Resource allocation to cell envelopes and the scaling of bacterial growth rate

Abstract

Although various empirical studies have reported a positive correlation between the specific growth rate and cell size across bacteria, it is currently unclear what causes this relationship. We conjecture that such scaling occurs because smaller cells have a larger surface-to-volume ratio and thus have to allocate a greater fraction of the total resources to the production of the cell envelope, leaving fewer resources for other biosynthetic processes. To test this theory, we developed a coarse-grained model of bacterial physiology composed of the proteome that converts nutrients into biomass, with the cell envelope acting as a resource sink. Assuming resources are partitioned to maximize the growth rate, the model yields expected scalings. Namely, the growth rate and ribosomal mass fraction scale negatively, while the mass fraction of envelope-producing enzymes scales positively with surface-to-volume. These relationships are compatible with growth measurements and quantitative proteomics data reported in the literature.

Evolutionary scaling of maximum growth rate with organism size

“…This being said, a different sort of physical-constraint argument may be relevant to the pattern in heterotrophic bacteria, e.g., increasing fractional volumetric requirements of nonscalable components such ribosomes, cell walls, membranes, and the nucleoid in very tiny cells 10 , 37 . Under this view, bacterial is assumed to be close to the maximum level of achievable perfection conditional upon these structural limitations, although the expected magnitude of growth-rate scaling has not been generated from first principles (but see Ref 50 ), and the pattern is not observed in phototrophs.…”

“…Any further increase in bacterial cell size might be advantageous in particular ecological contexts, but this would not be expected to further enhance maximum growth rates, regardless of the amount of ATP production. Smaller bacteria, with higher surface area:volume ratios and hence the potential for higher membrane-bioenergetic capacity, have reduced growth rates owing to the increased relative investment in the cell membrane itself 50 . Notably, strong selection for increased growth rate can yield a successful response in lab cultures of bacteria, but this seems always to be accompanied by an increase in cell volume and/or decrease in surface area:volume ratio [87][88][89] .…”

Metabolic scaling in small life forms

“…Such models may gain accuracy and improved resolution in size ranges by incorporating the more complicated metabolic scaling derived here. In addition, other cellular constraint perspectives have been proposed for explaining scaling in bacteria such as biosynthetic costs of the membrane [44], ribosome and protein abundances and costs [22, 45], the spatial location and number of organelles and genomes [16, 29], the increasing number of genes and their cost [16, 29, 45, 46], and transporter optimizations associated with the environment (e.g. [23] for a review).…”

An evolutionary optimum amid moderate heritability in prokaryotic cell size

“…There will be a minimal number of genes required for basic cellular functions, for example, which will dictate a certain minimal DNA mass, and hence a certain minimal volume occupied by DNA 60,61 . By contrast, bacterial membranes have largely invariant thickness and thus occupy an ever larger percentage of a cell’s total volume the smaller a cell is, constraining the relative space left for every other component, 62 . Just the consideration of membranes and DNA leads immediately to the existence of this limit.…”