Systems analysis of bioenergetics and growth of the extreme halophile Halobacterium salinarum

Halobacterium salinarum is a bioenergetically flexible, halophilic
microorganism that can generate energy by respiration,
photosynthesis, and the fermentation of arginine. In a previous
study, using a genome-scale metabolic model, we have shown that the
archaeon unexpectedly degrades essential amino acids under aerobic
conditions, a behavior that can lead to the termination of growth
earlier than necessary. Here, we further integratively investigate
energy generation, nutrient utilization, and biomass production
using an extended methodology that accounts for dynamically
changing transport patterns, including those that arise from
interactions among the supplied metabolites. Moreover, we widen the
scope of our analysis to include phototrophic conditions to explore
the interplay between different bioenergetic modes. Surprisingly,
we found that cells also degrade essential amino acids even during
phototropy, when energy should already be abundant. We also found
that under both conditions considerable amounts of nutrients that
were taken up were neither incorporated into the biomass nor used
as respiratory substrates, implying the considerable production and
accumulation of several metabolites in the medium. Some of these
are likely the products of forms of overflow metabolism. In
addition, our results also show that arginine fermentation,
contrary to what is typically assumed, occurs simultaneously with
respiration and photosynthesis and can contribute energy in levels
that are comparable to the primary bioenergetic modes, if not more.
These findings portray a picture that the organism takes an
approach toward growth that favors the here and now, even at the
cost of longer-term concerns. We believe that the seemingly
"greedy" behavior exhibited actually consists of adaptations by the
organism to its natural environments, where nutrients are not only
irregularly available but may altogether be absent for extended
periods that may span several years. Such a setting probably
predisposed the cells to grow as much as possible when the
conditions become favorable.