Independent colimitation for carbon dioxide and inorganic phosphorus.

Elly Spijkerman,Ursula Gaedke,Francisco De Castro,Zoe Finkel

doi:10.1371/journal.pone.0028219

Abstract

Simultaneous limitation of plant growth by two or more nutrients is increasingly acknowledged as a common phenomenon in nature, but its cellular mechanisms are far from understood. We investigated the uptake kinetics of CO2 and phosphorus of the algae Chlamydomonas acidophila in response to growth at limiting conditions of CO2 and phosphorus. In addition, we fitted the data to four different Monod-type models: one assuming Liebigs Law of the minimum, one assuming that the affinity for the uptake of one nutrient is not influenced by the supply of the other (independent colimitation) and two where the uptake affinity for one nutrient depends on the supply of the other (dependent colimitation). In addition we asked whether the physiological response under colimitation differs from that under single nutrient limitation.We found no negative correlation between the affinities for uptake of the two nutrients, thereby rejecting a dependent colimitation. Kinetic data were supported by a better model fit assuming independent uptake of colimiting nutrients than when assuming Liebigs Law of the minimum or a dependent colimitation. Results show that cell nutrient homeostasis regulated nutrient acquisition which resulted in a trade-off in the maximum uptake rates of CO2 and phosphorus, possibly driven by space limitation on the cell membrane for porters for the different nutrients. Hence, the response to colimitation deviated from that to a single nutrient limitation. In conclusion, responses to single nutrient limitation cannot be extrapolated to situations where multiple nutrients are limiting, which calls for colimitation experiments and models to properly predict growth responses to a changing natural environment. These deviations from single nutrient limitation response under colimiting conditions and independent colimitation may also hold for other nutrients in algae and in higher plants.

Highlights

Plant biomass forms the basis of food webs and its primary production promotes global economic and ecosystem services such as crop harvest, fish yield and carbon sequestration
CO2 and P uptake kinetics differed in the high and low CO2 acclimated algae (Fig. 2), e.g. Vmax,C was higher in the low CO2 acclimated cultures than in the high CO2 ones, when the effect of growth rate was accounted for (Fig. 2A; ANCOVA, F1,27 = 27.0, p,0.001)
This kinetic difference resulted from the lower cellular C content (Fig. S2A) in the low CO2 than in the high CO2 cells at a given steady state growth rate

Summary

Introduction

Plant biomass forms the basis of food webs and its primary production promotes global economic and ecosystem services such as crop harvest, fish yield and carbon sequestration. Massive plant growth such as large scale algal blooms, arising from an excess of nutrients, negatively affect biodiversity and are a nuisance to human activity This excessive plant growth often results from plants acclimated to scavenge the limiting nutrient but which are suddenly faced with saturating conditions often due to antropogenic impacts. A colimitation by nitrogen, P and iron was shown in the phytoplankton communities of Lake Kasumigaura [4] and Lake Erie [2] As illustrated in these two studies, nutrient supplementation alleviates each incremental limitation and produces a synergistic effect when all limiting nutrients are added together (see [5] for a nice illustration). A single species can show the effects of colimitation [6,7]

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