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A Cellulase and Lipase Producing Oleaginous Yeast ⇑ Sachin Vyas, Meenu Chhabra

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A Cellulase and Lipase Producing Oleaginous Yeast ⇑ Sachin Vyas, Meenu Chhabra Bioresource Technology 223 (2017) 250–258 Contents lists available at ScienceDirect Bioresource Technology journal homepage: www.elsevier.com/locate/biortech Isolation, identification and characterization of Cystobasidium oligophagum JRC1: A cellulase and lipase producing oleaginous yeast ⇑ Sachin Vyas, Meenu Chhabra Environmental Biotechnology Laboratory, Department of Biology, Indian Institute of Technology Jodhpur (IIT J), Jodhpur, Rajasthan 342011, India highlights graphical abstract Oleaginous yeast capable of cellulase and lipase production was isolated. It can grow on wide range of substrates including carboxylmethylcellulose (CMC). It can accumulate 36.46% (w/w) lipid on the medium with CMC as sole carbon source. Intracellular and extracellular lipase activity: 2.16 and 2.88 IU/mg respectively. The FAME composition suitable for use as biodiesel (glucose medium). article info abstract Article history: Oleaginous yeast closely related to Cystobasidium oligophagum was isolated from soil rich in cellulosic Received 15 August 2016 waste. The yeast was isolated based on its ability to accumulate intracellular lipid, grow on car- Received in revised form 12 October 2016 boxymethylcellulose (CMC) and produce lipase. It could accumulate up to 39.44% lipid in a glucose med- Accepted 13 October 2016 ium (12.45 ± 0.97 g/l biomass production). It was able to grow and accumulate lipids (36.46%) in the Available online 15 October 2016 medium containing CMC as the sole carbon source. The specific enzyme activities obtained for endoglu- canase, exoglucanase, and b-glucosidase were 2.27, 1.26, and 0.98 IU/mg respectively. The specific Keywords: enzyme activities obtained for intracellular and extracellular lipase were 2.16 and 2.88 IU/mg respec- Cystobasidium oligophagum tively. It could grow and accumulate lipids in substrates including glycerol (42.04%), starch (41.54%), Rhodotorula oligophaga Oleaginous yeast xylose (36.24%), maltose (26.31%), fructose (24.29%), lactose (21.91%) and sucrose (21.72%). The lipid pro- Cellulase file of the organism was suitable for obtaining biodiesel with desirable fuel properties. Cellulolytic yeast Ó 2016 Elsevier Ltd. All rights reserved. Lipase FAME 1. Introduction sustainable biofuels for the future (Li et al., 2008). The photoau- totrophic nature of algae is an obvious advantage, however, the A continuous increase in the population and demands for the slower growth rates and lower lipid productivity is still a challenge transportation fuel has urged the scientists across the globe to find for algal biofuels commercialization. Yeast, on the other hand, alternative fuel resources, of which the biomass derived fuels holds exhibit faster growth rate, high lipid productivity, can grow inde- the special place (Sitepu et al., 2014). Microbes such as algae and pendent of the climate condition and at low pH value which natu- yeasts have been extensively studied for their ability to provide rally suppresses the growth of many bacteria. Other useful characteristics of the yeast are the ability to grow on the wide range of waste substrates, lesser space requirements and easy ⇑ Corresponding author. genetic modification (Li et al., 2008; Sitepu et al., 2014). Yeasts like E-mail address: [email protected] (M. Chhabra). http://dx.doi.org/10.1016/j.biortech.2016.10.039 0960-8524/Ó 2016 Elsevier Ltd. All rights reserved. S. Vyas, M. Chhabra / Bioresource Technology 223 (2017) 250–258 251 Yarrowia lipolytia, Lipomyces starkeyi, Rhodotorula glutinis, etc., for TLC, p-nitrophenyl-b-D-glucopyranoside (pNPG), tributyrin and which can accumulate cellular lipids more than 20 percent of their vitamins were purchased from Hi-media Laboratories, India. The dry cell weight (DCW) (or biomass production) are known as PCR primers, FAME standard (for GC–MS analysis) and other chem- oleaginous yeasts (Ratledge, 2004). Oleaginous yeasts have been icals [i.e. Methanolic BF3, p-nitrophenyl palmitate (pNPP), etc.] extensively studied for biodiesel production in the past few years. were purchased from Sigma-Aldrich. Yeasts primarily accumulate lipids in the form of triacylglycerol (TAG), comprising of saturated and unsaturated chains of fatty 2.2. Isolation and screening of oleaginous yeast strain acids. However, biodiesel production from yeasts is also equally challenging since these are heterotrophic organisms and rely on The soil samples rich in cellulosic wastes such as decaying an external supply of organic carbon sources. leaves, vegetable wastes etc., were collected from the five different 0 00 Cellulose, a linear chain polymer of D-glucose attached by regions around the local area, Jodhpur (coordinates: 26°16 18.2 N, b-(1,4)-glycosidic bonds, is the most abundant carbohydrate in 73°01059.200E). Samples were collected in the sterile tubes and the world (Van Soest, 1982). Unlike starch, the cellulose is not a stored at 4 °C until further use. One gram of the homogenized sam- source of the nutrition for most of the higher level organisms; ple was aseptically suspended in 100 ml of the sterilized saline making it a sustainable raw material for biofuel production. Vari- solution (0.85% w/v NaCl). 1 ml of the dilution obtained was trans- ous oleaginous yeasts of the genera like Rhodotorula, Cryptococcus, ferred into 250 ml Erlenmeyer flask containing 100 ml of YPD med- Yarrowia, Lipomyces, Rhodosporidium, are recently reported to accu- ium (g/l): yeast extract, 10; peptone, 20; glucose, 10; and mulate higher amount of lipids on the pre-treated lignocellulosic incubated at 30 °C and 120 rpm (pH 6.0). Ampicillin (100 lg/ml) substrates, low cost agro-industrial waste (paper mill, crude glyc- was used to avoid the bacterial growth. Around 139 yeast colonies erol), and other renewable feedstocks such as animal fat, municipal were isolated on YPD agar supplemented with ampicillin. The iso- solid waste, etc., (Leiva-Candia et al., 2014). An enzymatic pre- lates obtained were further plated on the lipid production medium treatment of cellulosic biomass to release utilizable hexose and (g/l): Glucose, 40; KH2PO4, 7; NaH2PO4, 2; (NH4)2SO4,2; pentose sugars normally precedes the oil production step by MgSO4Á7H2O, 1.5; yeast extract, 1; agar powder, 20. Vitamins yeasts. Fewer reports discuss the lipid accumulation directly on (mg/l): D-biotin, 0.002; calcium pantothenate, 0.4; folic acid, the cellulosic substrate. Consolidated Bioprocessing (CBP) for the 0.002; inositol, 2; niacin, 0.4; para-aminobenzoic acid (PABA), accumulation of lipids from cellulosic materials without the use 0.2; pyridoxine HCl, 0.4; riboflavin, 0.2; thiamine, 0.4, at 30 °C of additional cellulase enzymes will be a very advantageous (pH 5.5). The yeast colonies growing on lipid production medium (Lynd et al., 2005). There are many fungi as well as bacteria, which were further screened for lipid accumulation using the nile red flu- are reported to be the excellent cellulase producers; limited stud- orescence microscopy protocol as described in the subsequent sec- ies are reported however for cellulolytic yeasts. Cellulose utiliza- tions. The yeast colonies which were showing significant lipid tion involves multi-enzyme complex consisting of three major droplets inside the cells were further grown in the production enzymes (i) endo-1,4 b-D-glucanase (or CMCase) (ii) cellobiohydro- medium described later, and the lipid outputs were determined. lase (or exoglucanase) and (iii) b-glucosidase. Certain genera of the yeast such as Rhodotorula, Cryptococcus, Candida, Sporobolomyces, 2.3. Screening of oleaginous yeasts for cellulase activity and Aureobasdium are reported to be the producer of different types of cellulases (Baldrian and Vendula, 2008; Strauss et al., The oleaginous yeasts obtained from the above step were cul- 2001). So far there is only one report on the oleaginous yeast accu- tured in the medium (g/l): CMC, 10; yeast extract, 0.6; KH2PO4, mulating lipids using carboxymethylcellulose (CMC) as a carbon 7; K2HPO4, 2; MgSO4 7H2O, 0.1; (NH4)2SO4, 1, agar 20 (pH 6.0) source (Kanti and sudiana, 2015) to the best of our knowledge. (Goldbeck et al., 2012), and incubated at 30 °C. The colonies which However, a systematic and quantitative estimation of cellulolytic showed growth were replica plated. Extracellular cellulase enzyme activity along with lipid accumulation is missing in the majority activity was confirmed using 0.2% congo red dye method (Teather of these studies. and Wood, 1982). In addition to the use of the cellulosic substrate, we wanted the same yeast to produce lipase, a potential transesterification cata- 2.4. Screening of selected yeasts for lipase activity lyst. Lipase holds a special interest in next generation biodiesel synthesis. Studies are underway to design efficient lipases and uti- The yeast cultures which were found to be oleaginous, and lize them for transesterification instead of conventional catalysts expressing cellulolytic activity, were further tested for lipase activ- to produce biodiesel (Aguieiras et al., 2015). ity. The lipase activity was detected by qualitative plate assay A successful attempt to isolate oleaginous cellulolytic yeast using tributyrin as a lipid source. The selected yeast cultures were with both intracellular and extracellular lipase activity was made. allowed to grow on plates containing (g/l): tributyrin, 10; peptone, The isolation of the yeast was followed by its identification, char- 5; yeast extract, 3; agar, 20, pH 6.0 (Sztajer et al., 1988), and incu- acterization and lipid profiling. Isolation of such an organism opens bated at 30 °C. The expression of lipase enzyme was confirmed by a up the possibility of intracellular FAEE (fatty acid ethyl ester) syn- zone of clearance around the colony. thesis directly by few more experimental interventions. This study thus opens up the new prospect of utilization of cellulosic or indus- 2.5. Identification and characterization of the yeast strain trial wastes directly for the production of biodiesel with desirable fuel properties. Identification of the selected yeast strain was performed by determining partial 18S rRNA gene sequence. Total DNA was extracted using yeast genomic DNA isolation kit (Himedia labora- 2.
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