Research Advances on Endogenous Cellulase Gene Resources of Termites

doi:10.13560/j.cnki.biotech.bull.1985.2015.12.004

Abstract

Abstract: Energy shortage has become a global problem, and cellulose is the most abundant and renewable resource in nature. Termites have evolved the unique and efficient cellulose-digesting system, in which there are rich resources of cellulase and its genes. In recent years, the significance of endogenous cellulose-digesting system in termite has been recognized gradually, and the researches on the endogenous cellulase genes have been reported continuously. In order to improve the new control technologies of termite pests and to explore the cellulosic biomass for biofuels, the review provides the information for the cloning and expressions of termite endogenous cellulase genes.

Key words: termite, endogenous cellulase gene, gene cloning

Liu Xiaolin, Li Zhiqiang, Zhang Dandan. Research Advances on Endogenous Cellulase Gene Resources of Termites[J]. Biotechnology Bulletin, 2015, 31(12): 25-33.

References

[1] Carroll A, Somerville C. Cellulosic biofuels[J]. Annual Review of Plant Biology, 2009, 60(1):165-182.
[2] Watanabe H, Tokuda, G. Animal Cellulases[J]. Cellular and Molecular Life Science, 2001, 58(9):1167-1178.
[3] Watanabe H, Tokuda, G. Cellulolytic systems in insects[J]. Annual Review of Entomology, 2010, 55:609-632.
[4] Prins RA, Kreulen DA. Comparative aspects of plant cell wall digestion in insects[J]. Animal Feed Science and Technology, 1991, 32(1-3):101-118.
[5] Breznak JA, Brune A. Role of microorganisms in the digestion of lignocellulose by termite[J]. Annual Review of Entomology, 1994, 39:453-487.
[6] Ohkuma M. Termite symbiotic systems:efficient bio-recycling of lignocelluloses[J]. Applied Microbiology and Biotechnology, 2003, 61(1):1-9.
[7] Watanabe H, Noda H, Nakamura M, et al. A cellulase gene of termite origin[J]. Nature, 1998, 394(6691):330-331.
[8] Tokuda G, Watanabe H, Hojo M, et al. Cellulolytic environment in themidgut of the wood-feeding higher termite Nasutitermes takasagoensis[J]. Journal of Insect Physiology, 2012, 58(1):147-154.
[9] Zhang D, Lax AR, Bland JM, et al. Characterization of a new endogenous endo-Β-1, 4-glucanase of Formosan subterranean termite(Coptotermes formosanus)[J]. Insect Biochemistry and Molecular Biology, 2011, 41(4):211-218.
[10] Nakashima K, Watanabe H, Saitoh H, et al. Dual cellulosedigesting system of the wood-feeding termite, Coptotermes formosanus(Shiraki)[J]. Insect Biochemistry and Molecular Biology, 2002, 32(7):777-784.
[11] Scharf ME, Karl ZJ, Sethi A, Boucias DG. Multiple levels of synergistic collaboration in termite lignocellulose digestion[J]. PLoS One, 2011, 6(7):e21709.
[12] Zhou X, Smith JA, Oi FM, et al. Correlation of cellulase gene expression and cellulolytic activity throughout the gut of the termite Reticulitermes flavipes[J]. Gene, 2007, 395(1-2):29-39.
[13] Tokuda G, Watanabe H, Lo N. Does correlation of cellulase gene expression and cellulolytic activity in the gut of termite suggest synergistic collaboration of cellulases?[J]. Gene, 2007, 401(1-2):131-134.
[14] Brune A, Friedrich M. Microecology of the termite gut:structure and function on a microscale[J]. Current Opinion in Microbiology, 2000, 3(3):263-269.
[15] Tokuda G, Lo N, Watanabe H, et al. Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage[J]. Molecular Ecology, 2004, 13(10):3219-3228.
[16] Aanen DK, Eggleton P, Rouland-Lefèvré C, et al. The evolution of fungus-growing termites and their mutualistic fungal symbionts[J]. Proceedings of the National Academy of Sciences, 2002, 99(23):14887-14892.
[17] 孙建中, 陈春润. 昆虫与生物质能源利用:一个新的交叉学科前沿[J]. 昆虫知识, 2010, 47(6):1033-1042.
[18] Yuki M, Moriya S, Inoue T, et al. Transcriptome analysis of the digestive organs of Hodotermopsis sjostedti, a lower termite that hosts mutualistic microorganisms in its hindgut[J]. Zoological Science, 2008, 25(4):401-406.
[19] Zhou X, Wheeler MM, Oi FM, et al. RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA[J]. Insect Biochemistry and Molecular Biology, 2008, 38(8):805-815.
[20] Watanabe H, Nakamura M, Tokuda G, et al. Site of secretion and properties of endogenous endo-Β-1, 4-glucanase components from Reticulitermes speratus(Kolbe), a Japanese subterranean termite[J]. Insect Biochemistry and Molecular Biology, 1997, 27(4):305-313.
[21] Li L, Fr?hlich J, Pfeiffer P, et al. Termite gut symbiotic archaezoa are becoming living metabolic fossils[J]. Eukaryotic Cell, 2003, 2(5):1091-1098.
[22] Tokuda G, Lo N, Watanabe H, et al. Metazoan cellulase genes from termites:intron/exon structures and sites of expression[J]. Biochimica et Biophysica Acta -Gene Structure and Expression, 1999, 1447(2-3):146-159.
[23] Zhang D, Lax AR, Raina AK, et al. Differential cellulolytic activity of native-form and C-terminal tagged-form cellulase derived from Coptotermes formosanus and expressed in E. coli. [J]. Insect Biochemistry and Molecular Biology, 2009, 39(8):516-522.
[24] Cairo JP, Oliveira LC, Uchima CA, et al. Deciphering the synergism of endogenous glycoside hydrolase families 1 and 9 from Coptotermes gestroi[J]. Insect Biochemistry and Molecular Biology, 2013, 43(10):970-981.
[25] Scharf ME, Wu-Scharf D, Zhou X, et al. Gene expression profiles among immature and adult reproductive castes of the termite Reticulitermes flavipes[J]. Insect Molecular Biology, 2005, 14(1):31-44.
[26] Ni J, Wu Y, Yun C, et al. cDNA cloning and heterologous expression of an endo-Β-1,4-glucanase from the fungus-growing termite Macrotermes barneyi[J]. Archives of Insect Biochemistry and Physiology, 2014, 86(3):151-164.
[27] Tokuda G, Saito H, Watanabe H. A digestiveb-glucosidase from the salivary glands of the termite, Neotermes koshunensis(Shiraki):distribution, characterization and isolation of its precursor cDNA by 5'- and 3'-RACE amplifications with degenerate primers[J]. Insect Biochemistry and Molecular Biology, 2002, 32(12):1681-1689.
[28] Scharf ME, Kovaleva ES, Jadhao S, et al. Functional and translational analyses of a beta-glucosidase gene(glycosyl hydrolase family 1)isolated from the gut of the lower termite Reticulitermes flavipes[J]. Insect Biochemistry and Molecular Biology, 2010, 40(8):611-620.
[29] Zhang D, Lax AR, Bland JM, et al. Hydrolysis of filter-paper cellulose to glucose by two recombinant endogenous glycosyl hydrolases of Coptotermes formosanus[J]. Insect Science, 2010, 17(3):245-252.
[30] Zhang D, Lax AR, Henrissat B, et al. Carbohydrate-active enzymes revealed in Coptotermes formosanus(Isoptera:Rhinotermitidae)transcriptome[J]. Insect Molecular Biology, 2012a, 21(2):235-245.
[31] Tokuda G, Miyagi M, Makiya H, et al. Digestive beta-glucosidases from the wood-feeding higher termite, Nasutitermes takasagoensis:Intestinal distribution, molecular characterization, and alteration in sites of expression[J]. Insect Biochemistry and Molecular Biology, 2009, 39(12):931-937.
[32] Wu Y, Chi S, Yun C, et al. Molecular cloning and characterization of an endogenous digestive beta-glucosidase from the midgut of the fungus-growing termite Macrotermes barneyi[J]. Insect Molecular Biology, 2012, 21(6):604-614.
[33] Bujang NS, Harrison NA, Su NY. Molecular cloning of five beta-glucosidases from four species of higher termites(Blattodea:Termitidae)[J]. Annals of the Entomological Society of America, 2014, 107(1):251-256.
[34] Hahn MW. Distinguishing among evolutionary models for the maintenance of gene duplicates[J]. Journal of Heredity, 2009, 100(5):605-617.
[35] Tokuda G, Lo N, Watanabe H. Marked variations in patterns of cellulase activity against crystalline- versus carboxymethyl-cellulose in the digestive systems of diverse, wood-feeding termites[J]. Physiological Entomology, 2005, 30(4):372-380.
[36] Reinhard J, Kaib M. Food exploitation in termites:indication for a general feeding stimulating signal in labial gland secretion of Isoptera[J]. Journal of Chemical Ecology, 2001a, 27(1):189-201.
[37] Reinhard J, Kaib M. Thin-layer chromatography assessing feeding stimulation by labial gland secretion compared to synthetic chemic-als in the subterranean termite Reticulitermes santonensis[J]. Journal of Chemical Ecology, 2001b, 27(1):175-187.
[38] Lamberty M, Zachary D, Lanot R, et al. Insect immunity:Constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect[J]. Journal of Biological Chemistry, 2001, 276(6):4085-4092.
[39] Matsuura K, Yashiro T, Shimizu K, et al. Cuckoo fungus mimics termite eggs by producing the cellulose-digesting enzyme Β-glucosidase[J]. Current Biology, 2009, 19(1):30-36.
[40] Fujita A, Shimizu I, Abe T. Distribution of lysozyme and protease, and amino acid concentration in the guts of a wood-feeding termite, Reticulitermes speratus(Kolbe):possible digestion of symbiont bacteria transferred by trophallaxis[J]. Physiological Entomology, 2001, 26(2):116-123.
[41] Xu Q, Singh A, Himmel ME. Perspectives and new directions for the productionof bioethanol using consolidated bioprocessing of lignocellulose[J]. CurrentOpinion in Biotechnology, 2009, 20(3):364-371.
[42] Seiboth B, Karimi RA, Phatale PA, et al. The putative protein met-hyltransferase LAE1 controlscellulase gene expression in Trichod-erma reeseimmi[J]. Molecular Microbiology, 2012, 84(6):1150-1164.
[43] Portnoy T, Margeot A, Linke R, et al. The CRE1 carbon catabolite repressor of thefungus Trichoderma reesei:a master regulator of carbon assimilation[J]. BMC Genomics, 2011, 12:269.
[44] Zou G, Shi S, Jiang Y, et al. Construction of a cellulase hyper-expressionsystem in Trichoderma reesei by promoter andenzyme engineering[J]. Microbial Cell Factories, 2012, 11:21.
[45] Lee SJ, Kim SR, Yoon HJ, et al. cDNA cloning, expression, and enzymatic activity of a cellulase from the mulberry longicorn beetle, Apriona germari[J]. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 2004, 139(1):107-116.
[46] Ni J, Takehara M, Watanabe H. Heterologous overexpression of a mutant termite cellulose gene in Escherichia coli by DNA shuffling of four orthologous parental cDNAs[J]. Bioscience, Biotechnology, and Biochemistry, 2005, 69(9):1711-1720.
[47] Ni J, Tokuda G, Takehara M, et al. Heterologous expression and enzymatic characterization of Β-glucosidase from the dry wood-eating termite, Neotermes koshunensis[J]. Applied Entomology and Zoology, 2007b, 42(3):457-463.
[48] Zhang D, Allen AB, Lax AR. Functional analyses of the digestive Β-glucosidase of Formosan subterranean termites(Coptotermes formosanus)[J]. Journal of Insect Physiology, 2012b, 58(1):205-210.
[49] Hirayama K, Watanabe H, Tokuda G, et al. Purification and characterization of termite endogenous Β-1, 4-endoglucanases produced in Aspergillus oryzae[J]. Bioscience, Biotechnology, and Biochemistry, 2010, 74(8):1680-1686.
[50] Ni J, Takehara M, Miyazawa M, et al. Random exchanges of non-conserved amino acid residues among four parental termite cellulases by family shuffling improved thermostability[J]. Protein Engineering, Design and Selection, 2007a, 20(11):535-542.
[51] Uchima CA, Tokuda G, Watanabe H, et al. Heterologous expression and characterization of a glucose-stimulated Β-glucosidase from the termite Neotermes koshunensis in Aspergillus oryzae[J]. Applied Microbiology and Biotechnology, 2011, 89(6):1761-1771.
[52] Uchima CA, Tokuda G, Watanabe H, et al. Heterologous expression in Pichia pastoris and characterization of an endogenous thermostable and high glucose-tolerant Β-glucosidase from the termite Nasutitermes takasagoensis[J]. Applied and Environmental Microbiology, 2012, 78(12):4288-4293.
[53] Uchima CA, Tokuda G, Watanabe H, et al. A novel glucose-tolerant Β-glucosidase from the salivary gland of the termite Nasutitermes takasagoensis[J]. The Journal of General and Applied Microbiology, 2013, 59(2):141-145.
[54] Watanabe H, Nakashima K, Saito H, et al. New endo-Β-1, 4-glucan-ases from the parabasalian symbionts, Pseudotrichonympha grassii and Holomastigotoides mirabile of Coptotermes termites[J]. Cellular and Molecular Life Science, 2002, 59(11):1983-1992.
[55] Tokuda G, Watanabe H, Matsumoto T, et al. Cellulose digestion in the wood-eating higher termite, Nasutitermes takasagoensis(Shiraki):distribution of cellulases and properties of endo-beta-1, 4-glucanase[J]. Zoological Science, 1997, 14(1):83-93.
[56] Warnecke F, Luginbuhl P, Ivanova N, et al. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite[J]. Nature, 2007, 450(7169):560-565.
[57] Burnum KE, Callister SJ, Nicora CD, et al. Proteome insights into the symbiotic relationship between a captive colony of Nasutitermes corniger and its hindgut microbiome[J]. The ISME Journal, 2011, 5(1):161-164.
[58] Terrapon N, Li C, Robertson HM, et al. Molecular traces of alterna-tive social organizationin a termite genome[J]. Nature Communi-cations, 2014, 5:3636.
[59] Poulsen M, Hu H, Li C, et al. Complementary symbiont contributions to plant decomposition in a fungus-farming termite[J]. Proceed-ings of the National Academy of Sciences, 2014, 111(40):14500-14505.
[60] Scharf ME. Omic research in termites:an overview and aroadmap[J]. Frontiers in Genetics, 2015, 6:76.
[61] Leonardo FC, da Cunha AF, da Silva MJ, et al. Analysis of the workers headtranscriptome of the Asian subterraneantermite, Coptotermes gestroi[J]. Bulletin of Entomological Research, 2011, 101(4):383-391.
[62] Tartar A, Wheeler MM, Zhou XG, et al. Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes[J]. Biotechnology for Biofuels, 2009, 2:25.
[63] Tokuda G, Tsuboi Y, Kihara K, et al. Metabolomic profiling of ¹³C-labelled cellulose digestion in a lower termite:insights into gut symbiont function[J]. Proceeding B of the Royal Society, 2014, 281:20140990.