appears that none of the proposed parameters satisfies all these requirements. Particularly, the various energetic efficiency parameters suffer from major intrinsic problems. However, this article will show that the Gibbs energy dissipation per amount of produced biomass (kJ/C-mod) is a parameter which satisfies the requirements without having intrinsic problems. A simple correlation is found which provides the Gibbs energy dissipation/C-mol biomass as a function of the nature of the C-source (expressed as the carbon chain length and the degree of reduction). This dissipation appears to be nearly independent of the nature of the electron acceptor (e.g., O(2), No(3) (-), fermentation). Hence, a single correlation can describe a very wide range of microbial growth systems. In this respect, Gibbs energy dissipation is much more useful than heat production/C-mol biomass, which is strongly dependent on the electron acceptor used. Evidence is presented that even a net heat-uptake can occur in certain growth systems.The correlation of Gibbs energy dissipation thus obtained shows that dissipation/C-mol biomass increases for C-sources with smaller chain length (C(6) --> C(1)), and increases for both higher and lower degrees of reduction than 4. It appears that the dissipation/C-mol biomass can be regarded as a simple thermodynamic measure of the amount of biochemical "work" required to convert the carbon source into biomass by the proper irreversible carbon-carbon coupling and oxidation/reduction reactions. This is supported by the good correlation between the theoretical ATP requirement for biomass formation on different C-sources and the dissipation values (kJ/C-mol biomass) found. The established correlation for the Gibbs energy dissipation allows the prediction of the chemotrophic biomass yield on substrate with an error of 13% in the yield range 0.01 to 0.80 C-mol biomass/(C)-mol substrate for aerobic/anaerobic/denitrifying growth systems.

Biothermodynamics of live cells: a tool for biotechnology and biochemical engineering

“…In reality, hundreds of different constituent components of biomass are derived from different points along the catabolic series of reactions. Hence, trying to use a real formulation of anabolism is unpractical due to the complexity of its details, which are often unknown [47]. Rather, a formal though somewhat unrealistic split such as the one in Figure 10 may be assumed.…”

“…As shown in Figure 19b the bioenergetic efficiencies of aerobic and anaerobic growth taken together vary in an unpredictable way from above 60% down to close to 0%. Moreover, Heijnen and van Dijken already pointed out in 1992, [47] and 1993, [63] that the concept of thermodynamic efficiency is plagued with serious internal inconsistencies. Their values indeed depend on exactly how the biosynthetic reaction is formulated.…”

Impact of Thermodynamic Principles in Systems Biology

“…Herewith, all yields are also available (yield is ratio of rates). Heijnen and Van Dijken [9] and Heijnen [10] apply this approach to any heterotrophic growth system under substrate limited condition. The only information needed is the nature of carbon source, electron donor, electron acceptor, N-source and temperature.…”

“…This amount has been found to depend only on two factors [9,10]: first, the nature of the carbon source for heterotrophic growth and, second, the nature of electron donor for autotrophic growth.…”

“…With these known rates all yields are known such as the biomass yield Y SX ¼ m q s or yield of catabolic products. This thermodynamic approach has been shown to predict biomass yield with 10-15% error for a wide variety (aerobic/anaerobic/hetero/autotrophic) of microbial systems where Y SX spans a range of near two orders of magnitude [9].…”