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Comparative Analysis of Growth and Carotenoid Accumulation of Trentepohlia Arborum in Aerial, Subaerial, and Aquatic Cultivation

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Comparative Analysis of Growth and Carotenoid Accumulation of Trentepohlia Arborum in Aerial, Subaerial, and Aquatic Cultivation J Appl Phycol DOI 10.1007/s10811-014-0436-x Comparative analysis of growth and carotenoid accumulation of Trentepohlia arborum in aerial, subaerial, and aquatic cultivation Lin Chen & Lanlan Zhang & Wei Zhang & Tianzhong Liu Received: 17 June 2014 /Revised and accepted: 30 September 2014 # Springer Science+Business Media Dordrecht 2014 Abstract The aerial filamentous microalga, Trentepohlia Introduction arborum (Chlorophyta), was cultured in three habitats - an aerial, a subaerial and an aquatic one - using different types of The algal genus Trentepohlia is widespread in different loca- bioreactors. The growth, carotenoid productivity, and morpho- tions such as tropical, subtropical, and temperate regions, even logic differences of T. arborum in different habitats were inves- in frigid zones (Allali et al. 2013;Nashetal.1987; Jorgensen tigated. The maximum specific growth rate (μ)ofthealga and Tonsberg 1988; Liu et al. 2012). The colonies of obtained in the logarithmic phase in the subaerial habitat was Trentepohlia generally grow on the surface of rocks, soil, 0.034 h−1. HPLC analysis also demonstrated that T. arborum walls, or tree trunks, to form a spectacular orange or red accumulated a high content of carotenoids. Zeaxanthin was the “carpet” named “Red stone” (Liu et al. 2012), because it is primary carotenoid in subaerial culture, while β,β-carotene was rich in carotenoid content, especially β-carotene (Kjosen et al. dominant in aerial culture. The maximum carotenoid produc- 1972; Czeczuga and Maximov 1996; Abe et al. 1998; tivity, 67.7 mg m−2 day−1, was reached when T. arborum was Mukherjee et al. 2010). Moreover, some carotenoids, unique cultured in the subaerial habitat under nitrogen depletion using to this group, have been found in Trentepohlia gobii a novel attached cultivation bioreactor. Overall, it was demon- Meyer (Czeczuga and Maximov 1996)andTrentepohlia strated that T. arborum exhibited a relatively high growth rate jolithus (L.) Wallroth (Kjosen et al. 1972;Nybraateand and carotenoid productivity under attached cultivation. Liaaen-Jensen 1974). In addition to carotenoids, Trentepohlia also produces some antioxidant and antimicrobially active substances such as phenolic and Keywords β-Carotene . Trentepohlia arborum . Attached flavonoid compounds (Simic et al. 2012). Therefore, this cultivation . Aerial algae alga has potential economic importance. Many studies have been carried out on Trentepohlia spp., most of them focused mainly on taxonomy (Lopez-Bautista et al. 2006; Rindi and Lopez-Bautista 2007; Rindi et al. 2009), ecology (Rindi and Guiry 2002; Rindi and Lopez-Bautista L. Chen : L. Zhang : W. Zhang : T. Liu (*) Key Laboratory of Biofuels, Qingdao Institute of Bioenergy and 2007; Liu et al. 2012; Allali et al. 2013), and physiological Bioprocess Technology, Chinese Academy of Sciences, characteristics (Abe et al. 1999; Chapman et al. 2001; Gupta Qingdao 266101, Shandong, People’s Republic of China and Agrawal 2004; Mukherjee et al. 2010). Only a few at- e-mail: [email protected] tempts have been made to culture Trentepohlia odorata (F.H. L. Chen Wiggers) Wittrock (Ho et al. 1983; Lee et al. 1990)and e-mail: [email protected] Trentepohlia aurea (L.) C.F.P. Martius (Abe et al. 1998; L. Zhang 2003; 2008) for biotechnological applications such as biolog- College of Food Science and Engineering, Ocean University of ical nitrogen removal. China, Qingdao 266003, People’s Republic of China Trentepohlia is referred to as an aerial (Abe et al. 1998)or subaerial genus (Ho et al. 1983; Rindi and Guiry 2002;Liu L. Chen University of Chinese Academy of Sciences, Beijing 100049, et al. 2012), with none ever found in natural aquatic habitats People’sRepublicofChina (Lopez-Bautista et al. 2002). However, some species, such as J Appl Phycol T. aurea,canbegrownsuccessfullyinliquidmediuminthe was dripped down onto the filter paper (Fig. 1d)througha laboratory (Abe et al. 1998). However, the relatively slow perforated nylon tubing positioned between the filter paper growth encountered in liquid-suspended cultures is unsuit- and glass plate at the top of the glass chamber, using a able to produce carotenoids for industrial purposes. It mini peristaltic pump. In the second type of reactor, the should also be noted, however, that some species of medium was spread onto the algae cells on the surface of Trentepohlia alternate between periods of exposure to air the filter paper using a mini ultrasonic atomizer (HL- and immersion by dew and rain in their natural habitats. MM001, Zhongshan Hongling Electrical Appliance Co., Therefore, Trentepohlia exhibits the ability to survive in Ltd., China), which was placed at the bottom of the cham- both aquatic and aerial conditions. Unlike other species of ber and was immerged in the liquid medium. The third Trentepohlia, T. arborum (C. Agardh) Hariot has been type of reactor was a conventional air-bubbling column reported growing very vigorously in natural habitats (Rindi with 3-cm diameter and 50-cm height (Fig. 1b). As a result, et al. 2005). However, there are no reports on its cultiva- the algae T. arborum was grown in three different artificial tion and product accumulation. habitats of subaerial (Fig. 1a), aerial (Fig. 1c), and aquatic In the present study, alga T. arborum was cultured in three (Fig. 1b)conditions. types of artificial habitats, namely, aquatic, subaerial, and For subaerial and aerial cultivation, the algal inoculum aerial, to study growth and carotenoid accumulation. Morpho- was evenly filtered onto a cellulose filter paper, which logical differences in the varying cultivation modes were also showed superior performance for algae growth compared compared. to glass fiber (GF), nitrocellulose (NC), and cellulose filter papers in preliminary experiments, to form an algal “disk” with a footprint of 10 cm2. The inoculum density Materials and methods of the algal disk was controlled at about 5 mg (dry weight) by adjusting the volume of the prepared algal The alga T. arborum was a gift of Prof. Liu Guo-Xiang from broth. Then, the algal “disk” wasplacedonthesurface the Institute of Hydrobiology, Chinese Academy of Sciences. of a glass plate, and finally, the device was placed into the The strain was isolated from the bark of a Ficus virens in chambers for attached cultivation with a constant medium Sichuan, China. The strain was identified by morphology and supply of 60 mL h−1 via the peristaltic pump or the SSU rDNA gene sequence comparison using the NCBI ultrasonic atomizer, respectively. For liquid cultivation, BLAST database (Liu et al. 2012). The alga was maintained the alga inoculum was concentrated by gravity settling on solid BG11 medium containing 1 % agar and then trans- and was resuspended in fresh BBM medium to a cell ferred into liquid modified Bold’s Basal medium (BBM) for densityof0.5gL−1. culturing. The composition of the modified BBM medium All of the three types of bioreactor were installed in a was as follows (Abe et al. 2008): 1.0 g NH4Cl, 175 mg cultivation room under constant temperature (25 °C), contin- KH2PO4,75mgK2HPO4,25mgMgSO4·7H2O, 25 mg NaCl, uously aerated with 1 % CO2 gas at 0.1 vvm, and illuminated 50 mg EDTA, 30 mg KOH, 5 mg FeSO4·7H2O, and 11 mg with artificial light, provided by fluorescent lamps, of around −2 −1 H3BO3 in 1 L of deionized (DI) water (pH adjusted prior to 35 μmol photons m s . autoclaving to 8.0). The relative humidity in the glass chamber was deter- The strain was firstly grown in liquid BBM in a glass mined using a digital hygrometer (S-WS8061A, Shenzhen bubbling column (5-cm diameter and 700 cm high) under a AOV Testing Technology Co., Ltd., China). constant temperature of 25 °C and a light intensity of 50 μmol photons m−2 s−1. The culture was continuously Measurement of algae growth aerated with CO2-enriched air (air:CO2=1:0.02, v/v) at a flow rate of 0.25 vvm. After 7 days of cultivation, the broth was The chlorophyll content and dry weight were measured used as the inoculum. to evaluate algae growth. For the aquatic culture, 3–5mL of the culture medium was filtered on a pre-weighted NC Photo-bioreactor and cultivation membrane under vacuum and washed three times with deionized water. Then the membranes were oven dried to Three types of photo bioreactor were employed in this a constant weight at 105 °C for 2 h. For the aerial and study to cultivate T. arborum.Thefirst(Fig.1a)and subaerial cultures, the absolute amounts of the biomass second types (Fig. 1c) of bioreactor, which were called on the filter paper could not be determined because the “attached cultivation bioreactors” in our previous studies algal filaments could not be completely separated from (Cheng et al. 2013; Liu et al. 2013), consisted of the same the cellulose of the filter paper. Therefore, the pigments “single-layer plate” system with different medium- per sample were determined. The cells and the filter supplying modes. In the first type of reactor, the medium paper were sampled together and soaked in 5 mL J Appl Phycol + Microbial Sci. & Tech. Co., Ltd., China). The NH4 –Nin filter paper was washed off with 5 mL of hydrochloric acid −1 + solution (1 mol L ), and then the concentration of NH4 –N (CN) was determined. The amount of water in the same filter paper was calculated from the difference between the weight before (Wo) and after (Wd) being dried at 105 °C for 2.5 h. The + −1 concentration of NH4 –N(gL ) in filter paper was calculated as follows: ÀÁ þ −1 NH4 –NgL ¼ CN Ã 5=ðÞW o−W d ð4Þ Analyses of pigments The pigments were extracted with DMSO, and absorbance was measured using a Varian 50 Bio UV-Visible spectropho- tometer (Varian Inc., USA). The chlorophyll and total carot- Fig. 1 The schematic diagrams of three photo-bioreactors.
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