Carbohydrate metabolism genes and pathways in insects: insights from the honey bee genome

Abstract

Carbohydrate‐metabolizing enzymes may have particularly interesting roles in the honey bee, Apis mellifera , because this social insect has an extremely carbohydrate‐rich diet, and nutrition plays important roles in caste determination and socially mediated behavioural plasticity. We annotated a total of 174 genes encoding carbohydrate‐metabolizing enzymes and 28 genes encoding lipid‐metabolizing enzymes, based on orthology to their counterparts in the fly, Drosophila melanogaster, and the mosquito, Anopheles gambiae . We found that the number of genes for carbohydrate metabolism appears to be more evolutionarily labile than for lipid metabolism. In particular, we identified striking changes in gene number or genomic organization for genes encoding glycolytic enzymes, cellulase, glucose oxidase and glucose dehydrogenases, glucose‐methanol‐choline (GMC) oxidoreductases, fucosyltransferases, and lysozymes.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 63

1. 1.

   Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, et al. The genome sequence of Drosophila melanogaster. Science. 2000;287:2185-2195.

   Not in our library10.1126/science.287.5461.2185

2. 2.

   Aitman TJ, Dong R, Vyse TJ, Norsworthy PJ, Johnson MD, Smith J, Mangion J, Roberton-Lowe C, Marshall AJ, Petretto E, Hodges MD, Bhangal G, Patel SG, Sheehan-Rooney K, Duda M, Cook PR, Evans DJ, Domin J, Flint J, Boyle JJ, Pusey CD, Cook HT. Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature. 2006;439:851-855.

   Not in our library10.1038/nature04489

3. 3.

   Bachali S, Jager M, Hassanin A, Schoentgen F, Jolles P, Fiala-Medioni A, Deutch JS. Phylogenetic analysis of invertebrate lysozymes and the evolution of lysozyme function. J Mol Evol. 2002;54:652-664.

   Not in our library10.1007/s00239-001-0061-6

4. 4.

   Bak TG. Studies on glucose dehydrogenase of Aspergillus oryzae. II. Purification and physical and chemical properties. Biochim Biophys Acta. 1967;139:277-293.

   Not in our library10.1016/0005-2744(67)90032-0

5. 5.

   Beenakkers AMTh, van der Horst DJ, van Marrewijk WJA. Insect flight muscle metabolism. Insect Biochem. 1984;14:243-260.

   Not in our library

6. 6.

   Bentley R, Boyer PD, Lardy H, Myrbak K. Glucose oxidase. The Enzymes. 1963;7:567-584.

   Not in our library

7. 7.

   Byrne KA, Lehnert SA, Johnson SE, Moore SS. Isolation of a cDNA encoding a putative cellulase in the red claw crayfish Cherax quadricarinatus. Gene. 1999;239:317-324.

   Not in our library10.1016/s0378-1119(99)00396-0

8. 8.

   Crane E. The removal of water from honey. Bee World. 1996;77:120-129.

   Not in our library

9. 9.

   Daffre S, Kylsten P, Samakovlis C, Hultmark D. The lysozyme locus in Drosophila melanogaster: an expanded gene family adapted for expression in the digestive tract. Mol Gen Genet. 1994;242:152-162.

   Not in our library10.1007/bf00391008

10. 10.

    Davison A, Blaxter M. Ancient Origin of Glycosyl Hydrolase Family 9 Cellulase Genes. Mol Biol Evol. 2005;22:1273-1284.

    Not in our library10.1093/molbev/msi107

11. 11.

    Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, et al. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science. 2002;298:2157-2167.

    Not in our library10.1126/science.1080049

12. 12.

    Eichler EE, Sankoff D. Structural dynamics of eukaryotic chromosome evolution. Science. 2003;301:793-797.

    Not in our library10.1126/science.1086132

13. 13.

    Ellison RT, Giehl TJ. Killing of gram-negative bacteria by lactoferrin and lysozyme. J Clin Invest. 1991;88:1080-1091.

    Not in our library10.1172/jci115407

14. 14.

    Ghisalberti EL. Propolis: a review. Bee World. 1979;60:59-84.

    Not in our library

15. 15.

    Gillett JD. Mosquitos. 1971.

    Not in our library

16. 16.

    Gmeinbauer R, Crailsheim K. Glucose ulitilzation during flight of honeybee (Apis mellifera) workers, drones and queens. J Insect Physiol. 1993;39:959-967.

    Not in our library

17. 17.

    Grogan DE, Hunt JH. Pollen proteases: their potential role in insect digestion. Insect Biochem. 1979;9:309-313.

    Not in our library

18. 18.

    Harrison JF, Roberts SP. Flight respiration and energetics. Annu Rev Physiol. 2000;62:179-205.

    Not in our library10.1146/annurev.physiol.62.1.179

19. 19.

    Harrison JM. Caste-specific changes in honeybee flight capacity. Physiol Zool. 1986;59:175-187.

    Not in our library

20. 20.

    Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, et al. The genome sequence of the malaria mosquito Anopheles gambiae. Science. 2002;298:129-149.

    Not in our library10.1126/science.1076181

21. 21.

    Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 2006.

    Not in our library10.1038/nature05260

22. 22.

    Hrassnigg N, Crailsheim K. Differences in drone and worker physiology in honeybees (Apis mellifera). Apidologie. 2005;36:255-277.

    Not in our library

23. 23.

    Hrassnigg N, Brodschneider R, Fleischmann PH, Crailsheim K. Unlike nectar foragers, honeybee drones (Apis mellifera) are not able to utilize starch as fuel for flight. Apidologie. 2005;36:547-557.

    Not in our library

24. 24.

    Hultmark D, Jolles P. Insect lysozymes. Lysozymes: Model Enzymes in Biochemistry and Biology. 1996;87-102.

    Not in our library

25. 25.

    Hurd EA, Domino SE. Increased susceptibility of secretor factor gene Fut2-null mice to experimental vaginal candidiasis. Infection Immunity. 2004;72:4279-4281.

    Not in our library10.1128/iai.72.7.4279-4281.2004

26. 26.

    Ito Y, Yoshikawa A, Hotani T, Fukuda S, Sugimura K, Imono T. Amino acid sequences of lysozymes newly purified from invertebrates imply wide distribution of a novel class in the lysozyme family. Eur J Biochem. 1999;259:456-461.

    Not in our library10.1046/j.1432-1327.1999.00064.x

27. 27.

    Iwamori M, Domino SE. Tissue-specific loss of fucosylated glycolipids in mice with targeted deletion of α (1,2) fucosyltransferase genes. Biochem J. 2004;380:75-81.

    Not in our library10.1042/bj20031668

28. 28.

    Javaud C, Dupuy F, Maftah A, Julien R, Petit JM. The fucosyltransferase gene family: an amazing summary of the underlying mechanisms of gene evolution. Genetica. 2003;118(2–3):157-170.

    Not in our library

29. 29.

    Jolles P, Jolles J. What's new in lysozyme research? Always a model system, today as yesterday. Mol Cell Biochem. 1984;63:165-189.

    Not in our library10.1007/bf00285225

30. 30.

    Kanehisa M, Goto S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 2000;28:27-30.

    Not in our library10.1093/nar/28.1.27

31. 31.

    Klowden MJ. Physiological Systems in Insects. 2002.

    Not in our library

32. 32.

    Knox RB, Heslop-Harrison J. Pollen-wall proteins: localization and enzymatic activity. J Cell Sci. 1970;6:1-27.

    Not in our library10.1242/jcs.6.1.1a

33. 33.

    Kubelka V, Altmann F, Staudacher E, Tretter V, Marz L, Hard K, Kamerling JP, Vliegenthart FG. Primary structures of the N-linked carbohydrate chains from honeybee venom phopholipase A2. Eur J Biochem. 1993;213:1193-1204.

    Not in our library10.1111/j.1432-1033.1993.tb17870.x

34. 34.

    Kubo T, Sasaki M, Nakamura J, Sasagawa H, Ohashi K, Takeuchi H, Natori S. Change in the expression of hypopharyngeal-gland proteins of the worker honeybees (Apis mellifera L.) with age and/or role. J Biochem. 1996;119:291-295.

    Not in our library10.1093/oxfordjournals.jbchem.a021237

35. 35.

    Lo N, Watanabe H, Sugimura M. Evidence for the presence of a cellulase gene in the last common ancestor of bilaterian animals. Proc Roy Soc Lond B Biol Sci. 2003;270:S69-S72.

    Not in our library10.1098/rsbl.2003.0016

36. 36.

    Martinez-Duncker I, Mollicone R, Candelier JJ, Breton C, Oriol R. A new superfamily of protein-O- fucosyltransferases, alpha2-fucosyltransferases, and alpha6-fucosyltransferases: phylogeny and identification of conserved peptide motifs. Glycobiology. 2003;13:1C-5C.

    Not in our library10.1093/glycob/cwg113

37. 37.

    Michener CD. The Social Behavior of the Bees: a Comparative Study. 1974.

    Not in our library

38. 38.

    Micheu S, Crailsheim K, Leonhard B. Importance of proline and other amino acids during honey bee flight (Apis mellifera carnica Pollmann). Amino Acids. 2000;18:157-175.

    Not in our library10.1007/s007260050014

39. 39.

    Nakashima K, Watanabe H, Saitoh H, Tokuda G, Azuma JI. Dual cellulose-digesting system of the wood-feeding termite, Coptotermes formosanus Shiraki. Insect Biochem Mol Biol. 2002;32(7):777-784.

    Not in our library10.1016/s0965-1748(01)00160-6

40. 40.

    Nayar JK, van Handel E. The fuel for sustained mosquito flight. J Insect Physiol. 1971;17:471-481.

    Not in our library10.1016/0022-1910(71)90095-3

41. 41.

    Neukirch A. Dependence of the life span of the honeybee (Apis mellifica) upon flight performance and energy consumption. J Comp Physiol. 1982;146:35-40.

    Not in our library

42. 42.

    Ohashi K, Sawata M, Takeuchi H, Natori S, Kubo T. Molecular cloning of cDNA and analysis of expression of the gene for α-glucosidase from the hypopharyngeal gland of the honeybee. Biochem Biophys Res Commun. 1996;221:380-385.

    Not in our library10.1006/bbrc.1996.0604

43. 43.

    Ohashi K, Natori S, Kubo T. Change in the mode of gene expression of the hypopharyngeal gland cells with an age-dependent role change of the worker honeybee Apis mellifera L. Eur J Biochem. 1997;249:797-802.

    Not in our library10.1111/j.1432-1033.1997.t01-1-00797.x

44. 44.

    Ohashi K, Natori S, Kubo T. Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependent role change of the worker honeybee (Apis mellifera L.). Eur J Biochem. 1999;265:127-133.

    Not in our library10.1046/j.1432-1327.1999.00696.x

45. 45.

    Panzenbock U, Crailsheim K. Glycogen in honeybee queens, workers and drones (Apis mellifera carnica Pollm). J Insect Physiol. 1997;43:155-165.

    Not in our library10.1016/s0022-1910(96)00079-0

46. 46.

    Regel R, Matioli SR, Terra WR. Molecular adaptation of Drosophila melanogaster lysozymes to a digestive function. Insect Biochem Mol Biol. 1998;28:309-319.

    Not in our library10.1016/s0965-1748(97)00108-2

47. 47.

    Robinson GE. Genomics and integrative analyses of division of labor in honey bee colonies. Am Nat. 2002;160:S160-S172.

    Not in our library10.1086/342901

48. 48.

    Roos C, Kolmer M, Mattila P, Renkonen R. Composition of Drosophila melanogaster proteome involved in fucosylated glycan metabolism. J Biol Chem. 2002;277:3168-3175.

    Not in our library10.1074/jbc.m107927200

49. 49.

    Schulz DJ, Huang ZY, Robinson GE. Effects of colony food shortage on behavioral development in honey bees. Behav Ecol Sociobiol. 1998;42:295-303.

    Not in our library

50. 50.

    Seeley TD. The Wisdom of the Hive. 1995.

    Not in our library

51. 51.

    Simpson J, Riedel IBM, Wilding M. Invertase in the hypopharyngeal gland in adult worker honey bees. Apidologie. 1968;21:457-468.

    Not in our library

52. 52.

    Soliman MH, van Herrewege J, Lints FA, Soliman MH. Nutrition. Drosophila as a Model Organism for Ageing Studies. 1988;46-57.

    Not in our library

53. 53.

    Stabentheiner A, Pressl H, Papst T, Hrassnigg N, Crailsheim K. Endothermic heat production in honeybee winter clusters. J Exp Biol. 2003;206:353-358.

    Not in our library10.1242/jeb.00082

54. 54.

    Surholt B, Newsholme EA. Maximum activities and properties of glucose- 6-phosphatase in muscles from vertebrates and invertebrates. Biochem J. 1981;198:621-629.

    Not in our library10.1042/bj1980621

55. 55.

    Suzuki K, Ojima T, Nishita K. Purification and cDNA cloning of a cellulase from abalone Haliotis discus Hannai. Eur J Biochem. 2003;270:771-778.

    Not in our library10.1046/j.1432-1033.2003.03443.x

56. 56.

    Tokuda G, Lo N, Watanabe H, Slaytor M, Matsumoto T, Noda H. Metazoan cellulase genes from termites: intron/exon structures and sites of expression. Biochim Biophys Acta. 1999;1447:146-159.

    Not in our library10.1016/s0167-4781(99)00169-4

57. 57.

    Tomme P, Warren RAJ, Gilkes NR. Cellulose hydrolysis by bacteria and fungi. Adv Microbiol Physiol. 1995;37:1-81.

    Not in our library10.1016/s0065-2911(08)60143-5

58. 58.

    Toth AL, Kantarovich S, Meisel AF, Robinson GE. Nutritional status influences socially regulated foraging ontogeny in honey bees. J Exp Biol. 2005;208:4641-4649.

    Not in our library10.1242/jeb.01956

59. 59.

    Watanabe H, Noda H, Tokuda G, Lo N. A cellulase gene of termite origin. Nature. 1998;394:330-331.

    Not in our library10.1038/28527

60. 60.

    White JW, Subers MH, Schepartz AI. The identification of inhibine, antibacterial factor in the honey, as hydrogen peroxide, and its origin in a honey glucose oxidase. Biochem Biophys Acta. 1963;73:57-70.

    Not in our library10.1016/0006-3002(63)90359-7

61. 61.

    Whitfield CW, Band MR, Bonaldo MF, Kumar CG, Liu L, Pardinas JR, Robertson HM, Soares MB, Robinson GE. Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee. Genome Res. 2002;12:555-566.

    Not in our library10.1101/gr.5302

62. 62.

    Whitfield CW, Cziko AM, Robinson GE. Gene expression profiles in the brain predict behavior in individual honey bees. Science. 2003;302:296-299.

    Not in our library10.1126/science.1086807

63. 63.

    Winston ML. The Biology of the Honeybee. 1987.

    Not in our library

Cited by papers we hold 1

• Gut Pathology and Responses to the Microsporidium Nosema ceranae in the Honey Bee Apis mellifera · 2012
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.