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Far-Red Light Acclimation for Improved Mass Cultivation of Cyanobacteria

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Far-Red Light Acclimation for Improved Mass Cultivation of Cyanobacteria H OH metabolites OH Article Far-Red Light Acclimation for Improved Mass Cultivation of Cyanobacteria Alla Silkina 1 , Bethan Kultschar 2 and Carole A. Llewellyn 2,* 1 Centre for Sustainable Aquatic Research (CSAR), Bioscience department, College of Science, Swansea University, Singleton Park, Swansea SA2 8PP, UK 2 Department of Biosciences, College of Science, Swansea University, Singleton Park, Swansea SA2 8PP, UK * Correspondence: [email protected] Received: 1 August 2019; Accepted: 15 August 2019; Published: 19 August 2019 Abstract: Improving mass cultivation of cyanobacteria is a goal for industrial biotechnology. In this study, the mass cultivation of the thermophilic cyanobacterium Chlorogloeopsis fritschii was assessed for biomass production under light-emitting diode white light (LEDWL), far-red light (FRL), and combined white light and far-red light (WLFRL) adaptation. The induction of chl f was confirmed at 24 h after the transfer of culture from LEDWL to FRL. Using combined light (WLFRL), chl f, a, and d, maintained the same level of concentration in comparison to FRL conditions. However, phycocyanin and xanthophylls (echinone, caloxanthin, myxoxanthin, nostoxanthin) concentration increased 2.7–4.7 times compared to LEDWL conditions. The productivity of culture was double under WLFRL compared with LEDWL conditions. No significant changes in lipid, protein, and carbohydrate concentrations were found in the two different light conditions. The results are important for informing on optimum biomass cultivation of this species for biomass production and bioactive product development. Keywords: cyanobacteria; chromatic adaptation; LED; far-red light; growth; photosynthesis; mass cultivation; pigments; Chlorogloeopsis 1. Introduction Cyanobacteria are photosynthetic prokaryotes that are increasingly explored for use in industrial biotechnology. They are extremely diverse and genetically tractable, making them attractive as cell factories, and can adapt to a wide range of extreme habitats, often with the production of unique metabolites [1]. These adaptations can be exploited in industry to increase productivity and for the production of useful compounds such as pigments, mycosporine-like amino acids (MAAs), and fatty acids [2,3]. Having a long evolutionary history, cyanobacteria have evolved with the ability to cope with varying light intensities and wavelengths. They are able to modify their chlorophylls (chls) and carotenoids, as well as rearrange photosystem I (PSI), PSII, and phycobilisomes (PBS) during excess or limited light conditions [4,5]. These rearrangements allow absorption of light to maximise photosynthetic efficiencies. These light-dependent acclimation processes include; complementary chromatic acclimation (CCA), far-red light photoacclimation (FaRLiP), and low light photoacclimation (LoLiP) [6]. Chlorophyll (chl) a is the major photosynthetic photo-pigment within almost all organisms that utilise oxygenic photosynthesis [7]. Some cyanobacteria have photoadaptive strategies for absorbing longer wavelengths in the far-red light region (700–750 nm) by the production of chl d and f [8]. Inducible production of these chls has been seen in a variety of species, such as Chlorogloeopsis fritschii, PCC 6912 [9], Synechococcus sp. PCC 7335 [10], Chroococcidiopsis thermalis PCC 7203, Leptolyngbya sp. Metabolites 2019, 9, 170; doi:10.3390/metabo9080170 www.mdpi.com/journal/metabolites Metabolites 2019, 9, 2 of 13 Metabolites 2019, 9, 170 2 of 13 JSC-1, and Calothrix sp. PCC 7507 [4]. This phenomena, FaRLiP, achieves remodeling of PSI and PSII JSC-1,as well and as theCalothrix PBS [11], sp. with PCC production 7507 [4]. This of phenomena,chl d, f, and far-red FaRLiP, light achieves (FRL) remodeling absorbing phycobiliproteins of PSI and PSII as wellto maximise as the PBS photosynthesis, [11], with production productivity, of chl andd, f, andsurvival far-red [7,12]. light (FRL) absorbing phycobiliproteins to maximiseChlorogloeopsis photosynthesis, fritschii productivity, (C. fritschii) is and a subsection survival [7 V,12 cyanobacterium,]. first isolated from soils of paddyChlorogloeopsis fields [13]. It fritschiihas a variety(C. fritschii of morphologies) is a subsection and Vis cyanobacterium, tolerant to a variety first of isolated growth from conditions, soils of paddywhich are fields good [13 attributes]. It has a for variety an industrial of morphologies species [14,15]. and is Previous tolerant to research a variety on ofC. growthfritschii conditions,has shown whichthe production are good of attributes chl d and for f under an industrial near infrared species radiation [14,15]. Previous [9]. research on C. fritschii has shown the productionAlgal biotechnology of chl d and isf undera developing near infrared area with radiation continued [9]. advancements in technologies for cultivationAlgal biotechnologyand downstream is aprocessing. developing The area main with commercial continued advancementsapplications of in algal technologies biomass are for aquaculturecultivation and feeding, downstream bioremediation, processing. and The high main value commercial products applications [16]. The mass of algal production biomass areof microalgaeaquaculture species, feeding, including bioremediation, cyanobacteria, and high is value investigated products around [16]. The the mass world. production This is ofbecause microalgae they arespecies, rich includingsources of cyanobacteria, bio-products issuch investigated as polysa aroundccharides, the world.lipids, Thisproteins is because, pigments, they are and rich bioactive sources compoundsof bio-products which such can as be polysaccharides, utilised as feed lipids, and food proteins, and pigments,for pharmaceuticals, and bioactive cosmetics, compounds and health which supplementscan be utilised [17]. as feedThe andspecies-spec food andific for production pharmaceuticals, of useful cosmetics, metabolites and healthfrom the supplements algal biomass, [17]. Theincluding species-specific cyanobacteria, production has been of widely useful metabolites reviewed for from industrial the algal biotechnological biomass, including applications cyanobacteria, [3,16– 18].has been widely reviewed for industrial biotechnological applications [3,16–18]. Additional research is required to understand understand th thee regulation regulation of of photosynthesis, photosynthesis, photoprotection, photoprotection, and photomorphogenesis in cyanobacteria and and the implication of of the use of FRL in increasing productivity andand/or/or pigment pigment accumulation accumulation as as a robusta robu platformst platform in industrialin industrial biotechnology biotechnology [19]. [19]. In this In thisstudy, study, we characterise we characterise the changes the changes in productivity, in productivity, pigment, pigment, and biochemical and biochemical composition composition of C. fritschii of C. fritschiiduring exposureduring exposure to light-emitting to light-emitting diode white diode light white (LEDWL) light and (LEDWL) FRL, followed and FRL, bya followed comparison by ofa whitecomparison light with of white combined light whitewith combined light and FRLwhite (WLFRL) light and results. FRL (WLFRL) We finish results. with a discussionWe finish with on the a discussionapplication on within the application industry. within industry. 2. Results Results 2.1. Growth Growth and Productivity of C. fritschii Under LED White Light and Far Red Light The two growth conditions (LEDWL and FRL) showed similar similar growth growth patterns patterns over over the the 9 9 days. days. Cultures grew in lag phase for the first first 4 days in both conditions, followed by an exponential growth phase for 5 consecutive days (Figure1 1).). Figure 1. GrowthGrowth curve, measured using opticaloptical densitydensity atat 750750 nmnm (OD(OD750750 nm)) of of ChlorogloeopsisChlorogloeopsis fritschii (C. fritschii) underunder either either light-emitting light-emitting diode diode white white light light (LEDWL) (LEDWL) or orfar-red far-red light light (FRL) (FRL) only only for for10 10days. days. The The dotted dotted line line represents represents the the transfer transfer of LEDWL of LEDWL cultures cultures into into FR FRLL for for a further a further 10 10days. days. An overalloverall average average growth growth rate rate (8 days, (8 days, 0 to 8)0 forto LEDWL8) for LEDWL was 0.32 was (STDEV 0.32= (STDEV0.01), in comparison= 0.01), in withcomparison FRL conditions, with FRL which conditions, provided which an averageprovided growth an average rate of growth 0.26 (STDEV rate of= 0.260.02), (STDEV showing = a0.02), low showinglight adaptation a low light of C. adaptation fritschii cultures. of C. fritschii No significant cultures. di Nofference significant was found difference for the was accumulation found for the of accumulation of biomass during the first 8 days under the two light conditions (p > 0.05). From day Metabolites 2019, 9, 3 of 13 4, both cultures reached an exponential growth rate. After 10 days of growth under LEDWL, the cultures were transferred from LEDWL to FRL conditions, these cultures were then exposed to FRL Metabolites 2019, 9, 170 3 of 13 for a further 10 days. The average growth rate of this period was 0.27. The growth of C. fritschii continued in the exponential phase, with a reduced rate compared to LEDWL. biomassThe during final biomass the first productivity 8 days under of the the two culture light under conditions LEDWL (p > was0.05). 0.014 From g L day−1d−1 4,(STDEV both cultures
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