Dagmar B. Stengel

Evolution and Diversity of Plant Cell Walls: From Algae to Flowering Plants

All photosynthetic multicellular Eukaryotes, including land plants and algae, have cells that are surrounded by a dynamic, complex, carbohydrate-rich cell wall. The cell wall exerts considerable biological and biomechanical control over individual cells and organisms, thus playing a key role in their environmental interactions. This has resulted in compositional variation that is dependent on developmental stage, cell type, and season. Further variation is evident that has a phylogenetic basis. Plants and algae have a complex phylogenetic history, including acquisition of genes responsible for carbohydrate synthesis and modification through a series of primary (leading to red algae, green algae, and land plants) and secondary (generating brown algae, diatoms, and dinoflagellates) endosymbiotic events. Therefore, organisms that have the shared features of photosynthesis and possession of a cell wall do not form a monophyletic group. Yet they contain some common wall components that can be explained increasingly by genetic and biochemical evidence.

Algal chemodiversity and bioactivity: Sources of natural variability and implications for commercial application

There has been significant recent interest in the commercial utilisation of algae based on their valuable chemical constituents many of which exhibit multiple bioactivities with applications in the food, cosmetic, agri- and horticultural sectors and in human health. Compounds of particular commercial interest include pigments, lipids and fatty acids, proteins, polysaccharides and phenolics which all display considerable diversity between and within taxa. The chemical composition of natural algal populations is further influenced by spatial and temporal changes in environmental parameters including light, temperature, nutrients and salinity, as well as biotic interactions. As reported bioactivities are closely linked to specific compounds it is important to understand, and be able to quantify, existing chemical diversity and variability. This review outlines the taxonomic, ecological and chemical diversity between, and within, different algal groups and the implications for commercial utilisation of algae from natural populations. The biochemical diversity and complexity of commercially important types of compounds and their environmental and developmental control are addressed. Such knowledge is likely to help achieve higher and more consistent levels of bioactivity in natural samples and may allow selective harvesting according to algal species and local environmental conditions for different groups of compounds.

Metal accumulation and toxicity measured by PAM—Chlorophyll fluorescence in seven species of marine macroalgae

The effects of five metals, copper (Cu), chromium (Cr), Zinc (Zn), cadmium (Cd) and lead (Pb), on photosynthetic activity, measured as pulse amplitude modulation (PAM) chlorophyll fluorescence yield, was monitored in seven species of green, red and brown macroalgae over a 14d period. The 10micromoll(-1) of Cr and Zn reduced chlorophyll fluorescence of all species by day 4, and 10micromoll(-1) of Cu and Cd reduced the fluorescence of some species; however, fluorescence yields of all species were unaffected by 10micromoll(-1) of Pb. Metals were generally accumulated in the order of Cu>Pb>Zn>Cr>Cd. Ulva intestinalis accumulated the highest amounts of all metals, and Cladophora rupestris the lowest. A relationship between internal metal concentration and fluorescence was not always evident as in some cases fluorescence was reduced at low metal contents. In the case of Zn, fluorescence was lowest in plants which contained lowest concentrations after 14d-exposure, possibly because plants had died and Zn leached out of the algal cells. The relationship between internal metal concentration and fluorescence was algal species and metal-specific.

Profiling phlorotannins in brown macroalgae by liquid chromatography-high resolution mass spectrometry.

INTRODUCTION Phlorotannins, phenolic compounds produced exclusively by Phaeophyceae (brown algae), have recently been associated with a wide variety of beneficial bioactivities. Several studies have measured the total phenolic content in extracts from various species, but little characterisation of individual phlorotannin components has been demonstrated. OBJECTIVE The purpose of this study was to develop a liquid chromatography-mass spectrometry (LC-MS) based method for rapid profiling of phlorotannins in brown algae. METHODOLOGY Phlorotannin-enriched extracts from five phaeophyceaen species were analysed by ultrahigh-pressure liquid chromatography (UHPLC) operating in hydrophilic interaction liquid chromatography (HILIC) mode combined with high resolution mass spectrometry (HRMS). The method was optimised using an extract of Fucus vesiculosus; separation was achieved in less than 15 min. The basic mobile phase enhanced negative-ion electrospray ionisation (ESI), and generated multiply charged ions that allowed detection of high molecular weight phlorotannins. RESULTS The phlorotannin profiles of Pelvetia canaliculata, Fucus spiralis, F. vesiculosus, Ascophyllum nodosum and Saccharina longicruris differed significantly. Fucus vesiculosus yielded a high abundance of low molecular weight (< 1200 Da) phlorotannins, while P. canaliculata exhibited a more evenly distributed profile, with moderate degrees of polymerisation ranging from 3 to 49. HRMS enabled the identification of phlorotannins with masses up to 6000 Da using a combination of accurate mass and ¹³C isotopic patterns. CONCLUSION The UHPLC-HRMS method described was successful in rapidly profiling phlorotannins in brown seaweeds based on their degree of polymerisation. HILIC was demonstrated to be an effective separation mode, particularly for low molecular weight phlorotannins.

Prospects and challenges for industrial production of seaweed bioactives

Large‐scale seaweed cultivation has been instrumental in globalizing the seaweed industry since the 1950s. The domestication of seaweed cultivars (begun in the 1940s) ended the reliance on natural cycles of raw material availability for some species, with efforts driven by consumer demands that far exceeded the available supplies. Currently, seaweed cultivation is unrivaled in mariculture with 94% of annual seaweed biomass utilized globally being derived from cultivated sources. In the last decade, research has confirmed seaweeds as rich sources of potentially valuable, health‐promoting compounds. Most existing seaweed cultivars and current cultivation techniques have been developed for producing commoditized biomass, and may not necessarily be optimized for the production of valuable bioactive compounds. The future of the seaweed industry will include the development of high value markets for functional foods, cosmeceuticals, nutraceuticals, and pharmaceuticals. Entry into these markets will require a level of standardization, efficacy, and traceability that has not previously been demanded of seaweed products. Both internal concentrations and composition of bioactive compounds can fluctuate seasonally, geographically, bathymetrically, and according to genetic variability even within individual species, especially where life history stages can be important. History shows that successful expansion of seaweed products into new markets requires the cultivation of domesticated seaweed cultivars. Demands of an evolving new industry based upon efficacy and standardization will require the selection of improved cultivars, the domestication of new species, and a refinement of existing cultivation techniques to improve quality control and traceability of products.

LC-PUFA-Enriched Oil Production by Microalgae: Accumulation of Lipid and Triacylglycerols Containing n-3 LC-PUFA Is Triggered by Nitrogen Limitation and Inorganic Carbon Availability in the Marine Haptophyte Pavlova lutheri

In most microalgal species, triacyglycerols (TAG) contain mostly saturated and monounsaturated fatty acids, rather than PUFA, while PUFA-enriched oil is the form most desirable for dietary intake. The ability of some species to produce LC-PUFA-enriched oil is currently of specific interest. In this work, we investigated the role of sodium bicarbonate availability on lipid accumulation and n-3 LC-PUFA partitioning into TAG during batch cultivation of Pavlova lutheri. Maximum growth and nitrate uptake exhibit an optimum concentration and threshold tolerance to bicarbonate addition (~9 mM) above which both parameters decreased. Nonetheless, the transient highest cellular lipid and TAG contents were obtained at 18 mM bicarbonate, immediately after combined alkaline pH stress and nitrate depletion (day nine), while oil body and TAG accumulation were highly repressed with low carbon supply (2 mM). Despite decreases in the proportions of EPA and DHA, maximum volumetric and cellular EPA and DHA contents were obtained at this stage due to accumulation of TAG containing EPA/DHA. TAG accounted for 74% of the total fatty acid per cell, containing 55% and 67% of the overall cellular EPA and DHA contents, respectively. These results clearly demonstrate that inorganic carbon availability and elevated pH represent two limiting factors for lipid and TAG accumulation, as well as n-3 LC-PUFA partitioning into TAG, under nutrient-depleted P. lutheri cultures.

Morphology and in situ growth rates of plants of Ascophyllum nodosum (Phaeophyta) from different shore levels and responses of plants to vertical transplantation

Morphological characters and growth rates of Ascophyllum nodosum were compared on fronds collected from different shore levels at one site in Strangford Lough, Northern Ireland. Both the bladders and axes of thallus tips were smaller and less variable on the upper shore than on the middle and lower shores, and the proportion of biomass invested in the production of bladders was smaller. The axes of upper shore plants were wider and flatter than on the lower shore, and the bladders were also relatively flat on the upper shore but more rounded on the lower shore. The maximum age of unbroken fronds, as estimated from the number of air bladders, was 6 years on the upper shore and 17 years on the lower shore, indicating the higher probability of breakage of plants caused by stress on the upper shore. In situ growth rates of individually marked plants along a vertical shore transect were monitored at 2- to 4-week intervals for 31 months. Length increase was highest (16 cm yr−1) in the middle of the Ascophyllum ...

Impacts of ambient salinity and copper on brown algae: 2. Interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin

The aim of this study was to establish in laboratory experiments a quantitative link between phenolic pool (production, composition and exudation) in Ascophyllum nodosum and Fucus vesiculosus and their potential to bind metals. Additionally, the copper binding capacity of purified phlorotannin was investigated. A reduction in salinity decreased total phenolic contents, altered phenolic composition by increasing proportion of cell-wall phenolics, and also increased phenolic exudation of the two seaweed species. After 15 days at a salinity of 5, the inhibition of photosynthesis observed previously for A. nodosum coincided with the high exudation of phenolic compounds into the surrounding water of the seaweed tips which resulted in a significant reduction of phenolic contents. Increased copper concentration also reduced total phenolic contents, changed phenolic composition (increase in proportion and level of cell-wall phenolics), and positively affected phenolic exudation of A. nodosum and F. vesiculosus. A decrease in salinity enhanced the copper toxicity and caused the earlier impact on the physiology of seaweed tips. An involvement of phlorotannins in copper binding is also demonstrated; purified phlorotannins from A. nodosum collected from a site with little anthropogenic activity contained all four metals tested. When placed in copper-enriched water, as for the seaweed material, copper contents of the phenolics increased, zinc and cadmium contents decreased, but no change in chromium content was observed. The use of cell-wall phenolic content as biomarker of copper contamination seems promising but needs further investigation.

A new HPLC method for the detection of iodine applied to natural samples of edible seaweeds and commercial seaweed food products.

Rich in micronutrients and considered to contain high iodine levels, seaweeds have multiple applications as food/supplements and nutraceuticals with potential health implications. Here, we describe the development and validation of a new analytical method to quantify iodine as iodide (I(-)) using an isocratic HPLC system with UV detection; algal iodine was converted to I(-) via dry alkaline incineration. The method was successfully applied to 19 macroalgal species from three taxonomic groups and five commercially available seaweed food products. Fesh kelps contained highest levels, reaching >1.0% per dry weight (DW), but concentrations differed amongst thallus parts. In addition to kelps, other brown (Fucales: ∼ 0.05% DW) and some red species (∼ 0.05% DW) can also serve as a rich source of iodine; lowest iodine concentrations were detected in green macroalgae (∼ 0.005% DW), implying that quantities recommended for seaweed consumption may require species-specific re-evaluation to reach adequate daily intake levels.

Connecting marine productivity to sea-spray via nanoscale biological processes: Phytoplankton Dance or Death Disco?

Bursting bubbles at the ocean-surface produce airborne salt-water spray-droplets, in turn, forming climate-cooling marine haze and cloud layers. The reflectance and ultimate cooling effect of these layers is determined by the spray’s water-uptake properties that are modified through entrainment of ocean-surface organic matter (OM) into the airborne droplets. We present new results illustrating a clear dependence of OM mass-fraction enrichment in sea spray (OMss) on both phytoplankton-biomass, determined from Chlorophyll-a (Chl-a) and Net Primary Productivity (NPP). The correlation coefficient for OMss as a function of Chl-a increased form 0.67 on a daily timescale to 0.85 on a monthly timescale. An even stronger correlation was found as a function of NPP, increasing to 0.93 on a monthly timescale. We suggest the observed dependence is through the demise of the bloom, driven by nanoscale biological processes (such as viral infections), releasing large quantities of transferable OM comprising cell debris, exudates and other colloidal materials. This OM, through aggregation processes, leads to enrichment in sea-spray, thus demonstrating an important coupling between biologically-driven plankton bloom termination, marine productivity and sea-spray modification with potentially significant climate impacts.