The maximum growth rate hypothesis is correct for eukaryotic photosynthetic organisms, but not cyanobacteria

Abstract

Summary The (maximum) growth rate (µmax) hypothesis predicts that cellular and tissue phosphorus (P) concentrations should increase with increasing growth rate, and RNA should also increase as most of the P is required to make ribosomes. Using published data, we show that though there is a strong positive relationship between the µmax of all photosynthetic organisms and their P content (% dry weight), leading to a relatively constant P productivity, the relationship with RNA content is more complex. In eukaryotes there is a strong positive relationship between µmax and RNA content expressed as % dry weight, and RNA constitutes a relatively constant 25% of total P. In prokaryotes the rRNA operon copy number is the important determinant of the amount of RNA present in the cell. The amount of phospholipid expressed as % dry weight increases with increasing µmax in microalgae. The relative proportions of each of the five major P‐containing constituents is remarkably constant, except that the proportion of RNA is greater and phospholipids smaller in prokaryotic than eukaryotic photosynthetic organisms. The effect of temperature differences between studies was minor. The evidence for and against P‐containing constituents other than RNA being involved with ribosome synthesis and functioning is discussed.

Testing the Growth Rate and Temperature Compensation Hypotheses in Marine Bacterioplankton

“…Overall, per-cell quotas of protein and RNA were all highest for A. macleodii HOT1A3, followed by A. mediterranea DE, Prochlorococcus NATL2A, and finally Prochlorococcus MIT9312 (Fig 1C and 1D). The larger, copiotrophic Alteromonas is expected to have higher cell quotas of macromolecules compared to Prochlorococcus which is often associated with oligotrophic environments, due to their size and a larger number of ribosomal RNA operons (5 in Alteromonas compared to 1-2 in Prochlorococcus ) (Rocap et al ., 2002; Schirrmeister et al ., 2012; López-Pérez et al ., 2013; Rees and Raven, 2021). Yet, the per-cell protein quotas of A. macleodii HOT1A3 (∼200-500fg/cell) were considerably higher than those of A. mediterranea DE (50-200fg/cell).…”

“…Therefore, we measured polyphosphates, while P-DNA was estimated based on the genome size of each bacterium and P-phospholipids was estimated from the total lipids in the cell membrane (Waldbauer et al ., 2012) (Fig 2B). The calculated fractions of P in DNA (8-13%) and phospholipids (3-12%) were in the same range as reported for heterotrophic bacteria and cyanobacteria (see Table S2 and (Rhee, 1973; Cotner et al ., 2006; Rees and Raven, 2021). In contrast, the fraction of P in polyphosphates was only 1-15% in both Alteromonas and Prochlorococcus (Fig 2B, Fig S6B), lower than previously suggested in cyanobacteria (29±9%, (Rees and Raven, 2021) and Table S2).…”

“…Further studies, potentially using chemostats to better control growth rate and detailed analyses of the rates of protein production and degradation, are needed in order to dissect the effect of these contrasting mechanisms. It is also possible that the GRH is best formulated in terms of maximal rather than actual (instantaneous) growth rate, and that molecular-genomic aspects such as the number of rRNA operons are also important (Rees and Raven, 2021).…”

“…It has been suggested that cellular P is associated mainly with RNA molecules, and to a lesser extent DNA, phospholipids and “P-esters” (e.g. phosphorylated proteins and metabolites) (Sterner and Elser, 2002; Rees and Raven, 2021). However, there are other pools of P not associated with these specific macromolecules, for example polyphosphate stores, which are often associated with ‘luxury uptake’ in response to nutrient pulses under P-limited conditions (Kulaev et al, 2005).…”

Protoplasmic streaming of chloroplasts enables rapid photoacclimation in large diatoms

“…Large diatoms are able to accumulate the nutrients with the periodic intensification of vertical exchange and consume them in a stable environment with a low nutrient concentration. These species are storage machineries, with nitrogen-to-phosphorus ratios in the cell significantly higher than the Redfield ratio (Klausmeier et al, 2004), low growth rates (consistent with the growth rate hypothesis; Rees and Raven, 2021). Mathematical modeling of population dynamics, suggests that these species can become dominant in conditions with a periodic regime of providing of the nutrients (Stolte and Riegman, 1996;Litchman et al, 2009;Abakumov et al, 2011).…”