Elucidating The Lignocellulose Digestion Mechanism Coptotermes curvignathus Based on Carbohydrate-Active Enzymes Profle Using The Meta-Transcriptomic Approach
Keywords:
Lignocellulose degradation;, RNA sequencing;, termite gut;, wood-feeding termiteAbstract
Termites are efficient lignocellulose decomposers that thrive on woody materials and contribute to carbon mineralization in both tropical and subtropical regions. Due to hydrolytic stability and crosslinking between the polysaccharides (cellulose & hemicellulose) and the lignin via ester and ether linkages, termites would require a large variety of enzymes to degrade lignocellulose. Coptotermes curvignathus, an endemic species of termite from Southeast Asia, has been classified as an urban pest in the region and is known as the largest and most aggressive among the oriental Coptotermes spp. Its Carbohydrate-Active enzymes (CAZymes) are the main interest of this study. RNA of C. curvignathus was extracted and sequenced using Illumina Hiseq 2000 sequencing platform, and de novo assembled with Trinity pipeline. There were 101 CAZymes families in C. curvignathus digestome. CAZymes break down complex carbohydrates and glycoconjugates for a large body of biological roles and perform their function, usually with high specificity. Enzymes coding for glycosyl hydrolase (GH) families had the highest transcript abundance, accounting for about 93% of the total CAZymes reads. This was followed by CBM (≈1%), GT family (≈4%), CE family (<1%), AA family (<2%), and PL family (<1%). Due to the carbohydrate diversity exceeding the number of protein folds, CAZymes have evolved from a limited number of progenitors by acquiring novel specificities at substrate and product levels. Such a dizzying array of substrates and enzymes makes C. curvignathus a high-performance lignocellulose degrader.
Downloads
Metrics
References
Agger, J., Viksø-Nielsen, A. & Meyer, A.S. 2010. Enzymatic xylose release from pretreated corn bran arabinoxylan: Differential effects of deacetylation and deferuloylation on insoluble and soluble substrate fractions. Journal of Agricultural and Food Chemistry, 58(10): 6141-6148. DOI: https://doi.org/10.1021/jf100633f
Baumann, M.J., Eklöf, J.M., Michel, G., Kallas, A.M., Teeri, T.T., Czjzek, M. & Brumer, H. 2007. Structural evidence for the evolution of xyloglucanase activity from xyloglucan endo-transglycosylases: Biological implications for cell wall metabolism. The Plant Cell, 19(6): 1947-1963. DOI: https://doi.org/10.1105/tpc.107.051391
Beaugrand, J., Chambat, G., Wong, V.W., Goubet, F., Rémond, C., Paës, G., Benamrouche, S., Debeire, P., O’Donohue, M. & Chabbert, B. 2004. Impact and efficiency of GH10 and GH11 thermostable endoxylanases on wheat bran and alkali-extractable arabinoxylans. Carbohydrate Research, 339(15): 2529-2540. DOI: https://doi.org/10.1016/j.carres.2004.08.012
Bray, N.L., Pimentel, H., Melsted, P. & Pachter, L. 2016. Near-optimal probabilistic RNA-seq quantification. Nature Biotechnology, 34: 525-527. DOI: https://doi.org/10.1038/nbt.3519
Brennan, Y., Callen, W.N., Christoffersen, L., Dupree, P., Goubet, F., Healey, S., Hernández, M., Keller, M., Li, K., Palackal, N., Sittenfeld, A., Tamayo, G., Wells, S., Hazlewood, G.P., Mathur, E.J., Short, J.M., Robertson, D.E. & Steer, B.A. 2004. Unusual microbial xylanases from insects guts. Applied and Environmental Microbiology, 70(6): 3609-3617. DOI: https://doi.org/10.1128/AEM.70.6.3609-3617.2004
Busk, P.K. & Lange, L. 2013. Function-based classification of carbohydrate-active enzymes by recognition of short, conserved peptide motifs. Applied and Environmental Microbiology, 79(11): 3380-3391. DOI: https://doi.org/10.1128/AEM.03803-12
Chan, S.P., Bong, C.F.J. & Lau, W.H. 2011. Damage pattern and nesting characteristic of Coptotermes curvignathus (Isoptera: Rhinotermitidae) in oil palm on peat. American Journal of Applied Science, 8(5): 420-427. DOI: https://doi.org/10.3844/ajassp.2011.420.427
Chandra, R.P., Bura, R., Mabee, W.E., Berlin, A., Pan, X. & Saddler, J.N. 2007. Substrate pretreatment: the key to effective enzymatic hydrolysis of lignocellulosics? Advances in Biochemical Engineering/Biotechnology, 108: 67-93. DOI: https://doi.org/10.1007/10_2007_064
Davies, G.J. & Sinnott, M.L. 2008. Sorting the diverse: The sequence-based classifications of carbohydrate-active enzymes. Biochemical Journal, 30(4): 26-32. DOI: https://doi.org/10.1042/BIO03004026
Drula, E., Garron, M.L., Dogan, S., Lombard, V., Henrissat, B. & Terrapon, N. 2022. The carbohydrate-active enzyme database: functions and literature. Nucleic Acid Research, 50(D1): D571-D577. DOI: https://doi.org/10.1093/nar/gkab1045
Fujita, A., Hojo, M., Aoyagi, T., Hayashi, Y., Arakawa, G., Tokuda, G. & Watanabe, H. 2010. Details of the digestive system in the midgut of Coptotermes formosanus Shiraki. Journal of Wood Science, 56: 222-226. DOI: https://doi.org/10.1007/s10086-009-1088-3
Geng, A., Cheng, Y., Wang, Y., Zhu, D., Le, Y., Xie, R., Yuan, J.S. & Sun, J.Z. 2018. Transcriptome analysis of the digestive system of a wood-feeding termite (Coptotermes formosanus) revealed a unique mechanism for effective biomass degradation. Biotechnology for Biofuels, 11:24. DOI: https://doi.org/10.1186/s13068-018-1015-1
Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, X., Fan, L., Raychowdhury R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F, Birren, B.W., Nusbaum, C., Lindblad-Toh, K., Friedman, N. & Regev, A. 2011. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nature Biotechnology, 29(7): 644-652. DOI: https://doi.org/10.1038/nbt.1883
Hoe, P.K., King, J.H.P., Ong, K.H., Bong, C.F.J. & Nor Muhammad, M. 2019. Laccases repertoire of a subterranean termite Coptotermes curvignathus Holmgren (Blattodea: Rhinotermitidae). Serangga, 24(2): 169-197.
Honda, Y. & Kitaoka, M. 2004. A family 8 glycoside hydrolase from Bacillus halodurans C-125 (BH2105) is a reducing end xylose-releasing oligoxylanase. The Journal of Biological Chemistry, 279(53): 55097-55103. DOI: https://doi.org/10.1074/jbc.M409832200
Hu, J. & Saddler, J.N. 2018. Why does GH10 xylanase have better performance than GH11 xylanase for the deconstruction of pretreated biomass? Biomass and Bioenergy, 110: 13-16. DOI: https://doi.org/10.1016/j.biombioe.2018.01.007
Ke, J., Laskar, D.D., Singh, D. & Chen, S. 2011. In situ lignocellulosic unlocking mechanism for carbohydrate hydrolysis in termites: Crucial lignin modification. Biotechnology for Biofuels, 4: 17. DOI: https://doi.org/10.1186/1754-6834-4-17
Ke, J., Laskar, D.D., Gao, D. & Chen, S. 2012. Advanced biorefinery in lower termite-effect of combined pretreatment during the chewing process. Biotechnology for Biofuels, 5(1): 11. DOI: https://doi.org/10.1186/1754-6834-5-11
Li, B. & Dewey, C.N. 2011. RSEM: Accurate transcript quantification from RNA-seq data with or without reference genome. BMC Bioinformatics, 12: 323. DOI: https://doi.org/10.1186/1471-2105-12-323
Merino, S.T. & Cherry, J. 2007. Progress and challenges in enzyme development for biomass utilization. Advances in Biochemical Engineering/Biotechnology, 108: 95-120. DOI: https://doi.org/10.1007/10_2007_066
Ni, J. & Tokuda, G. 2013. Lignocellulose-degrading enzymes from termites and their symbiotic microbiota. Biotechnology Advances, 31(6): 838-850. DOI: https://doi.org/10.1016/j.biotechadv.2013.04.005
O’Leary, N.A., Wright, M.W., Brister, J.R., Ciufo, S., Haddad, D., McVeigh, R., Rajput, B., Robbertse, B., Smith-White, B., Ako-Adjei, D., Astashyn, A., Badretdin, A., Bao, Y., Blinkova, O., Brover, V., Chetvernin, V., Choi, J., Cox, E., Ermolaeva, O., Farrell, C.M., Goldfarb, T., Gupta, T., Haft, D., Hatcher, E., Hlavina, W., Joardar, V.S., Kodali, V.K., Li, W., Maglott, D., Masterson, P., McGarvey, K.M., Murphy, M.R., O’Neilli, K., Pujar, S., Rangwala, S.H., Rausch, D., Riddick, L.D., Schoch, C., Shkeda, A., Storz, S.S., Sun, H., Thibaud-Nissen, F., Tolstoy, I., Tully, R.E., Vatsan, A.R., Wallin, C., Webb, D., Wu, W., Landrum, M.J., Kimchi, A., Tatusova, T., DiCuccio, M., Kitts, P., Murphy, T.D. & Pruitt, K.D. 2016. Reference sequence (RefSeq) database at NCBI: Current status, taxonomic expansion, and functional annotation. Nucleic Acids Research, 44(D1): D733-D745. DOI: https://doi.org/10.1093/nar/gkv1189
Patro, R., Duggal, G., Love, M.I., Irizarry, R.A. & Kingsford, C. 2017. Salmon provides fast and bias-aware quantification of transcript expression. Nature Methods, 14(4): 417-419. DOI: https://doi.org/10.1038/nmeth.4197
Rowell, R.M., Pettersen, R. & Tshabalala, M.A. 2012. Cell wall chemistry. In: Handbook of Wood Chemistry and Wood Composites. R.M. Rowell (Ed.). CRC Press, Boca Raton. pp. 34-72. DOI: https://doi.org/10.1201/b12487-5
Tartar, A., Wheeler, M.M., Zhou, X., Coy, M.R., Boucias, D.G. & Scharf, M.E. 2009. Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotechnology for Biofuels, 2: 25. DOI: https://doi.org/10.1186/1754-6834-2-25
Thapa, R.S. 1981. Termites of Sabah (East Malaysia). Sabah Forest Record No 12. Sabah Forestry Department. 1-374.
The UniProt Consortium. 2023. Uniprot: The Universal Protein Knowledge in 2023. Nucleic Acids Research, 51(D1): D523-D531.
Tho, Y.P. 1992. Termites of Peninsular Malaysia. Malayan Forest Record No 36. Forest Research Institute Malaysia, Kepong. pp. 56-64.
Todaka, N., Moriya, S., Saita, K., Hondo, T., Kiuchi, I., Takasu, H., Ohkuma, M., Piero, C., Hayashizaki, Y. & Kudo, T. 2007. Environmental cDNA analysis of the genes involved in lignocellulose digestion in the symbiotic protist community of Reticulitermes speratus. FEMS Microbiology Ecology, 59(3): 592-599. DOI: https://doi.org/10.1111/j.1574-6941.2006.00237.x
Tokuda, G., Lo, N., Watanabe, H., Arakawa, G., Matsumoto, T. & Noda, H. 2004. Major alteration of the expression site of endogenous cellulases in members of an apical termites lineage. Molecular Ecology, 13(10): 3219-3228. DOI: https://doi.org/10.1111/j.1365-294X.2004.02276.x
Veluchamy, C. & Kalamdhad, A.S. 2017. Influence of pretreatment techniques on anaerobic digestion of pulp and paper mill sludge: a review. Bioresource Technology, 245(Pt A): 1206-1219. DOI: https://doi.org/10.1016/j.biortech.2017.08.179
Woon, J.S, King, P.J.H, Mackeen, M.M, Mahadi, N. M, Wan Seman, W.M.K, Broughton, W.J, Abdul Murad, A.M. & Abu Bakar, F.D. 2017. Cloning, production and characterization of a glycoside hydrolase family 7 enzyme from the gut microbiota of the termite Coptotermes curvignathus. Molecular Biotechnology, 59(7): 271-283. DOI: https://doi.org/10.1007/s12033-017-0015-x
Xie, L., Zhang, L., Zhong, Y., Liu, N., Long, Y., Wang, S., Zhou, X., Zhou, Z., Huang, Y. & Wang, Q. 2012. Profiling the metatranscriptome of the protistan community in Coptotermes formosanus with emphasis on the lignocellulolytic system. Genomics, 99(4): 246-255. DOI: https://doi.org/10.1016/j.ygeno.2012.01.009
Yagi, H., Takehara, R., Tamaki, A., Teramoto, K., Tsutsui, S. & Kaneko, S. 2019. Functional characterization of the GH10 and GH11 xylanases from Streptomyces olivaceoviridis E-86 provide insights into the advantage of GH11 xylanase in catalysing biomass degradation. Journal of Applied Glycoscience, 66(1): 29-35. DOI: https://doi.org/10.5458/jag.jag.JAG-2018_0008
Zhang, H., Yohe, T., Huang, L., Entwistle, S., Wu, P., Yang, Z., Busk, P.K., Xu, Y. & Yin, Y. 2018. dBCAN2: A meta server for automated carbohydrate-active enzyme annotation. Nucleic Acid Research, 46(W1): W95-W101. DOI: https://doi.org/10.1093/nar/gky418
Zhao, L., Zhang, J., Zhao, D., Jia, L., Qin, B., Cao, X., Zang, L., Lu, F. and Liu, F. 2022. Biological degradation of lignin: A critical review on progress and perspectives. Industrial Crops and Products, 188(Pt B): 115715. DOI: https://doi.org/10.1016/j.indcrop.2022.115715
Published
How to Cite
Issue
Section
Any reproduction of figures, tables and illustrations must obtain written permission from the Chief Editor (wicki@ukm.edu.my). No part of the journal may be reproduced without the editor’s permission
Funding data
-
Kementerian Sains, Teknologi dan Inovasi
Grant numbers 02-05-20-SF11118