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Metabolic and Cellular Organization in Evolutionarily Diverse Microalgae As Related to Biofuels Production Hildebrand Et Al

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Metabolic and Cellular Organization in Evolutionarily Diverse Microalgae As Related to Biofuels Production Hildebrand Et Al Available online at www.sciencedirect.com Metabolic and cellular organization in evolutionarily diverse microalgae as related to biofuels production 1 1 3 Mark Hildebrand , Raffaela M Abbriano , Juergen EW Polle , 1 2 Jesse C Traller , Emily M Trentacoste , 1 1 Sarah R Smith and Aubrey K Davis Microalgae are among the most diverse organisms on the classes [2 ], especially in relation to the location of planet, and as a result of symbioses and evolutionary selection, carbon fixation enzymes and carbohydrate storage the configuration of core metabolic networks is highly varied (Figure 1). Organizational differences likely affect pro- across distinct algal classes. The differences in cesses such as photosynthesis, carbon flux through meta- photosynthesis, carbon fixation and processing, carbon bolic networks, and biosynthesis of fuel-relevant storage, and the compartmentation of cellular and metabolic compounds. The goal of this review is to highlight the processes are substantial and likely to transcend into the relevance of these aspects of algal diversity to biofuel efficiency of various steps involved in biofuel molecule molecule production. production. By highlighting these differences, we hope to provide a framework for comparative analyses to determine the Light harvesting and photoprotection efficiency of the different arrangements or processes. This sets The evolution of microalgae has generated a variety of the stage for optimization on the based on information derived components and organizational schemes of the photosyn- from evolutionary selection to diverse algal classes and to thetic apparatus (Figure 2). All microalgae have light synthetic systems. harvesting antenna complexes, PSII, the cytochrome b6f Addresses complex, and PSI. The use of the bulky phycobilisomes 1 Marine Biology Research Division, Scripps Institution of (peripherally associated with the thylakoid membrane) for Oceanography, University of California San Diego, 9500 Gilman Drive, La light harvesting in cyanobacteria, glaucophytes, and rho- Jolla, CA 92093-0202, USA 2 Integrated Oceanography Division, Scripps Institution of dophytes results in a relatively large spacing between the Oceanography, University of California San Diego, 9500 Gilman Drive, La photosynthetic membranes (Figure 2a and c), which could Jolla, CA 92093-0202, USA 3 affect photosynthetic capacity [3]. Downsizing of the light Department of Biology, CUNY Brooklyn College, 2900 Bedford Avenue harvesting complexes is apparent in rhodophytes, which 200 NE, Brooklyn, NY 11210, USA have membrane-integral LHCs, and cryptomonads, which Corresponding author: Hildebrand, Mark ([email protected]) utilize unassembled biliproteins in the lumen of the thy- lakoids, enabling stacked thylakoid grana (Figure 2). Stacked grana arose independently in both chlorophytes Current Opinion in Chemical Biology 2013, 17:506–514 and in derivatives of the red algae, and may serve to This review comes from a themed issue on Energy enhance light capture and connectivity between PSIIs Edited by Michael D Burkart and Stephen P Mayfield with large functional antenna size [3,4]. The numbers of For a complete overview see the Issue and the Editorial grana stacks differ; chromalveolates typically have three, while chlorophytes can have 2–3 times more [5 ]. In Available online 26th March 2013 chlorophytes, PSII is highly enriched in the grana and 1367-5931/$ – see front matter, # 2013 Elsevier Ltd. All rights PSI in the stroma thylakoids, while in chromalveolates, reserved. they are nearly equally distributed [6]. Chlorophytes use http://dx.doi.org/10.1016/j.cbpa.2013.02.027 LHCs specific for either PSI or PSII (Figure 2), and stramenopiles such as diatoms use fucoxanthin chlorophyll binding proteins (FCPs) in a similar capacity [7 ]. Strame- Introduction nopile FCPs have a carotenoid:chlorophyll ratio of 4:4 Improving the productivity of strains is a major factor in compared with 14:4 in LHCs for chlorophytes, resulting making algal biofuels economically viable [1 ]. Algal in a shift of absorbance into the 460–570 nm range, which is productivity is ultimately dependent on the efficiency not accessible to chlorophytes [8]. of carbon fixation and the downstream cellular processes that convert photosynthate into useful fuel precursors. Efficient photosynthesis requires balance between light The diversity of contemporary microalgal metabolism has absorbed by PSI and PSII and dissipation of energy from been shaped by multiple endosymbiotic acquisitions, excess absorbed light. The distribution of light between environmental factors, and evolutionary selection. The the photosystems in cyanobacteria, cryptomonads, rho- result has been distinct intracellular compartmentation dophytes, and chlorophytes (and higher plants) involves and unique organizational schemes among different algal state transitions in which a phosphatase/kinase driven Current Opinion in Chemical Biology 2013, 17:506–514 www.sciencedirect.com Metabolic and cellular organization in evolutionarily diverse microalgae as related to biofuels production Hildebrand et al. 507 Figure 1 Chloroplast Primary progenitor endosymbiont N N N Pyr Pyr Carboxysome Presence of Carboxysome pyrenoid is species Floridean dependent Starch Glycogen Starch Glycogen Chlorophytes, Charophytes, Rhodophytes Glaucophytes (e.g. Cyanophora) Prasinophytes, Trebouxiophytes Presence of pyrenoids and carbohydrate Cyanobacteria Granular starch stored in the cytoplasm. storage form are species dependent. Starch stored in the chloroplast Glycogen storage Peptidoglycan layer between inner and outer Floridean starch is a less crystalline form. concentrated around the pyrenoid ct membranes. Secondary endosymbiont N N N Pyr N Pyr Pyr Pyr Chrysolaminarin Vacuole Nm Nm Euglenophytes Paramylon (β-1,3, glucan) stored in the cytoplasm Chlorarachniophytes (e.g. Bigelowiella natans) Cryptophytes (e.g. Guillardia theta) Stramenopiles and Haptophytes β-1,3 glucan stored in vesicles surrounding the ctER Starch stored in periplastidic compartment β-1,3 glucan stored in chrysolaminarin vacuole Three membranes around the chloroplast around the pyrenoid. around the pyrenoid. with possible exception of Eustimatophytes. N = nucleus, Nm = nucleomorph, Pyr = pyrenoid Current Opinion in Chemical Biology Organization of carbon fixation and carbohydrate storage in evolutionarily-diverse classes of microalgae. Colored bars denote the overall class of algae: blue-green = glaucophyte; green = green algae and endosymbiotic derivatives; red = red algae and endosymbiotic derivatives. Membrane systems associated with the cell (cyanobacteria), cyanelle (glaucophytes), or chloroplasts (others), are color coded to denote cyanobacterial-like (blue- green), inner and outer chloroplast membranes [green, except in glaucophytes, which contain a peptidoglycan layer in between (purple)], and secondary endosymbiosis membranes in Euglenophytes (gold), Chlorarachniophytes (fuschia and blue for periplastid and ER, respectively) and Cryptophytes, Stramenopiles, and Haptophytes (red and blue for periplastid and ER, respectively). Different carbohydrate storage forms are labeled and denoted by different colors. Text highlights the major features in each. reversible physical movement of the LHC occurs between phycobilisome-containing organisms and the Chlorarach- PSII and PSI [9]. State transitions have not been docu- niophyta [11 ,13], and NPQ in cryptophytes differs from mented in diatoms [5], and none are reported for the other chromalveolates [14]. eustigmatophyceae. Instead, diatoms balance photosystem activity by quenching photon absorption by PSII as a result Differences in photosynthetic processes are likely to of de-epoxidation of xanthophyll pigments [10]. A direct affect light harvesting efficiency, which ultimately trans- comparison showed that this process resulted in 2-fold less lates into altered growth and product molecule accumu- generation of wasted electrons than state transitions in a lation. There are very few definitive analyses comparing chlorophyte [10]. Quenching in the antenna system also the relative efficiency of the described diverse photosyn- reduces damage to the photosystems, which carries a high thetic arrangements. Such information would not only aid energetic replacement cost [11 ]. Dissipation of excess in developing strategies for improved light capture in light in photosynthesis is primarily achieved through diverse classes of microalgae, but potentially in the de- non-photochemical quenching (NPQ). Different strat- velopment of artificial photosynthesis approaches. egies have developed for NPQ in evolutionarily distinct classes of algae, including rapid rates of synthesis or high Carbon fixation and concentration accumulation of de-expoidized xanthophylls [12]. Carbon fixation in the Calvin–Benson cycle is catalyzed Xanthophyll cycling systems are apparently lacking in by RuBisCO, which has a low CO2-saturated maximum www.sciencedirect.com Current Opinion in Chemical Biology 2013, 17:506–514 508 Energy Figure 2 (a) (b) Cyanobacteria and Glaucophytes Cryptomonads LHC PSII ATP PBS ATP LHC LHC PSII b6f PSI b6f PSI PSII PSII Biliproteins b6f PSI PSII b6f PSI LHC LHC ATP ATP PBS PSII LHC Rhodophytes Chlorophytes PBS ATP LHC PSII LHC ATP b6f PSI LHC LHC PSII b6f PSI PSII PSII b f PSI 6 LHC LHC PSII b6f PSI ATP LHC ATP PBS LHC PSII (c) Photosynthetic Membrane Arrangement (to scale) Diatoms FCP Phycobilisome-containing FCP PSII b6f PSI Lumen ATP FCP FCP PSII b6f PSI Lumen FCP PSII b6f PSI FCP ATP Other FCP PSII
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