A re-assessment of bacterial growth efficiency: the heat production and membrane potential of Streptococcus bovis in batch and continuous culture

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Abstract
Glucose-limited, continuous cultures (dilution rate 0.1 h-1) of Streptococcus bovis JB1 fermented glucose at a rate of 3.9 μmol mg protein-1 h-1 and produced acctate, formate and ethanol. Based on a maximum ATP yield of 32 cells/mol ATP (Stouthamer 1973) and 3 ATP/glucose, the theoretical glucose consumption for growth would have been 2.1 μmol mg protein-1 h-1. Because the maintenance energy requirement was 1.7 μmol/mg protein/h (Russell and Baldwin 1979), virtually all of the glucose consumption could be explained by growth and maintenance and the YATP was 30. Glucose-limited, continuous cultures produced heat at a rate of 0.29 mW/mg protein, and this value was similar to the enthalpy change of the fermentation (0.32 mW/mg protein). Batch cultures (specific growth rate 2.0 h-1) fermented glucose at a rate of 81 μmol mg protein-1 h-1, and produced only lactate. The heat production was in close agreement with the theoretical enthalpy change (1.72 versus 1.70 mW/mg protein), but only 80% of the glucose consumption could be accounted by growth and maintenance. The YATP of the batch cultures was 25. Nitrogen-limited, glucose-excess, non-growing cultures fermented glucose at a rate of 6.9 μmol mg protein-1 h-1, and virtually all of the enthalpy for this homolactic fermentation could be accounted as heat (0.17 mW/mg protein). The nitrogenlimited cultures had a membrane potential of 150 mV, and nearly all of the heat production could be explained by a futile cycle of protons through the cell membrane (watts = amperes x voltage where H+/ATP was 3). The membrane voltage of the nitrogen-limited cells was higher than the glucose-limited continuous cultures (150 versus 80 mV), and this difference in voltage explained why nitrogen-limited cultures consumed glucose faster than the maintenance rate. Batch cultures had a membrane potential of 100 mV, and this voltage could not account for increased glucose consumption (more than growth plus maintenance). It appears that another mechanism causes the increased heat production and lower growth efficiency of batch cultures.