Abstract
Availability of usable energy for biosynthesis and maintenance is a primary condition of life. In the case of microbial degradation of so-called recalcitrant compounds, growth is often prevented due to low energy production rates not exceeding maintenance requirements. However, any process that reduces biomass maintenance under these threshold conditions will increase the chance that productive degradation can occur. We have developed a growth model to explain the surprising observation that the growth of Aquincola tertiaricarbonis L108 and other bacterial strains on the groundwater pollutant methyl tert-butyl ether (MTBE) and its degradation product tert-butyl alcohol is accompanied by the accumulation of poly-3-hydroxybutyrate (PHB). The growth-coupled production of this storage polymer is remarkable since slow growth of all MTBE degraders indicates the difficulty to utilize this substrate. The modified model distinguished an active biomass fraction for which maintenance energy is required and a passive PHB fraction without maintenance requirements. Consequently, the presence of a PHB fraction saved specific maintenance costs and due to PHB accumulation, calculated overall growth yields were increased. More important, the structured model predicted an increased specific growth rate and a decreased minimum substrate concentration for growth Smin. Using experimentally determined parameters, it could be demonstrated that at low maximal growth rates PHB synthesis allowed for growth, whereas in its absence Smin became infinite. Additional reduction of maintenance in dependence on the rate of PHB formation was considered as the stoichiometry of PHB synthesis from MTBE resulted in a gain of energy equivalents. Our model thus showed that coupling of growth on slowly metabolized substrates with PHB synthesis is energetically advantageous. Hence, we propose a not yet considered role of PHB in delivering energy to compensate high maintenance costs while growing on recalcitrant xenobiotics.
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