John Beardall

Approaches for determining phytoplankton nutrient limitation

Abstract: Aquatic primary productivity is frequently limited by the availability of nutrients. The ability to identify factors limiting algal growth is of considerable importance to our understanding of the ecology of aquatic plants and to water management practices. Methods used to identify limiting resources in the past have included a) analysis of nutrient availability, b) elemental composition and cell quotas for various nutrients, c) bio-assays monitoring growth of test species or of natural populations following nutrient enrichment and d) measurements of various physiological parameters, such as enhancement of respiration and dark carbon fixation rates and perturbation of photosynthetic rate following re-supply of nutrients.¶In this paper we briefly review the merits and methodological limitations of these approaches for the assessment of the nutrient status of algal populations. We discuss how an understanding of biochemical and metabolic changes induced by nutrient limitation has led to the development of rapid and simple tools to monitor the nutrient status of aquatic plants and algae. In particular, we describe the use of transient changes in chlorophyll a fluorescence as a potential tool for rapid assessment of algal nutrient status and the development of molecular probes specific to nutrient limited cells, such as flavodoxin as a diagnostic tool for Fe-limitation.

The potential effects of global climate change on microalgal photosynthesis, growth and ecology

Abstract The global environment is currently experiencing a period of significant change in climate as a result of human activities. Although the planet has experienced very significant variations in climate in the geological past, the rate at which the present changes are occurring is extraordinary. Anthropogenic influences have resulted in an enhancement of atmospheric carbon dioxide levels which will amount to a two- to threefold increase over the next century and this has already led to a measurable rise in global temperature. At the same time, chlorofluorocarbons are reacting with ozone in the stratosphere, a process that has led to appreciable enhancement of UV-B radiation (UVBR) fluxes to the earths surface at high latitudes. This review addresses our present state of knowledge about the effects of enhanced carbon dioxide levels, elevated UVBR fluxes and higher temperatures on the ecophysiology of microalgae. We consider the potential interactions between these and other environmental factors, such as nutrient availability, and also address the ecological consequences of climate change for microalgal assemblages and the flow of materials to higher trophic levels.

What is conservation physiology? Perspectives on an increasingly integrated and essential science †

The definition of ‘conservation physiology’ is refined to be more inclusive, with an emphasis on characterizing diversity, understanding and predicting responses to environmental change and stressors, and generating solutions. The integrative discipline is focused on mechanisms and uses physiological tools, concepts, and knowledge to advance conservation and resource management.

FOURIER TRANSFORM INFRARED SPECTROSCOPY AS A NOVEL TOOL TO INVESTIGATE CHANGES IN INTRACELLULAR MACROMOLECULAR POOLS IN THE MARINE MICROALGA CHAETOCEROS MUELLERII (BACILLARIOPHYCEAE)

Fourier Transform Infrared (FT‐IR) spectroscopy was used to study carbon allocation patterns in response to changes in nitrogen availability in the diatom Chaetoceros muellerii Lemmerman. The results of the FT‐IR measurements were compared with those obtained with traditional chemical methods. The data obtained with both FT‐IR and chemical methods showed that nitrogen starvation led to the disappearance of the differences in cell constituents and growth rates existing between cells cultured at either high [NO3−] or high [NH4+]. Irrespective of the nitrogen source supplied before nitrogen starvation, a diversion of carbon away from protein, chlorophyll, and carbohydrates into lipids was observed. Under these conditions, cells that had previously received nitrogen as nitrate appeared to allocate a larger amount of mobilized carbon into lipids than cells that had been cultured in the presence of ammonia. All these changes were reversed by resupplying the cultures with nitrogen. The rate of protein accumulation in the N‐replete cells was slower than the rate of decrease under nitrogen starvation. This study demonstrates that the relative proportions of the major macromolecules contained in microalgal cells and their changes in response to external stimuli can be determined rapidly, simultaneously, and inexpensively using FT‐IR. The technique proved to be equally reliable to and less labor intensive than more traditional chemical methods.

Fourier Transform Infrared microspectroscopy and chemometrics as a tool for the discrimination of cyanobacterial strains

Abstract Fourier Transform Infrared (FTIR) microspectroscopy, in combination with chemometrics, was investigated as a novel method to discriminate between cyanobacterial strains. In total, 810 absorbance spectra were recorded from one eukaryotic and five cyanobacterial taxa spanning three genera and including two strains of one species, Microcystis aeruginosa . Principal Component Analysis (PCA) based classification techniques such as Soft Independent Modelling of Class Analogy (SIMCA) and K-Nearest Neighbours (KNN) were investigated. Different spectral regions using derivative spectra were investigated to find the best combinations for classification. The highest rate of correct classifications (99–100%) was achieved using first derivative spectra with a spectral region of 1800–950 cm −1 for both the SIMCA and KNN. A dendrogram constructed using averaged spectra of the six taxa studied showed that the two strains of Microcystis aeruginosa exhibited the highest degree of similarity, while the eukaryotic taxon was the most dissimilar from the prokaryotic taxa.

Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles

Oxygenic photosynthesis evolved at least 2.4 Ga; all oxygenic organisms use the ribulose bisphosphate carboxylase-oxygenase (Rubisco)–photosynthetic carbon reduction cycle (PCRC) rather than one of the five other known pathways of autotrophic CO2 assimilation. The high CO2 and (initially) O2-free conditions permitted the use of a Rubisco with a high maximum specific reaction rate. As CO2 decreased and O2 increased, Rubisco oxygenase activity increased and 2-phosphoglycolate was produced, with the evolution of pathways recycling this inhibitory product to sugar phosphates. Changed atmospheric composition also selected for Rubiscos with higher CO2 affinity and CO2/O2 selectivity correlated with decreased CO2-saturated catalytic capacity and/or for CO2-concentrating mechanisms (CCMs). These changes increase the energy, nitrogen, phosphorus, iron, zinc and manganese cost of producing and operating Rubisco–PCRC, while biosphere oxygenation decreased the availability of nitrogen, phosphorus and iron. The majority of algae today have CCMs; the timing of their origins is unclear. If CCMs evolved in a low-CO2 episode followed by one or more lengthy high-CO2 episodes, CCM retention could involve a combination of environmental factors known to favour CCM retention in extant organisms that also occur in a warmer high-CO2 ocean. More investigations, including studies of genetic adaptation, are needed.

Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change.

Carbon dioxide concentrating mechanisms (also known as inorganic carbon concentrating mechanisms; both abbreviated as CCMs) presumably evolved under conditions of low CO2 availability. However, the timing of their origin is unclear since there are no sound estimates from molecular clocks, and even if there were, there are no proxies for the functioning of CCMs. Accordingly, we cannot use previous episodes of high CO2 (e.g. the Palaeocene–Eocene Thermal Maximum) to indicate how organisms with CCMs responded. Present and predicted environmental change in terms of increased CO2 and temperature are leading to increased CO2 and HCO3− and decreased CO32− and pH in surface seawater, as well as decreasing the depth of the upper mixed layer and increasing the degree of isolation of this layer with respect to nutrient flux from deeper waters. The outcome of these forcing factors is to increase the availability of inorganic carbon, photosynthetic active radiation (PAR) and ultraviolet B radiation (UVB) to aquatic photolithotrophs and to decrease the supply of the nutrients (combined) nitrogen and phosphorus and of any non-aeolian iron. The influence of these variations on CCM expression has been examined to varying degrees as acclimation by extant organisms. Increased PAR increases CCM expression in terms of CO2 affinity, whilst increased UVB has a range of effects in the organisms examined; little relevant information is available on increased temperature. Decreased combined nitrogen supply generally increases CO2 affinity, decreased iron availability increases CO2 affinity, and decreased phosphorus supply has varying effects on the organisms examined. There are few data sets showing interactions amongst the observed changes, and even less information on genetic (adaptation) changes in response to the forcing factors. In freshwaters, changes in phytoplankton species composition may alter with environmental change with consequences for frequency of species with or without CCMs. The information available permits less predictive power as to the effect of the forcing factors on CCM expression than for their overall effects on growth. CCMs are currently not part of models as to how global environmental change has altered, and is likely to further alter, algal and aquatic plant primary productivity.

Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation

The capacity of algae to express CO2 concentrating mechanisms (CCMs) is regulated by environmental factors. Some of these factors, especially photon flux, can influence the instantaneous activity of a CCM without necessarily affecting gene expression or the capacity of the cell to transport inorganic carbon. Other environmental parameters, especially those causing changes in the availability of CO2 dissolved in the surrounding medium, act at a transcriptional level. In this review, the complex interactions between environmental factors in controlling CCM activity will be discussed, as will the ecological consequences of CCMs as they relate to the growth and ecological performance of algal cells in nature. We also consider the consequences of global climate change for the performance of algae with and without CCMs.

Put out the light, and then put out the light

The lowest photon flux density of photosynthetically active radiation at which O 2 -evolving marine photolithotrophs appear to be able to grow is some 10 nmol photon m −2  s −1 , while marine non-O 2 -evolvers can grow at 4 nmol photon m −2  s −1 , in both cases with the photon flux density averaged over the 24 hour L:D cycle. Constraints on the ability to grow at very low fluxes of photosynthetically active radiation fall into three categories. Category one includes essential processes whose efficiency is independent of the rate of energy input, but whose catalysts show phylogenetic variation leading to different energy costs for a given process in different taxa, e.g. light-harvesting complexes, RUBISCO and probably in the sensitivity of PsII to photodamage. The second category comprises essential processes whose efficiency decreases with decreasing energy input rate as a result of back-reactions independent of the energy input rate, e.g. charge recombination following charge separation by PsII and short-circuit H + fluxes across the thylakoid membrane which decrease the fraction of pumped H + which can be used in adenosine diphosphate phosphorylation. Category two also includes that component of protein turnover which cannot be related to replacement of polypeptides which were incorrectly assembled following uncorrected errors of transcription or translation, or which were damaged by processes whose rate increases with increasing energy input rate such as photodamage to PsII. The third category includes only O 2 -dependent damage to the D1 protein of PsII whose rate increases with a decreasing incident flux of photosynthetically active radiation. Processes in categories two and three are most likely to impose the lower limit on the photon flux density which can support photolithotrophic growth. The available literature, mainly on organisms which are not adapted to growth at very low photon flux densities, suggests that three major limitations (charge recombination in PsII, H + leakage and slippage, and protein turnover) can individually impose lower limits in excess of 20 nmol photon m −2  s −1 on photolithotrophic growth. Furthermore, these three limitations are interactive, so that considering all three processes acting in series leads to an even higher predicted lower photon flux density limit for photolithotrophic growth.

Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance

There are too few data to allow any confident statements on the effects of global climate change on the diversity of marine plant life. However, on the basis of information available in the literature, it is possible to make predictions about the physiological responses of plants under situations of anticipated increases in CO2 concentrations, temperature and UV-B fluxes and point out how differences in the responses of major marine plant groups might lead to changes in performance and distribution of these organisms. For instance we may predict that macrophytes such as seagrasses will show enhanced photosynthetic rates and growth as atmospheric CÜ2 levels continue to rise whilst many intertidal macroalgae are already at CO2 saturation and may not show any enhanced performance as COi increases. Decreasing ozone concentrations in the stratosphere will lead to enhanced UV-B fluxes and could consequently favour those species with UV tolerance or repair mechanisms. It has been suggested that interactions between temperature range and photoperiod can be responsible for excluding species from particular regions of the worlds oceans. Other species might be affected in this way as temperatures at a given latitude change. Temperature will also influence the relationship between atmospheric and dissolved CC>2 and the proportions of the various components of dissolved inorganic carbon available for growth. Climate change may well have other effects on the efficiency with which marine plants use other resources such as N, Fe or Zn and these will also be discussed.