Animal cellulases with a focus on aquatic invertebrates

Fisheries Science

Volumn 79, Issue 1, 2013, Pages 1-13

  Tanimura, Aya ^a   Liu, Wen ^a   Yamada, Kyohei ^a   Kishida, Takushi ^a   Toyohara, Haruhiko ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Breakdown; Cellulase; Cellulose; Endo 1,4 glucanase; Endogenous; GHF9; Invertebrate; Symbiosis

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); FUNGI; INVERTEBRATA; PHOTOBACTERIA; PROTOZOA;

EID: 84872265118     PISSN: 09199268     EISSN: 14442906     Source Type: Journal    
DOI: 10.1007/s12562-012-0559-4     Document Type: Article

References (105)

1. Watanabe H, Tokuda G (2001) Animal cellulases. Cell Mol Life Sci 58: 1167-1178.
2. Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol Annu Rev 55: 609-632.
3. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Bio 6: 850-861.
4. Henrissat B, Claeyssens M, Tomme P, Lemesle L, Mornon JP (1989) Cellulase families revealed by hydrophobic cluster-analysis. Gene 81: 83-95.
5. Karrer P, Schubert P, Wehrli W (1925) Polysaccharides XXXIII. On the enzymatic breakdown of artificial silk and native cellulose. Helv Chim Acta 8: 797-810.
6. Lenski RE (2003) Life's solution: inevitable humans in a lonely universe. Nature 425: 767-768.
7. Watanabe H, Noda H, Tokuda G, Lo N (1998) A cellulase gene of termite origin. Nature 394: 330-331.
8. Martin MM (1991) The evolution of cellulose digestion in insects. Philos Trans R Soc B 333: 281-288.
9. Sugimura M, Watanabe H, Lo N, Saito H (2003) Purification, characterization, cDNA cloning and nucleotide sequencing of a cellulase from the yellow-spotted longicorn beetle, Psacothea hilaris. Eur J Biochem 270: 3455-3460.
10. Nishida Y, Suzuki K, Kumagai Y, Tanaka H, Inoue A, Ojima T (2007) Isolation and primary structure of a cellulase from the Japanese sea urchin Strongylocentrotus nudus. Biochimie 89: 1002-1011.
11. Smant G, Stokkermans J, Yan YT, de Boer JM, Baum TJ, Wang XH, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J (1998) Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci USA 95: 4906-4911.
12. Sakamoto K, Touhata K, Yamashita M, Kasai A, Toyohara H (2007) Cellulose digestion by common Japanese freshwater clam Corbicula japonica. Fish Sci 73: 675-683.
13. Imjongjirak C, Amparyup P, Sittipraneed S (2008) Cloning, genomic organization and expression of two glycosyl hydrolase family 10 (GHF10) genes from golden apple snail (Pomacea canaliculata). DNA Seq 19: 224-236.
14. Kostanjsek R, Milatovic M, Srus J (2010) Endogenous origin of endo-beta-1, 4-glucanase in common woodlouse Porcellio scaber (Crustacea, Isopoda). J Comp Physiol B 180: 1143-1153.
15. Lo N, Watanabe H, Sugimura M (2003) Evidence for the presence of a cellulase gene in the last common ancestor of bilaterian animals. Proc R Soc Lond B Bio 270: S69-S72.
16. Davison A, Blaxter M (2005) Ancient origin of glycosyl hydrolase family 9 cellulase genes. Mol Biol Evol 22: 1273-1284.
17. Hungate RE (1946) The cellulose-decomposing bacteria in the rumen of cattle. J Bacteriol 51: 589.
18. Wood TM, Wilson CA, Stewart CS (1982) Preparation of the cellulase from the cellulolytic anaerobic rumen bacterium Ruminococcus albus and its release from the bacterial-cell wall. Biochem J 205: 129-137.
19. Coleman GS (1986) The distribution of carboxymethylcellulase between fractions taken from the rumens of sheep containing no protozoa or one of 5 different protozoal populations. J Agric Sci 106: 121-127.
20. Bernalier A, Fonty G, Bonnemoy F, Gouet P (1992) Degradation and fermentation of cellulose by the rumen anaerobic fungi in axenic cultures or in association with cellulolytic bacteria. Curr Microbiol 25: 143-148.
21. Varel VH, Fryda SJ, Robinson IM (1984) Cellulolytic bacteria from pig large-intestine. Appl Environ Microbiol 47: 219-221.
22. Cleveland LR (1924) The physiological and symbiotic relationships between the intestinal protozoa of termites and their host, with special reference to Reticulitermes flavipes Kollar. Biol Bull US 46: 178-201.
23. Trager W (1932) A cellulase from the symbiotic intestinal flagellates of termites and of the roach, Cryptocercus punctulatus. Biochem J 26: 1762-1771.
24. Delalibera I, Handelsman J, Raffa KF (2005) Contrasts in cellulolytic activities of gut microorganisms between the wood borer, Saperda vestita (Coleoptera: Cerambycidae), and the bark beetles, Ips pini and Dendroctonus frontalis (Coleoptera: Curculionidae). Environ Entomol 34: 541-547.
25. Wenzel M, Schonig I, Berchtold M, Kampfer P, Konig H (2002) Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis. J Appl Microbiol 92: 32-40.
26. Watanabe H, Takase A, Tokuda G, Yamada A, Lo N (2006) Symbiotic "archaezoa" of the primitive termite Mastotermes darwiniensis still play a role in cellulase production. Eukaryot Cell 5: 1571-1576.
27. Martin MM, Martin JS (1978) Cellulose digestion in midgut of fungus-growing termite Macrotermes natalensis-role of acquired digestive enzymes. Science 199: 1453-1455.
28. Rouland C, Civas A, Renoux J, Petek F (1988) Purification and properties of cellulases from the termite Macrotermes mulleri (Termitidae, Macrotermitinae) and its symbiotic fungus Termitomyces sp. Comp Biochem Phys B 91: 449-458.
29. Popham JD, Dickson MR (1973) Bacterial associations in the teredo Bankia australis (Lamellibranchia: Mollusca). Mar Biol 19: 338-340.
30. Waterbury JB, Calloway CB, Turner RD (1983) A cellulolytic nitrogen-fixing bacterium cultured from the gland of Deshayes in shipworms (Bivalvia: Teredinidae). Science 221: 1401-1403.
31. Distel DL, DeLong EF, Waterbury JB (1991) Phylogenetic characterization and in situ localization of the bacterial symbiont of shipworms (Teredinidae: Bivalvia) by using 16S rRNA sequence analysis and oligodeoxynucleotide probe hybridization. AEM 57: 2376-2382.
32. Distel DL, Morrill W, Maclaren-Toussaint N, Franks D, Waterbury J (2002) Teredinibacter turnerae gen. nov., sp. nov., a dinitrogen-fixing, cellulolytic, endosymbiotic g-proteobacterium isolated from the gills of wood-boring molluscs (Bivalvia: Teredinidae). IJSEM 52: 2261-2269.
33. Distel DL, Roberts SJ (1997) Bacterial endosymbionts in the gills of the deep-sea wood-boring bivalves Xylophaga atlantica and Xylophaga washingtona. Biol Bull 192: 253-261.
34. Duperron S, Laurent MCZ, Gaill F, Gros O (2008) Sulphur-oxidizing extracellular bacteria in the gills of Mytilidae associated with wood falls. FEMS Microbiol Ecol 63: 338-349.
35. Zbinden M, Pailleret M, Ravaux J, Gaudron SM, Hoyoux C, Lambourdiere J, Waren A, Lorion J, Halary S, Duperron S (2010) Bacterial communities associated with the wood-feeding gastropod Pectinodonta sp. (Patellogastropoda, Mollusca). FEMS Microbiol Ecol 74: 450-463.
36. Cary SC (1994) Vertical transmission of a chemoautotrophic symbiont in the protobranch bivalve, Solemya reidi. Mol Mar Biol Biotech 3: 121-130.
37. Sipe AR, Wilbur AE, Cary SC (2000) Bacterial symbiont transmission in the wood-boring shipworm Bankia setacea (Bivalvia: Teredinidae). Environ Microbiol 66: 1685-1691.
38. Boyle JP (1978) Absence of microorganism in crustacean digestive tracts. Science 200: 1157-1159.
39. King AJ (2010) Molecular insight into lignocelluloses digestion by a marine isopod in the absence of gut microbes. Proc Natl Acad Sci USA 107: 5345-5350.
40. Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma JI (2000) Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol 32: 777-784.
41. Lo N, Tokuda G, Watanabe H, Rose H, Slaytor M, Maekawa K, Bandi C, Noda H (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10: 801-804.
42. Willis JD, Oppert B, Oppert C, Klingeman WE, Jurat-Fuentes JL (2011) Identification, cloning, and expression of a GHF9 cellulase from Tribolium castaneum (Coleoptera: Tenebrionidae). J Insect Physiol 57: 300-306.
43. Gao BL, Allen R, Maier T, McDermott JP, Davis EL, Baum TJ, Hussey RS (2002) Characterisation and developmental expression of a chitinase gene in Heterodera glycines. Int J Parasitol 32: 1293-1300.
44. Yan YT, Smant G, Stokkermans J, Qin L, Helder J, Baum T, Schots A, Davis E (1998) Genomic organization of four beta-1, 4-endoglucanase genes in plant-parasitic cyst nematodes and its evolutionary implications. Gene 220: 61-70.
45. Jones JT, Furlanetto C, Kikuchi T (2005) Horizontal gene transfer from bacteria and fungi as a driving force in the evolution of plant parasitism in nematodes. Nematology 7: 641-646.
46. Kikuchi T, Jones JT, Aikawa T, Kosaka H, Ogura N (2004) A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. FEBS Lett 572: 201-205.
47. Byrne KA, Lehnert SA, Johnson SE, Moore SS (1999) Isolation of a cDNA encoding a putative cellulase in the red claw crayfish Cherax quadricarinatus. Gene 239: 317-324.
48. Suzuki K, Ojima T, Nishita K (2003) Purification and cDNA cloning of a cellulase from abalone Haliotis discus hannai. Eur J Biochem 270: 771-778.
49. Nikapitiya C, Oh C, De Zoysa M, Whang I, Kang DH, Lee SR, Kim SJ, Lee J (2010) Characterization of beta-1, 4-endoglucanase as a polysaccharide-degrading digestive enzyme from disk abalone, Haliotis discus discus. Aquac Int 18: 1061-1078.
50. Li YH, Yin QY, Ding M, Zhao FK (2009) Purification, characterization and molecular cloning of a novel endo-beta-1, 4-glucanase AC-EG65 from the mollusc Ampullaria crossean. Comp Biochem Phys B 153: 149-156.
51. Xu BZ, Janson JC, Sellos D (2001) Cloning and sequencing of a molluscan endo-beta-1, 4-glucanase gene from the blue mussel, Mytilus edulis. Eur J Biochem 268: 3718-3727.
52. Sakamoto K, Toyohara H (2009) Molecular cloning of glycoside hydrolase family 45 cellulase genes from brackish water clam Corbicula japonica. Comp Biochem Phys B 152: 390-396.
53. Guo R, Ding M, Zhang SL, Xu GJ, Zhao FK (2008) Molecular cloning and characterization of two novel cellulase genes from the mollusc Ampullaria crossean. J Comp Physiol B 178: 209-215.
54. Won NI, Kawamura T, Takami H, Hoshikawa H, Watanabe Y (2011) Comparison of abalone (Haliotis discus hannai) catches in natural habitats affected by different current systems: implication of climate effects on abalone fishery. Fish Res 110: 84-91.
55. Xing RL, Wang CH, Cao XB, Chang YQ (2008) Settlement, growth and survival of abalone, Haliotis discus hannai, in response to eight monospecific benthic diatoms. J Appl Phycol 20: 47-53.
56. Hawkins AJS, Navarro E, Iglesias JIP (1990) Comparative allometries of gut-passage time, gut content and metabolic fecal loss in Mytilus edulis and Cerastoderma edule. Mar Biol 105: 197-204.
57. Antonio ES, Kasai A, Ueno M, Kurikawa Y, Tsuchiya K, Toyohara H, Ishihi Y, Yokoyama H, Yamashita Y (2010) Consumption of terrestrial organic matter by estuarine molluscs determined by analysis of their stable isotopes and cellulase activity. Estuar Coast Shelf Sci 86: 401-407.
58. Kasai A, Nakata A (2005) Utilization of terrestrial organic matter by the bivalve Corbicula japonica estimated from stable isotope analysis. Fish Sci 71: 151-158.
59. Qiu JW, Chan MT, Kwong KL, Sun J (2011) Consumption, survival and growth in the invasive freshwater snail Pomacea Canaliculata: does food freshness matter? J Mollus Stud 77: 189-195.
60. Kanaya G, Suzuki T, Kikuchi E (2011) Spatio-temporal variations in macrozoobenthic assemblage structures in a river-affected lagoon (Idoura Lagoon, Sendai Bay, Japan): influences of freshwater inflow. Estuar Coast Shelf Sci 92: 169-179.
61. Kanaya G, Takagi S, Kikuchi E (2008) Spatial dietary variations in Laternula marilina (Bivalva) and Hediste spp. (Polychaeta) along environmental gradients in two brackish lagoons. Mar Ecol Prog Ser 359: 133-144.
62. Sakamoto K, Uji S, Kurokawa T, Toyohara H (2009) Molecular cloning of endogenous beta-glucosidase from common Japanese brackish water clam Corbicula japonica. Gene 435: 72-79.
63. Sakamoto K, Uji S, Kurokawa T, Toyohara H (2008) Immunohistochemical, in situ hybridization and biochemical studies on endogenous cellulase of Corbicula japonica. Comp Biochem Phys B 150: 216-221.
64. Sakamoto K, Toyohara H (2009) Putative endogenous xylanase from brackish-water clam Corbicula japonica. Comp Biochem Phys B 154: 85-92.
65. Sakamoto K, Toyohara H (2009) A comparative study of cellulase and hemicellulose activities of brackish water clam Corbicula japonica with those of other marine Veneroida bivalves. J Exp Biol 212: 2812-2818.
66. Ootsuka S, Saga N, Suzuki K, Inoue A, Ojima T (2006) Isolation and cloning of an endo-beta-1, 4-mannanase from Pacific abalone Haliotis discus hannai. J Biotechnol 125: 269-280.
67. Shimizu E, Ojima T, Nishita K (2003) cDNA cloning of an alginate lyase from abalone, Haliotis discus hannai. Carbohydr Res 338: 2841-2852.
68. Kumagai Y, Ojima T (2009) Enzymatic properties and the primary structure of a beta-1, 3-glucanase from the digestive fluid of the Pacific abalone Haliotis discus hannai. Comp Biochem Phys B 154: 113-120.
69. Xu BZ, Hagglund P, Stalbrand H, Janson JC (2002) Endo-beta-1, 4-mannanases from blue mussel, Mytilus edulis: purification, characterization, and mode of action. J Biotechnol 92: 267-277.
70. Zahura UA, Rahman MM, Inoue A, Tanaka H, Ojima T (2011) cDNA cloning and bacterial expression of an endo-beta-1, 4-mannanase, AkMan, from Aplysia kurodai. Comp Biochem Phys B 159: 227-235.
71. Kumagai Y, Ojima T (2010) Isolation and characterization of two types of beta-1, 3-glucanases from the common sea hare Aplysia kurodai. Comp Biochem Phys B 155: 138-144.
72. Niiyama T, Toyohara H (2011) Widespread distribution of cellulase and hemicellulose activities among aquatic invertebrates. Fish Sci 77: 649-655.
73. Toyohara H, Park Y, Tsuchiya K, Liu W (2012) Cellulase activity in meiobenthos in wetlands. Fish Sci 78: 133-137.
74. Yamada K, Toyohara H (2012) Functions of meiobenthos and microorganisms in cellulose breakdown in sediments of wetlands with different origins in Hokkaido. Fish Sci 78: 699-706.
75. Liu W, Toyohara H (2012) Sediment-complex-binding cellulose breakdown in wetlands of rivers. Fish Sci 78: 661-665.
76. Dehal P, Satou Y, Campbell RK, Chapman J et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298: 2157-2167.
77. Nakashima K, Yamada L, Satou Y, Azuma J, Satoh N (2004) The evolutionary origin of animal cellulose synthase. Dev Genes Evol 214: 81-88.
78. Bhat MK (2000) Cellulases and related enzymes in biotechnology. Biotechnol Adv 18: 355-383.
79. Murad HA, Azzaz HH (2010) Cellulase and dairy animal feeding. Biotechnology 9: 1-19.
80. Demirbas A (2007) Progress and recent trends in biofuels. Prog Energy Combust 33: 1-18.
81. Demain AL (2009) Biosolutions to the energy problem. J Ind Microbiol Biol 36: 319-332.
82. Yin QY, Teng YG, Li YH, Ding M, Zhao FK (2011) Expression and characterization of full-length Ampullaria crossean endoglucanase EG65s and their two functional modules. Biosci Biotech Biochem 75: 240-246.
83. Yanagisawa M, Ojima T, Nakasaki K (2011) Bioethanol from sea lettuce with the use of crude enzymes derived from waste. J Mater Cycl Waste Manag 13: 321-326.
84. Ohkuma M (2003) Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 61: 1-9.
85. Silina AV, Zhukova NV (2007) Growth variability and feeding of scallop Patinopecten yessoensis on different bottom sediments: evidence from fatty acid analysis. J Exp Mar Biol Ecol 348: 46-59.
86. Inoue A, Mashino C, Kodama T, Ojima T (2011) Protoplast preparation from Laminaria japonica with recombinant alginate lyase and cellulase. Mar Biotechnol 13: 256-263.
87. Zhao FY, Lin JF, Zeng XL, Guo LQ, Wang YH, You LR (2010) Improvement in fruiting body yield by introduction of the Ampullaria crossean multi-functional cellulase gene into Volvariella volvacea. Bioresour Technol 101: 6482-6486.
88. Nozaki M, Miura C, Tozawa Y, Miura T (2009) The contribution of endogenous cellulase to the cellulose digestion in the gut of earthworm (Pheretima hilgendorfi: Megascolecidae). Soil Biol Biochem 41: 762-769.
89. Shimada K, Maekawa K (2008) Correlation between social structure and nymphal wood-digestion ability in the xylophagous cockroaches Salgallea esakii and Panesthia angustipennis (Blaberidae: Panesthiinae). Sociobiology 52: 417-427.
90. Tokuda G, Lo N, Watanabe H, Slaytor M, Matsumoto T, Noda H (1999) Metazoan cellulase genes from termites: intron/exon structures and site of expression. BBA Struct Expr 1447: 146-159.
91. Tokuda G, Lo N, Watanabe H, Arakawa G, Matsumoto T, Noda H (2004) Major alternation of the expression site of endogenous cellulases in members of an apical termite linage. Mol Ecol 13: 3219-3228.
92. Zhang DH, Lax AR, Bland JM, Allen AB (2011) Characterization of a new endogenous endo-beta-1, 4-glucanase of Formosan subterranean termite (Coptotermes formosanus). Insect Biochem Mol Biol 41: 211-218.
93. Zhang DH, Lax AR, Raina AK, Bland JM (2009) 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 39: 516-522.
94. Li L, Frohich J, Pfeiffer P, Konig H (2003) Termite gut symbiotic archaezoa are becoming living metabolic fossils. Eucaryot Cell 2: 1091-1098.
95. Scharf ME, Wu-Scharf D, Zhou X, Pittendrich BR, Bennett GW (2005) Gene expression profiles among immature and adult reproductive castes of the termite Reticulitermes flavipes. Insect Mol Biol 14: 31-44.
96. Itakura S, Masuta T, Tanaka H, Enoki A (2006) Identification of two subterranean termite species (Isoptera: Rhinotermitidae) using cellulase genes. J Econ Entomol 99: 123-128.
97. Kim N, Choo YM, Lee KS, Hong SJ, Seol KY, Je YH, Sohn HD, Jin BR (2008) Molecular cloning and characterization of a glycosyl hydrolase family 9 cellulase distributed throughout thr digestive tract of the cricket Teleogryllus emma. Comp Biochem Phys B 150: 368-376.
98. Ito K, Nozakli M, Ohta T, Miura C, Tozawa Y, Miura T (2011) Differences of two polychaete species reflected in enzyme activities. Mar Biol 158: 1211-1221.
99. Davison A, Blaxter ML (2005) An expression sequence tag survey of gene expression in the pond snail Lymnaea stagnalis, an intermediate vector of Fasciola hepatica. Parasitology 130: 539-552.
100. Clark NL, Gasper J, Sekino M, Springer SA, Aquadro CF, Swanson WJ (2009) Coevolution of interacting fertilization proteins. PLoS Genet 5: e1000570.
101. Crawford AC, Kricker JA, Anderson AJ, Richardson NR, Mather PB (2004) Structure and function of a cellulase gene in redclaw crayfish, Cherax quadricarinatus. Gene 340: 267-274.
102. Zhu XD, Mahairas G, Illies M, Cameron RA, Davidson EH, Ettensohn CA (2001) A large-scale analysis of mRNAs expressed by primary mesenchyme cells of the sea urchin embryo. Development 128: 2615-2627.
103. Edvardsen RB, Seo HC, Jensen MF, Mialon A, Mikhaleva J, Bjordal M, Cartry J, Reinhardt R, Weissenbach J, Wincker P, Chourrout D (2005) Remodeling of the homeobox gene complement in the tunicate Oikopleura dioica. Curr Biol 15: R12-R13.
104. Seo HC, Edvardsen RB, Maelnd AD, Bjordal M, Jansen MF, Hansen A, Flaat M, Weissenbach J, Lahrach H, Wincker P, Reinhardt R, Chourrout D (2004) Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431: 67-71.
105. Schloss PD, Delalibera I, Handelsman J, Radda KF (2006) Bacteria associated with the guts of two wood-boring beetles: Anoplophora glabripennis and Saperda vestita (Cerambycidae). Environ Entomol 35: 625-629.