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Description and Application of a Marine Microalga Auxenochlorella Protothecoides Isolated from Ulleung-Do

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Description and Application of a Marine Microalga Auxenochlorella Protothecoides Isolated from Ulleung-Do ISSN (Print) 1225-9918 ISSN (Online) 2287-3406 Journal of Life Science 2017 Vol. 27. No. 10. 1152~1160 DOI : https://doi.org/10.5352/JLS.2017.27.10.1152 Description and Application of a Marine Microalga Auxenochlorella protothecoides Isolated from Ulleung-do Hyeong Seok Jang1, Nam Seon Kang2, Kyeong Mi Kim1, Byung Hee Jeon1, Joon Sang Park1 and Ji Won Hong1* 1Department of Taxonomy and Systematics, National Marine Biodiversity Institute of Korea, Seocheon 33662, Korea 2Marine Life-resources Management Department, National Marine Biodiversity Institute of Korea, Seocheon 33662, Korea Received July 26, 2017 /Revised September 8, 2017 /Accepted September 9, 2017 A unicellular green alga was axenically isolated from a tidal pool on Ulleung-do, Korea. Morphological, molecular, and biochemical analyses revealed that the isolate belonged to Auxenochlorella protothecoides. The current study is the first record of this species in Korea. The microalgal strain was named as A. protothecoides MM0011 and its growth, lipid and pigment compositions, and biomass properties were investigated. The strain is able to thrive in a wide range of temperatures (5~35°C) and to withstand up to 1.5 M NaCl. The results of GC/MS analysis showed that the isolate was rich in nutritionally important polyunsaturated fatty acids (PUFAs). Its major fatty acids were linoleic acid (27.6%) and α -linolenic acid (39.6%). Thus, this indigenous microalga has potential as an alternative source of ω3 and ω6 PUFAs, which currently come from fish and plant oils. Also, the HPLC analysis revealed that the value-added antioxidant, lutein, was biosynthesized as the accessory pigments by the microalga. A proximate analysis showed that the volatile matter content was 85.6% and an ultimate analysis in- dicated that the gross calorific value was 20.3 MJ kg-1. Since 40.5% of total nitrogen and 27.9% of total phosphorus were removed from the medium, respectively, it also has potential as a feedstock for bio- fuel applications which could be coupled to wastewater treatment. In addition, the biomass may also serve as an excellent animal feed because of its high protein content (51.4%). Therefore, A. proto- thecoides MM0011 shows promise for application in production of microalgae-based biochemicals and as a biomass feedstock. Key words : Auxenochlorella protothecoides, first record, lutein, PUFAs, Ulleung-do Introduction cordingly many studies have focused on the assessment of their biotechnological potential [4, 25, 32]. Green microalgae (Chlorophyta) are photosynthetic mi- In this study, we have isolated and identified a unicellular croorganisms that can be found in every conceivable aquatic microalga A. protothecoides MM0011 from a tidal pool on habitat from seawater to freshwater. Marine microalgae are Ulleung-do, Ullenug-gun, Gyeonsangbuk-do, Korea. Auxeno- known to play indispensable roles in global carbon, nitro- chlorella was ranked as a subgenus of Chlorella in 1965 [28], gen, and phosphorus cycles as the major primary producers then it was upgraded to the genus rank based on physio- in the maritime ecosystem [1, 6, 11]. Since they are capable logical and biochemical characteristics by Kalina and of taking up water (H2O) and carbon dioxide (CO2) and con- Punčochářová in 1987 [12]. It was reported that A. proto- verting them into a variety of energy-rich organic com- thecoides was isolated from the sap secreted from Populus and pounds such as lipids, hydrocarbons, carbohydrates, and Ulmus trees in Germany [8, 30]. It was also found in munici- other valuable compounds via photosynthesis [7, 15, 20], mi- pal wastewater in Minnesota, USA [18]. Due to the fast cell croalgae have recently received considerable interest and ac- growth and high lipid content of A. protothecoides, a number of heterotrophic cultivation researches have been carried out *Corresponding author to produce biodiesel by sequestering CO2 [5, 10, 38, 42, 43]. *Tel : +82-41-950-0743, Fax : +82-41-950-0727 In addition, many previous studies have also shown that *E-mail : [email protected] A. protothecoides was able to produce relatively high concen- This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License tration of lutein when grown under heterotrophic conditions (http://creativecommons.org/licenses/by-nc/3.0) which permits [26, 27, 29, 34, 39]. unrestricted non-commercial use, distribution, and reproduction The present report provides information on the first re- in any medium, provided the original work is properly cited. Journal of Life Science 2017, Vol. 27. No. 10 1153 cord of the species in Korea and its morphological, molec- observed with a field emission scanning electron microscopy ular, and chemotaxonomic features were investigated. (FE-SEM, SUPRA 55VP, Carl Zeiss, Jena, Germany). For transmission electron microscopy (TEM), cells were Materials and Methods transferred to a 10 ml tube and fixed in 2.5%(v/v) gluta- raldehyde (final concentrations) for 2 hr, the contents of the Sample collection and isolation tube were placed in a 10 ml centrifuge tube and concentrated Seawater samples were collected in April 2016 from a ti- at 1,610 g for 10 min in a Vision Centrifuge VS-5500 (Vision, dal pool near Turtle Rock (37° 27’ 35.86’’N, 130° 51’ 23.49”E) Bucheon, Korea). The resulting pellet was subsequently on Ulleung-do, Seo-myeon, Ullenug-gun, Gyeonsangbuk-do, transferred to a 1.5 ml tube and rinsed in 0.2 M sodium Korea. Samples were then transported to the laboratory and cacodylate buffer (Electron Microscopy Sciences, Hatfield, 1 ml of each sample was inoculated into 100 ml BG-11 me- PA, USA) at pH 7.4. After several rinses in 0.2 M sodium dium [21]. The broad-spectrum antibiotics chloramphenicol cacodylate buffer, cells were post-fixed for 90 min in 1% (Sigma-Aldrich, St. Louis, MO, USA) and imipenem (JW (w/v) OsO4 in deionized H2O. The pellet was then em- Pharmaceutical, Seoul, Korea) were added to the medium bedded in agar. Dehydration was performed in a graded at a concentration of 100 µg ml-1, respectively in order to ethanol series (50, 60, 70, 80, 90, and 100% ethanol, followed prevent bacterial growth. The flasks were incubated in a stat- by two changes in 100% ethanol). The material was em- ic condition at 25℃ under cool fluorescent light (approxim- bedded in Spurr’s resin (Electron Microscopy Sciences, ately 40 μmole m-2 s-1) in a light:dark cycle (16:8 hr) until Hatfield, PA, USA). Sections were prepared on an EM UC7 algal growth was apparent. Well-grown algal cultures (1.5 ultramicrotome (Leica, Wetzlar, Germany) and stained with ml) were centrifuged at 3,000× g for 3 min to harvest algal 3%(w/v) aqueous uranyl acetate (Electron Microscopy Sci- biomass. The resulting pellets were streaked onto R2A agar ences, Hatfield, PA, USA) followed by lead citrate (Electron (Becton, Dickinson and Company, Sparks, MD, USA) sup- Microscopy Sciences, Hatfield, PA, USA). The sections were plemented with imipenem (20 μg ml-1) and incubated under visualized on an H-7650 TEM (Hitachi, Tokyo, Japan) using the aforementioned conditions. A single colony was then a voltage of 100 kV. aseptically restreaked onto a fresh R2A agar plate to obtain an axenic culture. Molecular identification For molecular analysis, genomic DNA was extracted us- Morphological identification ing a DNeasy Plant Mini kit (Qiagen, Hilden, Germany). The The isolate was grown in R2A medium for 8 days. Live universal primers NS1/NS8 and ITS1/ITS4 described by cells were harvested by centrifugation at 3,000× g for 3 min, White et al. [35] were used to amplify the 18S rRNA se- washed three times with sterile distilled H2O, and examined quence and internal transcribed spacer (ITS) region, at 1,000× magnification under a Zeiss Axio Imager.A2 light respectively. Phylogenetic analysis was performed with the microscope (Carl Zeiss, Göttingen, Germany). For scanning 18S rRNA sequence of strain MM0011 using the software electron microscopy (SEM), 10 ml aliquots of cultures at ap- package MEGA ver. 6.0 [33]. Its closely related Auxenochlorella proximately 1,000 cells ml-1 were fixed for 10 min in osmium and Chlorella sequences were downloaded and aligned in the tetroxide (OsO4, Electron Microscopy Sciences, Hatfield, PA, MEGA software, with the ClustalW tool. The best-fit nucleo- USA) at a final concentration of 2%(v/v). The fixed cells tide substitution model (Kimura 2-parameter) was selected were collected on a 3 µm pore size, polycarbonate membrane using MEGA 6.0 based on the Bayesian information criterion. filter (Whatman, Kent, UK) and washed three times with This model was used to build a maximum likelihood (ML) distilled H2O to remove residual media components. The phylogenetic tree with 1,000 bootstrap replicates. Due to the membranes were dehydrated in an ethanol series (Merck, highly conserved nature of rRNA, the region RuBisCO rbcL Darmstadt, Germany) and immediately dried using an auto- was also amplified with primers, rbcL 7F and rbcL 1391R, mated critical point dryer (EM CPD300, Leica, Wetzlar, described by Verbruggen et al. [37]. All analyses were car- Germany). The dried filters were mounted on a stub and ried out in triplicate, unless otherwise stated. DNA se- coated with gold-palladium in a low vacuum coater (EM quences obtained in this study were deposited in the data- ACE200, Leica, Wetzlar, Germany). Surface morphology was base of the National Center for Biotechnology Information 1154 생명과학회지 2017, Vol. 27. No. 10 under accession numbers MF040300, MF040301, and veloped by Zapata et al. [41]. Briefly, 1 mg of freeze-dried MF043910 (Table 2). biomass was extracted in 90% HPLC grade acetone (Dae- jung, Siheung, Korea) and filtered through a Whatman PTFE Temperature and NaCl tolerance testing syringe filter with a pore size of 0.2 μm (Florham Park, NJ, Routine serial subculturing on R2A agar slant was per- USA) before injection.
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