Systems Analysis of Bioenergetics and Growth of the Extreme Halophile Halobacterium salinarum

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Abstract
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. Living cells can produce usable energy through various means. For example, animals derive energy, through respiration, from nutrients that they consume, and plants from light using photosynthesis. The particular microorganism that we study, Halobacterium salinarum, is a model organism for the archaeal domain of life. It is bioenergetically flexible in that it can perform both respiration and photosynthesis and in addition can also derive energy using fermentation. Accordingly, it is a good model system for investigating the interplay between different energy generating mechanisms. In this study, we investigate these relationships as well as how energy production is linked to the other processes involved in growth, including the consumption of nutrients and the production of cellular material. Because Halobacterium salinarum thrives in salt-saturated solutions, such as those that may be found in salt lakes and solar salterns, our study yields insight on how these cellular processes operate in environments that are lethal to most life on Earth.

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