Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes

Biotechnology for Biofuels

Volumn 2, Issue 1, 2009, Pages

  Tartar, Aurélien ^a,b   Wheeler, Marsha M ^a,c   Zhou, Xuguo ^a,d   Coy, Monique R ^a   Boucias, Drion G ^a   Scharf, Michael E ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b NOVA SOUTHEASTERN UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 70449408785     PISSN: 17546834     EISSN: None     Source Type: None    
DOI: 10.1186/1754-6834-2-25     Document Type: Article

References (101)

1. Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ Jr, Hallett JP, Leak DJ, Liotta CL, Mielenz JR, Murphy R, Templer R, Tschaplinski T: The path forward for biofuels and biomaterials. Science 2006, 311:484-489.
2. Saha BC: Hemicellulose bioconversion. J Ind Microbiol Biotechnol 2003, 30:279-291.
3. Anderson WF, Akin DE: Structural and chemical properties of grass lignocelluloses related to conversion for biofuels. J Ind Microbiol Biotechnol 2008, 35:355-366.
4. Rubin EM: Genomics of cellulosic biofuels. Nature 2008, 454:841-845.
5. Scharf ME, Tartar A: Termite digestomes as sources for novel lignocellulases. Biofuels Bioprod Bioref 2008, 2:540-552.
6. Ohkuma M: Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 2003, 61:1-9.
7. Brune A: Microbiology: woodworker's digest. Nature 2007, 450:487-488.
8. Chaffron S, von Mering C: Termites in the woodwork. Genome Biol 2007, 8:229.
9. Brune A: Symbiotic associations between termites and prokaryotes. Prokaryotes 2006, 1:439-474.
10. Ohkuma M, Hongoh Y, Noda S: Symbiotic complex in the termite gut microbial community. Tanpakushitsu Kakusan Koso 2008, 53:1841-1849.
11. Wood TG, Johnson RA: The biology, physiology, and ecology of termites. In Economic impact and control of social insects Edited by: Vinson SB, Johnson RA. Santa Barbara, CA, USA: Praeger; 1986:1-68.
12. Breznak JA, Brune A: Role of microorganisms in the digestion of lignocellulose by termites. Annu Rev Entomol 1994, 39:453-487.
13. Watanabe H, Nakamura M, Tokuda G, Yamaoka I, Scrivener AM, Noda H: Site of secretion and properties of endogenous endo-?-1,4-glucanase components from Reticulitermes speratus (Kolbe), a Japanese subterranean termite. Insect Biochem Mol Biol 1997, 27:305-313.
14. Watanabe H, Noda H, Tokuda G, Lo N: A cellulase gene of termite origin. Nature 1998, 394:330-331.
15. Nakashima K, Azuma JI: Distribution and properties of endo-β-1,4-glucanase from a lower termite Coptotermes formosanus. Biotechnol Biochem 2000, 64:1500-1506.
16. Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma J-I: Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus. Insect Biochem Mol Biol 2002, 32:777-784.
17. Zhou X, Smith JA, Oi FM, Koehler PG, Bennett GW, Scharf ME: Correlation of cellulase gene expression and cellulolytic activity throughout the gut of the termite Reticulitermes flavipes. Gene 2007, 395:29-39.
18. Wheeler MM, Zhou X, Scharf ME, Oi FM: Molecular and biochemical markers for monitoring dynamic shifts in cellulolytic protozoa in Reticulitermes flavipes. Insect Biochem Mol Biol 2007, 37:1366-1374.
19. 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? Gene 2007, 401:131-134.
20. Todaka N, Moriya S, Saita K, Hondo T, Kiuchi I, Takasu H, Ohkuma M, Piero C, Hayashizaki Y, Kudo T: Environmental cDNA analysis of the genes involved in lignocellulose digestion in the symbiotic protist community of Reticulitermes speratus. FEMS Microbiol Ecol 2007, 59:592-599.
21. Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang X, Hernández M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, et al.: Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 2007, 450:560-565.
22. Margonelli L: Gut reactions. [http://www.theatlantic.com/doc/200809/termites].
23. Hongoh Y, Sharma VK, Prakash T, Noda S, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, Ohkuma M: Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc Natl Acad Sci USA 2008, 105:5555-5560.
24. Hongoh Y, Sharma VK, Prakash T, Noda S, Toh H, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, Ohkuma M: Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 2008, 322:1108-1109.
25. Johjima T, Taprab Y, Noparatnaraporn N, Kudo T, Ohkuma M: Large-scale identification of transcripts expressed in a symbiotic fungus (Termitomyces) during plant biomass degradation. Appl Microbiol Biotechnol 2006, 73:195-203.
26. Slaytor M, Sugimoto A, Azuma J, Murashima K, Inoue T: Cellulose and xylan utilisation in the lower termite Reticulitermes speratus. J Insect Physiol 1997, 43:235-242.
27. Tokuda G, Watanabe H, Matsumoto T, Noda H: Cellulose digestion in the wood-eating higher termite, Nasutitermes takasagoensis (Shiraki): distribution of cellulases and properties of endo-beta-1,4-glucanase. Zoolog Sci 1997, 14:83-93.
28. Tokuda G, Saito H, Watanabe H: A digestive beta-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. Insect Biochem Mol Biol 2002, 32:1681-1689.
29. Watanabe H, Nakashima K, Saito H, Slaytor M: New endo-beta-1,4-glucanases from the parabasalian symbionts, Pseudotrichonympha grassii and Holomastigotoides mirabile of Coptotermes termites. Cell Mol Life Sci 2002, 59:1983-1992.
30. Zhou X, Wheeler MM, Oi FM, Scharf ME: Inhibition of termite cellulases by carbohydrate-based cellulose inhibitors: evidence from in vitro biochemistry and in vivo feeding studies. Pestic Biochem Physiol 2008, 90:31-41.
31. Yuki M, Moriya S, Inoue T, Kudo T: Transcriptome analysis of the digestive organs of Hodotermopsis sjostedti, a lower termite that hosts mutualistic microorganisms in its hindgut. Zoolog Sci 2008, 25:401-406.
32. Lange JP: Lignocellulose conversion: an introduction to chemistry, process and economics. Biofuels Bioprod Bioref 2007, 1:39-48.
33. Yang B, Wyman CE: Pretreatment: the key to unlocking lowcost cellulosic ethanol. Biofuels Bioprod Bioref 2008, 2:26-40.
34. Brune A, Miambi E, Breznak JA: Roles of oxygen and the intestinal microflora in the metabolism of lignin-derived phenylpropanoids and other monoaromatic compounds by termites. Appl Env Microbiol 1995, 61:2688-2695.
35. Sarkar N: Polyadenylation of mRNA in prokaryotes. Annu Rev Biochem 1997, 66:173-197.
36. Genereux DP, Logsdon JM Jr: Much ado about bacteria-to-vertebrate lateral gene transfer. Trends Genet 2003, 19:191-195.
37. Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren JH: Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 2007, 317:1753-1756.
38. Lozupone CA, Hamady M, Cantarel BL, Coutinho PM, Henrissat B, Gordon JI, Knight R: The convergence of carbohydrate active gene repertoires in human gut microbes. Proc Natl Acad Sci USA 2008, 105:15076-15081.
39. Wheeler MM, Tarver MR, Coy MR, Scharf ME: Characterization of four esterase genes and esterase activity from the gut of the termite Reticulitermes flavipes. Arch Insect Biochem Physiol in press.
40. Zhou X, Wheeler MM, Oi FM, Scharf ME: RNA interference in the termite Reticulitermes flavipes through ingestion of doublestranded RNA. Insect Biochem Mol Biol 2008, 38:805-815.
41. Smith JA, Koehler PG: Changes in Reticulitermes flavipes gut xylanolytic activities in response to dietary xylan content. Ann Entomol Soc Am 2007, 100:568-573.
42. Smith JA, Scharf ME, Pereira RM, Koehler PG: Comparison of gut carbohydrolase activity patterns in Reticulitermes flavipes and Coptotermes formosanus workers and soldiers. Sociobiology 2009, 53:13-22.
43. Smith JA, Scharf ME, Pereira RM, Koehler PG: pH optimization of gut cellulase and xylanase activities from the Eastern subterranean termite, Reticulitermes flavipes. Sociobiology 2009, 54:199-210.
44. de Vries RP, Michelsen B, Poulsen CH, Kroon PA, Heuvel RH van den, Faulds CB, Williamson G, Hombergh JP van den, Visser J: The faeA genes from Aspergillus niger and Aspergillus tubingensis encode ferulic acid esterases involved in degradation of complex cell wall polysaccharides. Appl Environ Microbiol 1997, 63:4638-4644.
45. de Vries RP, vanKuyk PA, Kester HC, Visser J: The Aspergillus niger faeB gene encodes a second feruloyl esterase involved in pectin and xylan degradation and is specifically induced in the presence of aromatic compounds. Biochem J 2002, 363:377-386.
46. Crepin VF, Faulds CB, Connerton IF: Functional classification of the microbial feruloyl esterases. Appl Microbiol Biotechnol 2004, 63:647-652.
47. Benoit I, Danchin EGJ, Bleichrodt RJ, de Vries RP: Biotechnological applications and potential of fungal feruloyl esterases based on prevalence, classification and biochemical diversity. Biotechnol Letters 2008, 30:387-396.
48. Smith M, Thurston CF, Wood DA: Fungal laccases - role in delignification and possible industrial applications. In Multi-copper oxidases Edited by: Messerschmidt A. Hackensack, NJ, USA: World Scientific; 1997:201-224.
49. Baldrian P: Fungal laccases - occurrence and properties. FEMS Microbiol Rev 2006, 30:215-242.
50. Ohkuma M, Saita K, Inoue T, Kudo T: Comparison of four protein phylogeny of parabasalian symbionts in termite guts. Mol Phylogen Evol 2007, 42:847-853.
51. Leadbetter JR, Breznak JA: Physiological ecology of Methanobrevibacter cuticularis sp. nov. and Methanobrevibacter curvatus sp. nov., isolated from the hindgut of the termite Reticulitermes flavipes. Appl Environ Microbiol 1996, 62:3620-3631.
52. Yang H, Schmitt-Wagner D, Stingl U, Brune A: Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis). Environ Microbiol 2005, 7:916-932.
53. Herlemann DP, Geissinger O, Ikeda-Ohtsubo W, Kunin V, Sun H, Lapidus A, Hugenholtz P, Brune A: Genomic analysis of Elusimicrobium minutum, the first cultivated representative of the phylum Elusimicrobia (formerly termite group 1). Appl Environ Microbiol 2009, 75:2841-2849.
54. Ikeda-Ohtsubo W, Brune A: Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and Candidatus Endomicrobium trichonymphae. Mol Ecol 2009, 18:332-342.
55. Sato T, Hongoh Y, Noda S, Hattori S, Ui S, Ohkuma M: Candidatus Desulfovibrio trichonymphae, a novel intracellular symbiont of the flagellate Trichonympha agilis in termite gut. Environ Microbiol 2009, 11:1007-1015.
56. Todaka N, Lopez CM, Inoue T, Saita K, Maruyama JI, Arioka M, Kitamoto K, Kudo T, Moriya S: Heterologous expression and characterization of an endoglucanase from a symbiotic protist of the lower termite, Reticulitermes speratus. Appl Biochem Biotechnol in press.
57. Bayer EA, Belaich JP, Shoham Y, Lamed R: The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu Rev Microbiol 2004, 58:521-554.
58. Wyman CE: Twenty years of trials, tribulations, and research progress in bioethanol technology. Appl Biochem Biotechnol 2001, 91-93:5-21.
59. Geib SM, Filley TR, Hatcher PG, Hoover K, Carlson JE, del Mar Jimenez-Gasco M, Nakagawa-Izumi A, Sleighter RL, Tien M: Lignin degradation in wood-feeding insects. Proc Natl Acad Sci USA 2008, 105:12932-12937.
60. Esenther GR, Kirk TK: Catabolism of aspen sapwood in Reticulitermes flavipes. Ann Entomol Soc Am 1974, 67:989-991.
61. Brune A, Emerson D, Breznak JA: Termite gut microflora as an oxygen sink: microelectrode determinations of oxygen and pH gradients in guts of lower and higher termites. Appl Env Microbiol 1995, 61:2681-2687.
62. Butler JHA, Buckerfield JC: Digestion of lignin by termites. Soil Biol Biochem 1979, 11:507-511.
63. Cookson LJ: 14C-lignin degradation by three Australian termite species. Wood Sci Technol 1987, 21:11-25.
64. Cookson LJ: The site and mechanism of 14C-lignin degradation by Nasutitermes exitosus. J Insect Physiol 1988, 34:409-414.
65. Shuji I, Ueshima K, Tanaka H, Enoki A: Degradation of wood components by subterranean termite, Coptotermes formosanus. Mokuzai Gakkaishi 1995, 41:580-586.
66. Kuhnigk T, König H: Degradation of dimeric lignin model compounds by aerobic bacteria isolated from the hindgut of xylophagous termites. J Basic Microbiol 1997, 37:205-211.
67. Katsumata KS, Jin Z, Hori K, Iiyama K: Structural changes in lignin of tropical woods during digestion by termite, Cryptotermes brevis. J Wood Sci 2007, 53:419-426.
68. Feyereisen R: Insect cytochrome P450. In Comprehensive molecular insect science Volume 4. Edited by: Gilbert LI, Iatrou K, Gill SS. New York, USA: Elsevier; 2005:1-77.
69. Vetrano AM, Heck DE, Mariano TM, Mishin V, Laskin DL, Laskin JD: Characterization of the oxidase activity in mammalian catalase. J Biol Chem 2005, 280:35372-35381.
70. Sutay-Kocabas D, Bakir U, Phillips SE, McPherson MJ, Ogel ZB: Purification, characterization, and identification of a novel bifunctional catalase-phenol oxidase from Scytalidium thermophilum. Appl Microbiol Biotechnol 2008, 79:407-415.
71. Arakane Y, Muthukrishnan S, Beeman RW, Kanost MR, Kramer KJ: Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proc Natl Acad Sci USA 2005, 103:11337-11342.
72. Yatsu J, Asano T: Cuticle laccase of the silkworm, Bombyx mori: purification, gene identification and presence of its inactive precursor in the cuticle. Insect Biochem Mol Biol 2009, 39:254-262.
73. Dittmer NT, Suderman RJ, Jiang H, Zhu Y-C, Gorman MJ, Kramer KJ, Kanost MR: Characterization of cDNAs encoding putative laccase-like multicopper oxidases and developmental expression in the tobacco hornworm, Manduca sexta, and the malaria mosquito, Anopheles gambiae. Insect Biochem Mol Biol 2003, 34:29-41.
74. Hattori M, Konishi H, Tamura Y, Konno K, Sogawa K: Laccase-type phenoloxidase in salivary glands and watery saliva of the green rice leafhopper, Nephotettix cincticeps. J Insect Physiol 2005, 51:1359-1365.
75. Zhang D, Lax AR, Raina AK, Bland JM: Differential cellulolytic activity of native-form and C-terminal tagged-form cellulase derived from Coptotermes formosanus and expressed in E. coli. Insect Biochem Mol Biol 2009, 39:516-522.
76. Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U: Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 2006, 273:2308-2326.
77. Taprab Y, Johjima T, Maeda Y, Moriya S, Trakulnaleamsai S, Noparatnarapron N, Okhuma M, Kudo T: Symbiotic fungi produce laccases potentially involved in phenol degradation in fungus combs of fungus-growing termites in Thailand. Appl Env Microbiol 2005, 71:7696-7704.
78. Sreerama L, Veerabhadrappa PS: Purification and properties of carboxylesterases from the mid-gut of the termite Odontotermes horni. Insect Biochem 1991, 21:833-844.
79. Sreerama L, Veerabhadrappa PS: Isolation and properties of carboxylesterases of the termite gut-associated fungus, Xylaria nigripes, and their identity from the host termite, Odontotermes horni. Int J Biochem 1993, 25:1637-1651.
80. Wyss-Huber M: Caste differences in haemolymph proteins in two species of termites. Insectes Soc 1981, 28:71-86.
81. Ruvolo-Takasusuki MCR, Collet T: Characterization of Nasutitermes globiceps esterases. Biochem Genet 2000, 38:367-375.
82. Davis RW, Kamble ST, Prabhakaran SK: Characterization of general esterases in workers of the Eastern subterranean termite. J Econ Entomol 1995, 88:574-578.
83. Valles SM, Oi FM, Strong CA: Purification and characterization of trans-permethrin metabolizing microsomal esterases from workers of the eastern subterranean termite, Reticulitermes flavipes. Insect Biochem Mol Biol 2001, 31:715-725.
84. Oakeshott JG, Claudianos C, Campbell PM, Newcombe RD, Russell RJ: Biochemical genetics and genomics of insect esterases. In Comprehensive molecular insect science Volume 5. Edited by: Gilbert LI, Iatrou K, Gill SS. New York, USA: Elsevier-Pergamon; 2005:309-382.
85. Simmons BA, Loque D, Blanch HW: Next-generation biomass feedstocks for biofuel production. Genome Biol 2008, 9:242.
86. Ni J, Takehara M, Watanabe H: Heterologous overexpression of a mutant termite cellulase gene in Escherichia coli by DNA shuffling of four orthologous parental cDNAs. Biosci Biotechnol Biochem 2005, 69:1711-1720.
87. Ni J, Takehara M, Miyazawa M, Watanabe H: Random exchanges of non-conserved amino acid residues among four parental termite cellulases by family shuffling improve thermostability. Protein Eng Des Sel 2007, 20:535-542.
88. Sasaguri S, Maruyama J, Moriya S, Kudo T, Kitamoto K, Arioka M: Codon optimization prevents premature polyadenylation of heterologously-expressed cellulases from termite-gut symbionts in Aspergillus oryzae. J Gen Appl Microbiol 2008, 54:343-351.
89. O'Connell KP, Kovaleva E, Campbell JH, Anderson PE, Brown SG, Davis DC, Valdes JJ, Welch RW, Bentley WE, van Beek NA: Production of a recombinant antibody fragment in whole insect larvae. Mol Biotechnol 2007, 36:44-51.
90. Szalanski AL, Austin JW, Owens CB: Identification of Reticulitermes spp. (Isoptera: Rhinotermitidae) by polymerase chain reaction - restriction fragment length polymorphism. J Econ Entomol 2003, 96:1514-1519.
91. Zhu YY, Machleder EM, Chenchik A, Li R, Siebert PD: Reverse transcriptase template switching: a SMART approach for fulllength cDNA library construction. Biotechniques 2001, 30:892-897.
92. Zhulidov PA, Bogdanova EA, Shcheglov AS, Vagner LL, Khaspekov GL, Kozhemyako VB, Matz MB, Meleshkevitch A, Moroz LL, Lukyanov SA, Shagin DA: Simple cDNA normalization using Kamchatka crab duplex-specific nuclease. Nucleic Acids Res 2004, 32:e37.
93. Shagin DA, Rebrikov DV, Kozhemyako VB, Altshuler IM, Schlegov AS, Zhulidov PA, Bogdanova EA, Staroverov DB, Rasskazov VA, Lukyanov S: A novel method for SNP detection using a new duplex-specific nuclease from crab hepatopancreas. Genome Res 2002, 12:1935-1942.
94. Sambrook J, Fritsch EF, Maniatis T: Molecular cloning, a laboratory manual. >Cold Spring Harbor Laboratory Press; 1989.
95. Huang X, Madan A: CAP3: A DNA sequence assembly program. Genome Res 1999, 9:868-877.
96. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B: The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 2009, 37:D233-238.
97. Bendtsen JD, Nielsen H, von Heijne G, Brunak S: Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795.
98. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 1997, 24:4876-4882.
99. Chance B, Maehly AC: Assays of catalases and peroxidases. Meth Enzymol 1955, 2:773-775.
100. Rozen S, Skaletsky HJ: Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics methods and protocols, methods in molecular biology Edited by: Krawetz S, Misener S. Totowa, NJ, USA: Humana Press; 2000:365-386.
101. Lee B: ESTin: a program for building a dbEST submission file from massive EST sequences. Genom Info 2006, 4:170-172.