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Submitted by ADEPU KIRAN KUMAR for the Award of the Degree of INDIAN INSTITUTE of TECHNOLOGY GUWAHATI CHARACTERISTICS and APPLIC

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Submitted by ADEPU KIRAN KUMAR for the Award of the Degree of INDIAN INSTITUTE of TECHNOLOGY GUWAHATI CHARACTERISTICS and APPLIC CHARACTERISTICS AND AP PLICATION POTENTIAL OF AN ALCOHOL OXIDASE FR OM THE HYDROCARBON - DEGRADING FUNGUS A SPERGILLUS TERREUS A THESIS submitted by ADEPU KIRAN KUMAR for the award of the degree of DOCTOR OF PHILOSOPHY DEPARTMENT OF BIOTECHNOLOGY INDIAN INSTITUTE OF TECHNOLOGY GUWAHATI JANUARY 2009 Dedicated to my Beloved Parents & Puchyadal TH-770_05610605 Department of Biotechnology INDIAN INSTITUTE OF TECHNOLOGY GUWAHATI STATEMENT I do hereby declare that the matter embodied in this thesis is the result of investigations carried out by me in the Department of Biotechnology, Indian Institute of Technology Guwahati, India, under the guidance of Dr. Pranab Goswami. In keeping with the general practice of reporting scientific observations, due acknowledgements have been made wherever the work described is based on the findings of other investigators. January, 2009. Adepu Kiran Kumar TH-770_05610605 DEPARTMENT OF BIOTECHNOLOGY Indian Institute of Technology Guwahati Guwahati 781 039, Assam, INDIA Tel: +91-(0)361 2582202 Dr. Pranab Goswami Fax: +91-(0)361 2582249/2690762 Email: [email protected] Associate Professor & Head CERTIFICATE This is to certify that the thesis/dissertation entitled “Characteristics and application potential of an alcohol oxidase from the hydrocarbon-degrading fungus Aspergillus terreus”, that is being submitted by Mr. Adepu Kiran Kumar for the award of degree of Doctor of Philosophy is an authentic record of the results obtained from the research work carried out under my supervision in the Department of Biotechnology, Indian Institute of Technology Guwahati, India. The results embodied in this thesis have not been submitted to any other University or Institute for the award of any degree. January, 2009. Dr. Pranab Goswami Associate Professor (Research Supervisor) TH-770_05610605 ACKNOWLEDGEMENTS The thesis is ready… I look at this manuscript wondering how I managed to squeeze the last four years into 130 pages of text and figures. But then I look more carefully and I see all of what is written in between the lines. All the discussions we had, coffee (and dinner) breaks, games, “gossiping”, group meetings, alcheringa, techniche, & manthan events but also my visits to the lab when all the others were sleeping, enjoying in the rain, little frustrations caused for instance during protein purifications that, for unknown reason, did not work for weeks, etc. All of it is an integral part of this thesis. The thesis is ready… I am filled with pride but at the same time I realize it would not be possible without the help of many people. It is now the time to acknowledge you all. First my guide, Dr. Pranab Goswami, I would like to thank him for giving me the opportunity to perform research in his lab and for all the support I got from him over these years. He showed me the guidelines I hope to follow in the future. Several people deserve special acknowledgements. Dr. Ghosh, Dr. Bora and Dr. Khijwania I thank for endless discussions, critical evaluations and all the support they gave me. I would like to thank Ms. Preety Vatsyayan, for her support and useful discussions in designing several critical experiments. I would like to mention all the members of my research group, those who shared every small events: Shiva, Preety, Gopi, Lepakshi, Vishnu, Raju, the friendly atmosphere created in the lab and also in the hostel compensated for the separation with my family and friends. They all inspired me to become a Ph.D. student in this group. Also, colleagues that joined the group later: Naresh, Urmila, Seraj, Asim, and Vinod, each of them contributed to the fact that I felt really well in the group and they were always there to help. Thank you all. Our wonderful non-teaching staff members: Nurul, Anitha and Sharan, I would like to acknowledge their inestimable help in administrative works I had to go through during all these years. My brothers, Nagraj (toppanagulu) and Rajesh, friends Shiva and Preety, the preparations for the seminars would be very difficult without them. Also, I would like to mention people without whom my life in the Guwahati would not be the same, Vijay Raj, Dr. Gopi, Dr. Ramaraju, Dr. Veerababu, they have been great friends. I would not get to this point without the support of my best friends, Raghavendra and Srilatha. It is a great honor to have in my life. Finally my beloved Parents, I thank for their patience and encouragement all the time. I am grateful for all the support and kindness I received from them. Adepu Kiran Kumar January 2009 TH-770_05610605 i ABSTRACT A hydrocarbon-degrading Aspergillus terreus was isolated from the oil contaminated soil. The organism could degrade a wide range of petroleum hydrocarbons including the immediate oxidation products of hydrocarbons, like alkanols and alkanals. Among all the linear chain carbon substrates, highest growth of 39 ± 4 g l−1 (wet weight) was observed when n-hexadecane was used as the sole source of carbon and energy. Using SEM the morphological change of the hyphae during growth of the fungi on hydrocarbon substrates was demonstrated. In glucose- grown cells the hyphae were smooth with a thick cell wall, whereas, the cell wall of the n-hexadecane cells was uneven and thin. The adaptation of the cells for up taking the hydrophobic hydrocarbon substrates through sorption mechanism and accumulation of high lipid content in the cells, as evident from the nearly seven-fold more lipid production (4.4 g%) in the n-hexadecane-grown cells than the glucose- grown cells (0.62 g%), were attributed to the observed morphological change. Analyses of the fatty acid profile by ESI/MS in the isolated lipid showed that nine different fatty acids induced in the hexadecane-grown cells were void in the glucose- grown cells. The oleic acid and palmitic acid were the fatty acids with highest peak intensity in the spectral profile corresponding to the glucose-grown cells and hexadecane-grown cells, respectively. It was revealed by analyzing the percentage distribution of different fatty acids in each cell type that palmitic and stearic acids were the predominant fatty acids in the hexadecane-grown cells; whereas, oleic and linoleic acids were the predominant fatty acids observed in the glucose-grown cells. Unlike glucose-grown cells, considerably high amount of fatty acids with chain length C32 and C33 were present in n-hexadecane-grown cells and each accounted nearly 9% (based on peak intensity) of the total fatty acid content in the cells. A microsomal membrane bound alcohol oxidase enzyme was isolated from this fungus during its growth on n-hexadecane substrate. This oxidase could oxidize short chain alcohol-, TH-770_05610605 long chain alcohol-, secondary alcohol-, and aryl alcohol- substrates and was localized in the microsomes of the cell. The optimal pH and temperature of the enzyme were found to be 8.1 ± 0.5 and 27-33 oC, respectively. The stability of the alcohol oxidase was drastically decreased beyond 30 oC. The enzyme showed 33% enantiomeric excess for the R(-)2-octanol over S(+)2-octanol, which may be correlated with the lower Km values of the enzyme for the R(-)2-octanol than the S(+)2-octanol. The fluorescence emission spectrum of the protein (at 443 nm excitation) was similar to that obtained with authentic FAD. In this flavoenzyme, flavin was non-covalently but avidly associated. The native protein molecular mass was 269 ± 5kDa and the subunit molecular masses were 85-, 63-, 43-, 27-, and 13- kDa. The enzyme showed highest affinity for n-heptanol (Km = 0.498 mM, Kcat = 2.7 x 102 s-1). The isoelectric point of the proteins was within 8.3-8.5. High aggregating property of the protein was demonstrated by AFM, DLS and TEM analyses. Chemical analysis showed the presence of oleic acid and palmitic acid at a ratio of 2:1 in the purified protein. The high aggregating property of the alcohol oxidase may be correlated with the observed lipoidic nature of these protein particles. Peptide mass fingerprinting studies showed the presence of two FAD binding domains in 63kDa protein. Among these two FAD binding domain sequences only the YPVIDHEYDAVVVGAGGAGLR peptide shows 45-50% sequence similarity with the reported N-terminal sequences of other known alcohol oxidases. Non-redundant database search of 63- and 43-kDa subunits peptide sequences showed no sequence similarity with the other alcohol oxidase protein reported till now. The aggregated multimeric alcohol oxidase protein when treated with β-mercaptoethanol (β-ME) at an optimum concentration of 0.74M for 8 h at 4 oC, the protein was dissociated to subunit level and also nearly 87% of the total flavin present in the native protein was simultaneously separated. This dissociation process had traversed through two intermediate protein (IP) stages, IP1 and IP2, which were associated with the FAD. The IP1 (size 10 nm) that contained the subunits 85-, 63-, 43-, 25-, 13-kDa was functionally active, whereas, the IP2 (size 9 nm) that contained 85-, 63-, 25-, 13-kDa was inactive, which indicates the critical role of the 43kDa protein for the alcohol oxidase activity. A functionally inactive reconstituted apoprotein (PR) with molecular mass and subunits similar to IP1 was generated upon removal of β-ME from the subunit level dissociated proteins. The PR when mixed with FAD and incubated TH-770_05610605 iii prolong with substrate (minimum 12 hr), a catalytically active PR was formed and is evident from the protein conformational change (at 280 nm) and FAD emission quenching (at 525 nm) studies. The solvent effect caused by the high concentration of β-ME is attributed to the observed dissociation and associated deflavination of these multimeric alcohol oxidase protein particles. The alcohol oxidase protein reported here was demonstrated as a green catalyst in several oxidation reactions due to its catalytic activity for high molar yield conversions of broad range of alcohols to the corresponding carbonyl compounds under room temperature, atmospheric pressure and aqueous environment.
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