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- Two-stage lipid induction in the microalga tetraselmis striata CTP4 upon exposure to different abiotic stressesPublication . Monteiro, Ivo; Schüler, Lisa M.; Santos, Eunice; Pereira, Hugo; Schulze, Peter S.C.; Florindo, Claudia; Varela, João; Barreira, LuísaTetraselmis striata CTP4 is a euryhaline, robust, fast-growing microalga suitable for wastewater treatment and industrial production. Lipid production was induced through a two-stage cultivation strategy: a 1st stage under standard growth-promoting conditions (100 mu mol photons m- 2 s- 1, salinity 36 ppt and 20 degrees C) to achieve high biomass concentration and a 2nd stage of 6 days for lipid induction by the application of abiotic stresses such as nutrient depletion, high light intensity (200 and 400 mu mol photons m- 2 s- 1), high salinity (75 and 100 ppt), and extreme temperatures (5 and 35 degrees C). Although nutrient depletion always resulted in a decrease in biomass productivity, it had also the highest impact on lipid induction. The highest lipid content (43.2%) and lipid productivity (29.2 mg L-1 d-1) were obtained using a combination of nutrient depletion and high light intensity (400 mu mol m- 2 s- 1). The fatty acid profile was mainly composed of C16:0 (palmitic), C18:1 (oleic) and C18:2 (linoleic) acids. The low content of unsaturated fatty acids and absence of C18:3 (linolenic) acid render the oil of this microalga suitable for biodiesel production, a renewable source of energy.
- Optimisation of biomass production and nutritional value of two marine diatoms (Bacillariophyceae), Skeletonema costatum and Chaetoceros calcitransPublication . Bastos, Carolina R. V.; Maia, Inês Beatriz; Pereira, Hugo; Navalho, João; Varela, JoãoS. costatum and C. calcitrans are two cosmopolitan high-value centric diatoms, with a rich nutritional profile. The following work optimised the culture medium of S. costatum and C. calcitrans cultures, respectively, in a stepwise process as follows: 2.4 mM and 1.2 mM of silicate, 4 mM of nitrate, 100 µM of phosphate, 20 and 80 µM iron, and 0.5 mL L−1 of micronutrients. The results that were obtained revealed an increase in biomass productivity with a 1.8- and 3.2-fold increase in biomass that was produced by S. costatum and C. calcitrans, respectively. The biochemical profile showed an increase in high-value PUFAs such as 2.6-fold and 2.3-fold increase in EPA for S. costatum and C. calcitrans, respectively, whilst a 2.6-fold increase in DHA was detected in S. costatum cultures. The present work provides the basic tools for the industrial cultivation of S. costatum and C. calcitrans with enhanced productivity as well as improved biomass quality, two factors which are highly relevant for a more effective application of these diatoms to aquaculture and nutraceutical production.
- Nutritional and functional evaluation of inula crithmoides and mesembryanthemum nodiflorum grown in different salinities for human consumptionPublication . Ribeiro Lima, Alexandre; Gama, Florinda; Castañeda-Loaiza, Viana; Costa, Camila; Schueler, Lisa M.; Santos, Tamara; Salazar, Miguel; Nunes, Carla; Cruz, Rui M. S.; Varela, J.; Barreira, LuísaThe nutritional composition and productivity of halophytes is strongly related to the biotic/abiotic stress to which these extremophile salt tolerant plants are subjected during their cultivation cycle. In this study, two commercial halophyte species (Inula crithmoides and Mesembryanthemum nodiflorum) were cultivated at six levels of salinity using a soilless cultivation system. In this way, it was possible to understand the response mechanisms of these halophytes to salt stress. The relative productivity decreased from the salinities of 110 and 200 mmol L−1 upwards for I. crithmoides and M. nodiflorum, respectively. Nonetheless, the nutritional profile for human consumption remained balanced. In general, I. crithmoides vitamin (B1 and B6) contents were significantly higher than those of M. nodiflorum. For both species, β-carotene and lutein were induced by salinity, possibly as a response to oxidative stress. Phenolic compounds were more abundant in plants cultivated at lower salinities, while the antioxidant activity increased as a response to salt stress. Sensory characteristics were evaluated by a panel of culinary chefs showing a preference for plants grown at the salt concentration of 350 mmol L−1. In summary, salinity stress was effective in boosting important nutritional components in these species, and the soilless system promotes the sustainable and safe production of halophyte plants for human consumption.
- Comparison of various microbial inocula for the efficient anaerobic digestion of Laminaria hyperboreaPublication . Sutherland, Alastair D.; Varela, J.Background: The hydrolysis of seaweed polysaccharides is the rate limiting step in anaerobic digestion (AD) of seaweeds. Seven different microbial inocula and a mixture of these (inoculum 8) were therefore compared in triplicate, each grown over four weeks in static culture for the ability to degrade Laminaria hyperborea seaweed and produce methane through AD. Results: All the inocula could degrade L. hyperborea and produce methane to some extent. However, an inoculum of slurry from a human sewage anaerobic digester, one of rumen contents from seaweed-eating North Ronaldsay sheep and inoculum 8 used most seaweed volatile solids (VS) (means ranged between 59 and 68% used), suggesting that these each had efficient seaweed polysaccharide digesting bacteria. The human sewage inoculum, an inoculum of anaerobic marine mud mixed with rotting seaweed and inoculum 8 all developed to give higher volumes of methane (means between 41 and 62.5 ml g-1 of seaweed VS by week four) ,compared to other inocula (means between 3.5 and 27.5 ml g-1 VS). Inoculum 8 also gave the highest acetate production (6.5 mmol g-1 VS) in a single-stage fermenter AD system and produced most methane (8.4 mL mmol acetate-1) in phase II of a two-stage AD system. Conclusions: Overall inoculum 8 was found to be the most efficient inoculum for AD of seaweed. The study therefore showed that selection and inclusion of efficient polysaccharide hydrolysing bacteria and methanogenic archaea in an inoculum offer increased methane productivity in AD of L. hyperborea. This inoculum will now being tested in larger scale (10L) continuously stirred reactors optimised for feed rate and retention time to determine maximum methane production under single-stage and two-stage AD systems.
- Antileishmanial activity of meroditerpenoids from the macroalgae Cystoseira baccataPublication . Sousa, Carolina Bruno de; Gangadhar, Katkam N.; Morais, Thiago R.; Conserva, Geanne A. A.; Vizetto-Duarte, C; Pereira, H.; Laurenti, Marcia D.; Campino, Lenea; Levy, Debora; Uemi, Miriam; Barreira, Luísa; Custódio, L.; Passero, Luiz Felipe D.; Lago, Joao Henrique G.; Varela, JoãoThe development of novel drugs for the treatment of leishmaniases continues to be crucial to overcome the severe impacts of these diseases on human and animal health. Several bioactivities have been described in extracts from macroalgae belonging to the Cystoseira genus. However, none of the studies has reported the chemical compounds responsible for the antileishmanial activity observed upon incubation of the parasite with the aforementioned extracts. Thus, this work aimed to isolate and characterize the molecules present in a hexane extract of Cystoseira baccata that was found to be bioactive against Leishmania infantum in a previous screening effort. A bioactivity-guided fractionation of the C. baccata extract was carried out and the inhibitory potential of the isolated compounds was evaluated via the MIT assay against promastigotes and murine macrophages as well as direct counting against intracellular amastigotes. Moreover, the promastigote ultrastructure, DNA fragmentation and changes in the mitochondrial potential were assessed to unravel their mechanism of action. In this process, two antileishmanial meroditerpenoids, (3R)- and (3S)-tetraprenyltoluquinol (1a/1b) and (3R)- and (3S)-tetraprenyltoluquinone (2a/2b), were isolated. Compounds 1 and 2 inhibited the growth of the L. infantum promastigotes (IC50 = 44.9 +/- 4.3 and 94.4 +/- 10.1 mu M, respectively), inducing cytoplasmic vacuolization and the presence of coiled multilamellar structures in mitochondria as well as an intense disruption of the mitochondrial membrane potential. Compound 1 decreased the intracellular infection index (IC50 = 25.0 +/- 4.1 mu M), while compound 2 eliminated 50% of the intracellular amastigotes at a concentration > 88.0 mu M. This work identified compound 2 as a novel metabolite and compound 1 as a biochemical isolated from Cystoseira algae displaying antileishmanial activity. Compound 1 can thus be an interesting scaffold for the development of novel chemotherapeutic molecules for canine and human visceral leishmaniases studies. This work reinforces the evidence of the marine environment as source of novel molecules. (C) 2017 Elsevier Inc. All rights reserved.
- Isolation of a euryhaline microalgal strain, Tetraselmis sp CTP4, as a robust feedstock for biodiesel productionPublication . Pereira, Hugo; Gangadhar, Katkam N.; Schulze, Peter S.C.; Santos, Tamara; de Sousa, Carolina Bruno; Schueler, Lisa; Custódio, Luísa; Malcata, F. Xavier; Gouveia, Luísa; Varela, J.; Barreira, LuísaBioprospecting for novel microalgal strains is key to improving the feasibility of microalgae-derived biodiesel production. Tetraselmis sp. CTP4 (Chlorophyta, Chlorodendrophyceae) was isolated using fluorescence activated cell sorting (FACS) in order to screen novel lipid-rich microalgae. CTP4 is a robust, euryhaline strain able to grow in seawater growth medium as well as in non-sterile urban wastewater. Because of its large cell size (9-22 mu m), CTP4 settles down after a six-hour sedimentation step. This leads to a medium removal efficiency of 80%, allowing a significant decrease of biomass dewatering costs. Using a two-stage system, a 3-fold increase in lipid content (up to 33% of DW) and a 2-fold enhancement in lipid productivity (up to 52.1 mg L-1 d(-1)) were observed upon exposure to nutrient depletion for 7 days. The biodiesel synthesized from the lipids of CTP4 contained high levels of oleic acid (25.67% of total fatty acids content) and minor amounts of polyunsaturated fatty acids with >= 4 double bonds (< 1%). As a result, this biofuel complies with most of the European (EN14214) and American (ASTM D6751) specifications, which commonly used microalgal feedstocks are usually unable to meet. In conclusion, Tetraselmis sp. CTP4 displays promising features as feedstock with lower downstream processing costs for biomass dewatering and biodiesel refining.
- Maritime halophyte species from southern Portugal as sources of bioactive moleculesPublication . Rodrigues, Maria Joao; Gangadhar, Katkam N.; Vizetto-Duarte, C; Wubshet, Sileshi G.; Nyberg, Nils T.; Barreira, Luísa; J. C. or Varela J. or Varela J.C.S., Varela; Custodio, LuisaExtracts of five halophytes from southern Portugal (Arthrocnemum macrostachyum, Mesembryanthemum edule, Juncus acutus, Plantago coronopus and Halimione portulacoides), were studied for antioxidant, anti-inflammatory and in vitro antitumor properties. The most active extracts towards the 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical were the methanol extracts of M. edule (IC50 = 0.1 mg/mL) and J. acutus (IC50 = 0.4 mg/mL), and the ether extracts of J. acutus (IC50 = 0.2 mg/mL) and A. macrostachyum (IC50 = 0.3 mg/mL). The highest radical scavenging activity (RSA) against the 2,2-azino-bis (3-ethylbenzothiazoline-6-sulphonic acid) (ABTS) radical was obtained in the ether extract of J. acutus (IC50 = 0.4 mg/mL) and H. portulacoides (IC50 = 0.9 mg/mL). The maximum total phenolic content (TPC) was found in the methanol extract of M. edule (147 mg gallic acid equivalents (GAE)/g) and in the ether extract of J. acutus (94 mg GAE/g). Significant decreases in nitric oxide (NO) production were observed after incubation of macrophages with lipopolysaccharide (LPS) and the chloroform extract of H. portulacoides (IC50 = 109 mu g/mL) and the hexane extract of P. coronopus (IC50 = 98.0 mu g/mL). High in vitro cytotoxic activity and selectivity was obtained with the ether extract of J. acutus. Juncunol was identified as the active compound and for the first time was shown to display selective in vitro cytotoxicity towards various human cancer cells.
- Assessment and comparison of the properties of biodiesel synthesized from three different types of wet microalgal biomassPublication . Gangadhar, Katkam N.; Pereira, Hugo; Diogo, Herminio P.; Borges dos Santos, R. M.; Devi, B. L. A. Prabhavathi; Prasad, R. B. N.; Custódio, Luísa; Xavier Malcata, F.; Varela, João; Barreira, LuísaIn recent years, microalgae-based carbon-neutral biofuels (i.e., biodiesel) have gained considerable interest due to high growth rate and higher lipid productivity of microalgae during the whole year, delivering continuous biomass production as compared to vegetable-based feedstocks. Therefore, biodiesel was synthesized from three different microalgal species, namely Tetraselmis sp. (Chlorophyta) and Nannochloropsis oculata and Phaeodactylum tricornutum (Heterokontophyta), and the fuel properties of the biodiesel were analytically determined, unlike most studies which rely on estimates based on the lipid profile of the microalgae. These include density, kinematic viscosity, total and free glycerol, and high heating value (HHV), while cetane number (CN) and cold filter plugging point (CFPP) were estimated based on the fatty acid methyl ester profile of the biodiesel samples instead of the lipid profile of the microalgae. Most biodiesel properties abide by the ASTM D6751 and the EN 14214 specifications, although none of the biodiesel samples met the minimum CN or the maximum content of polyunsaturated fatty acids with a parts per thousand yen4 double bonds as required by the EN 14214 reference value. On the other hand, bomb calorimetric experiments revealed that the heat of combustion of all samples was on the upper limit expected for biodiesel fuels, actually being close to that of petrodiesel. Post-production processing may overcome the aforementioned limitations, enabling the production of biodiesel with high HHV obtained from lipids present in these microalgae.
- Trends and strategies to enhance triacylglycerols and high-value compounds in microalgaePublication . Lisa Schueler, Lisa M. Schueler; Schulze, Peter S.C.; Pereira, Hugo; Barreira, Luísa; Leon, Rosa; J. C. or Varela J. or Varela J.C.S., VarelaMicroalgae are important sources of triacylglycerols (TAGs) and high-value compounds such as carotenoids and long-chain polyunsaturated fatty acids (LC-PUFAs). TAGs are feedstocks for biofuels or edible oils; carotenoids are used as pigments in the food and feed industries; and LC-PUFAs are beneficial for human health, being also key to the correct development of fish in aquaculture. Current trends in microalgal biotechnology propose the combined production of biofuels with high-value compounds to turn large-scale production of microalgal biomass into an economically feasible venture. As TAGs, carotenoids and LC-PUFAs are lipophilic biomolecules, they not only share biosynthetic precursors and storage sinks, but also their regulation often depends on common environmental stimuli. In general, stressful conditions favor carotenoid and TAGs biosynthesis, whereas the highest accumulation of LC-PUFAs is usually obtained under conditions promoting growth. However, there are known exceptions to these general rules, as a few species are able to accumulate LC-PUFAs under low light, low temperature or long-term stress conditions. Thus, future research on how microalgae sense, transduce and respond to environmental stress will be crucial to understand how the biosynthesis and storage of these lipophilic molecules are regulated. The use of high-throughput methods (e.g. fluorescent activated cell sorting) will provide an excellent opportunity to isolate triple-producers, i.e. microalgae able to accumulate high levels of LC-PUFAs, carotenoids and TAGs simultaneously. Comparative transcriptomics between wild type and tripleproducers could then be used to identify key gene products involved in the regulation of these biomolecules even in microalgal species not amenable to reverse genetics. This combined approach could be a major step towards a better understanding of the microalgal metabolism under different stress conditions. Moreover, the generation of triple-producers would be essential to raise the biomass value in a biorefinery setting and contribute to meet the world's rising demand for food, feed and energy.
- Effects of LED lighting on Nannochloropsis oceanica grown in outdoor raceway pondsPublication . Carneiro, M.; Maia, Inês Beatriz; Cunha, P.; Guerra, I.; Magina, T.; Santos, Tamara; Schulze, Peter S.C.; Pereira, H.; Malcata, F. X.; Navalho, J.; Silva, J.; Otero, A.; Varela, JoãoGrowth in most microalgal mass cultivation systems is light-limited, particularly in raceway ponds (RWP) where the light path is higher. Artificial lighting can be a promising solution to diminishing dark zones and enhance microalgal productivity. Therefore, our goal was to prevent the cell shift from photosynthesis to a respiration-only stage by resorting to LED illumination. Nannochloropsis oceanica cultures were accordingly grown out-doors in a preliminary small-scaleexperiment, followed by pilot-scale trials. In the former, three 3.0-m(2) RWP were set up under three distinct conditions: 1) without LEDs (control); 2) LEDs turned on during the night; and 3) LEDs turned on for 24 h. In the pilot-scale trial, one of two 28.9-m(2) pilot-scale RWPs was coupled to the best LED setup - determined in the small-scale preliminary experiment - using the same light intensity (normal mode) and half of the intensity (economy mode), with the second RWP serving as a control. In the preliminary experiment, the use of LEDs for 24 h was deemed as not helpful during daytime, before the culture reached asymptotic to 0.5 g DW L-1 - when dark zones appeared during the day due to sunlight attenuation in the 0.1 m-deep cultures. Overall, use of LEDs increased biomass growth chiefly by increasing nighttime productivities - materialized in higher chlorophyll, protein, and carbohydrate productivities in LED-lit cultures. A higher impact of LED lighting was observed under lower sunlight irradiances. A preliminary economic analysis indicates that use of LEDs in RWPs outdoors should be considered for high-value metabolites only.