Testing the Growth Rate and Temperature Compensation Hypotheses in Marine Bacterioplankton

Abstract

Two different hypotheses have been raised as to how temperature affects resource allocation in microorganisms. The translation-compensation hypothesis (TCH) predicts that the increase in enzymatic efficiency with temperature results in fewer required ribosomes per cell and lower RNA:protein ratio. In contrast, the growth rate hypothesis (GRH) predicts that increasing growth rate with temperature requires more ribosomes and hence a higher cellular RNA:protein. We tested these two hypotheses in lab cultures of Prochlorococcus and Alteromonas as well as over an annual cycle in the Eastern Mediterranean Sea. The RNA:protein of Alteromonas mostly decreased with temperature in accordance with the TCH, while that of Prochlorococcus increased with temperature, as predicted by the GRH. No support was found for either hypotheses in surface waters from the Eastern Mediterranean, whereas the fraction of phosphorus in RNA was positively correlated with per-cell bacterial production in the deep chlorophyll maximum, supporting the GRH in this niche. A considerable part of the cellular phosphorus was not allocated to RNA, DNA, phospholipids or polyphosphate, raising the question which cellular molecules contain these P reserves. While macromolecular quotas differed significantly between laboratory cultures and field samples, these were connected through a power law, suggesting common rules of resource allocation. Originality-Significance statementWe investigated whether the translation-compensation hypothesis (TCH) or growth rate hypothesis (GRH) affect the macromolecular composition and phosphorus allocation in both lab cultures of Prochlorococcus and Alteromonas as well as in seawater with natural microbial communities. Our results highlight that the TCH and GRH may each be applicable to different organisms (autotroph or heterotroph), physiological states or environmental conditions. Testing the applicability of theoretical models such as the TCH and GRH in lab cultures and field samples is an important step toward mechanistic models of bacterial physiology. This is especially important to our understanding of how bacterioplankton allocate resources in response to changes in environmental conditions such as temperature and nutrient stress, which are likely to expand due to the predicted global changes.