Abstract
Bacteria must balance the different needs for substrate assimilation, growth functions, and resilience in order to thrive in their environment. Of all cellular macromolecules, the bacterial proteome is by far the most important resource and its size is limited. Here, we investigated how the highly versatile 'knallgas' bacterium Cupriavidus necator reallocates protein resources when grown on different limiting substrates and with different growth rates. We determined protein quantity by mass spectrometry and estimated enzyme utilization by resource balance analysis modeling. We found that C. necator invests a large fraction of its proteome in functions that are hardly utilized. Of the enzymes that are utilized, many are present in excess abundance. One prominent example is the strong expression of CBB cycle genes such as Rubisco during growth on fructose. Modeling and mutant competition experiments suggest that CO2-reassimilation through Rubisco does not provide a fitness benefit for heterotrophic growth, but is rather an investment in readiness for autotrophy.
Highlights
Cupriavidus necator is a model aerobic lithoautotroph and formatotroph, and is notable for production of the storage polymer polyhydroxybutyrate (PHB) [Yishai et al, 2016, Brigham, 2019]
We found that C. necator allocates its resources in response to the imposed environmental challenges, but invests more than 40% of its protein mass in genes that are either unlikely to be utilized or have no known function
C. necator expresses most of its annotated genes
Summary
Cupriavidus necator (formerly Ralstonia eutropha) is a model aerobic lithoautotroph and formatotroph, and is notable for production of the storage polymer polyhydroxybutyrate (PHB) [Yishai et al, 2016, Brigham, 2019]. Cupriavidus necator H16 (hereafter abbreviated C. necator) is a soil-dwelling bacterium with a large genome (~6,600 genes) distributed on two chromosomes and one megaplasmid [Pohlmann et al, 2006] It features a wide arsenal of metabolic pathways for xenobiotics degradation, hydrogen and formate oxidation, carbon fixation via the Calvin-Benson-Bassham (CBB) cycle, and utilization of nitrate/nitrite as alternative electron acceptors (de-nitrification) [Cramm, 2008]. The metabolic versatility of C. necator is interesting from a biotechnological point of view, this benefit could come at a considerable cost for the cell It is not known if the expression of the various substrate assimilation pathways is efficiently regulated under different conditions, and if gene expression is optimal to maximize growth or rather another trait such as environmental readiness. There, a large investment in the CO2-fixation (2-7% protein mass is Rubisco) and photosynthesis machinery (20-40% protein mass are antennae and photosystems) may reduce proteome space for ribosomes, resulting in lower growth rates than heterotrophs
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