Effects of alternative methyl group acceptors on the growth energetics of the O-demethylating anaerobe Holophaga foetida

Abstract

The anaerobic bacterium Holophaga foetida can metabolize the methyl groups of methoxylated aromatic compounds either to acetate or to dimethyl sulphide. The effects of this metabolic flexibility were investigated under conditions of excess substrate (batch culture) and substrate limitation (chemostat culture). Growth yield data suggest that transfer of the methyl groups to sulphide, in contrast to the homoacetogenic transfer to CO2, was not coupled to energy conservation. Under conditions of excess substrate, methyl groups were quantitatively transferred to sulphide. Growth yields decreased but growth rates increased upon the addition of sulphide during exponential growth in pH- and sulphide-regulated batch cultures. From the measured growth yields, the Gibbs free energy dissipation of catabolism plus anabolism (-∆G0'D) was calculated using stoichiometric equations incorporating biomass formation (macrochemical equations). The observed increase in growth rate correlated well with an increase in -∆G0'D, suggesting a relationship between growth kinetics and growth energetics. During steady-state growth in pH- and sulphide-regulated chemostat culture, a considerable fraction of the methyl groups was converted to acetate, despite the presence of sulphide. This resulted in similar growth yields and correspondingly similar -∆G0'D values in the presence and absence of sulphide. Apparently, H. foetida uncouples catabolism and anabolism in batch culture under conditions of excess substrate to a greater extent than in the chemostat under substrate limitation, by transferring the methyl groups quantitatively to sulphide and thereby dissipating the Gibbs free energy change of the methyl transfer. The physiological significance of these findings could be that H. foetida adjusts the energetics of its metabolism to the growth conditions (i) to maximize the growth rate if substrate is available in excess or, (ii) to maximize the growth yield if substrate is limiting.