# Resource acquisition in diel cycles and the cost of growing quickly

## TL;DR

Microalgae must balance carbon fixation during the day with growth needs at night, and faster-growing species face trade-offs that limit their geographic range.

## Contribution

A new model explains how microalgae optimize carbon fixation and growth by adjusting metabolite pool sizes and resource acquisition rates.

## Key findings

- Faster-growing microalgae require higher carbon fixation rates and larger metabolite pools to sustain growth.
- The optimal metabolite pool size scales with the ratio of light duration to doubling time.
- This trade-off limits fast-growing species to regions with long daylight periods.

## Abstract

Many organisms, notably phototrophs, routinely acquire resources over only a fraction of the day. They have to balance their main period of initial biosynthesis against cell cycle events. Because of their short generation times, this challenge is especially acute for the planktonic microalgae that perform 50% of global C-fixation. Empirical evidence indicates that microalgal day-average growth is a function of the ability to acquire resources rapidly when available, retaining initial products of assimilation to support growth. A fundamental question arises over the optimal physiological configuration to support such activity. Here, we applied computer simulations implementing a development of the quota concept, in which the internal limiting resource is itself C, ratioed against total organism C-biomass. The model comprises metabolite and core pools of carbon C (MC and CC, respectively), with growth modulated by MC/(MC + CC); MC supports growth of CC in the absence of concurrent resource acquisition. Dynamic feedback interactions from the relative size of MC controls resource acquisition. The model reproduces the general pattern of growth at different light:day fraction (LD), and of afternoon-depression of C-fixation. We explored the efficiency of the physiological cell configuration to locate optimal configurations at different combinations of maximum growth rates (Umax) and LD values across plausible parameter values for microalgae. While the optimum maximum resource acquisition rate deployed during the L phase scales with Umax/LD, the maximum size of the metabolite pool scales to LD/DV, where DV is division time (i.e. Umax/Ln(2)). Accordingly, we conclude that faster growing organisms carry a penalty limiting their geographic spread to latitudes and seasons where LD is high. Larger, vacuolated organisms (such as diatoms), having a bigger metabolite compartment, may be at an advantage in such situations.

Planktonic microalgae that support 50% of global primary productivity have a problem: for half of their growing lives, during night time, they cannot fix C. We explored how they may optimise C-fixation during the illuminated fraction of the day (LD) to support biosynthesis over the whole day. We constructed a model describing a metabolite pool, into which the initial results from C-fixation accumulate, and a core structural pool. Consistent with how real organisms function, the relative size of the metabolite pool modulates, or controls, not only the synthesis (growth) of the core structure, but also modulates C-fixation; both modulations used sigmoidal functions in line with allosteric biochemical controls. We found that, while the C-fixation rate required to support a given growth rate potential (Umax) increases broadly linearly with 1/LD, the relationship with the maximum size of the metabolite pool relative to the whole organism biomass (Mmax) relates to the ratio of LD to the organism’s doubling time. Faster growing organisms thus need not only a higher resource acquisition rate (C-fixation) for a given combination of LD and Umax, but also a larger Mmax. We suggest this limits the competitiveness of faster growing organisms to lower latitudes and/or longer day-light periods.