Aphid genome expression reveals host-symbiont cooperation in the production of amino acids

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 7, 2011, Pages 2849-2854

  Hansen, Allison K ^a   Moran, Nancy A ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Acyrthosiphon pisum; Animal nutrition; Coevolution; Microbiota; Nitrogen recycling

Indexed keywords

AMINO ACID; GLUTAMATE AMMONIA LIGASE; GLUTAMATE SYNTHASE;

AMINO ACID SYNTHESIS; APHID; ARTICLE; BUCHNERA; GENE EXPRESSION; GENE SEQUENCE; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SYMBIONT; UPREGULATION;

AMINO ACIDS, ESSENTIAL; ANIMALS; APHIDS; BASE SEQUENCE; BUCHNERA; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; GLUTAMATE SYNTHASE; GLUTAMATE-AMMONIA LIGASE; MOLECULAR SEQUENCE DATA; QUATERNARY AMMONIUM COMPOUNDS; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY; SYMBIOSIS;

ACYRTHOSIPHON PISUM; ANIMALIA; APHIDIDAE; BACTERIA (MICROORGANISMS); BUCHNERA (PROTEOBACTERIA);

EID: 79952612931     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1013465108     Document Type: Article

References (44)

1. Slansky FJ, Scriber JM (1985) Food consumption and utilization. Comprehensive Insect Physiology, Biochemistry and Pharmacology, eds Kerkut GA, Gilbert LI (Pergamon, Oxford), Vol 4, pp 87-163.
2. Sandström J, Pettersson J (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea apid (Acyrthosiphon pisum) performance. J Insect Physiol 40:947-955. (Pubitemid 2161542)
3. Sandström J, Moran N (1999) Amino acid budgets in three aphid species using the same host plant. Physiol Entomol 26:202-211. (Pubitemid 32918968)
4. Baumann P (2005) Biology bacteriocyte-associated endosymbionts of plant sapsucking insects. Annu Rev Microbiol 59:155-189.
5. Buchner P (1965) Endosymbiosis of Animals with Plant Microorganisms (Interscience, New York), p 909.
6. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81-86.
7. Douglas AE, Prosser WA (1992) Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. J Insect Physiol 38:565-568.
8. Wilson ACC, et al. (2010) Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol Biol 19 (Suppl 2):249-258.
9. Douglas AE (1988) Sulphate utilisation in an aphid symbiosis. Insect Biochem 18: 599-605.
10. Sasaki T, Fukuchi N, Ishikawa H (1993) Amino acid flow through aphid and its symbiont: Study with 15N-labeled glutamine. Zoolog Sci 10:787-791.
11. Baumann P, et al. (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: Intracellular symbionts of aphids. Annu Rev Microbiol 49:55-94.
12. Febvay G, Liadouze I, Guillaud J, Bonnot G (1995) Analysis of energetic amino acid metabolism in Acyrthosiphon pisum: A multidimensional approach to amino acid metabolism in aphids. Arch Insect Biochem Physiol 29:45-69.
13. International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8:e1000313.
14. Nakabachi A, et al. (2005) Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. Proc Natl Acad Sci USA 102:5477-5482. (Pubitemid 40530283)
15. Sandström J, Moran N (1999) How nutritionally imbalanced is phloem sap for aphids? Entomol Exp Appl 91:203-210.
16. Whitehead LF, Wilkinson TL, Douglas AE (1992) Nitrogen recycling in the pea aphid symbiosis. Proc Biol Sci 250:115-117. (Pubitemid 24408837)
17. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165-190.
18. Moran NA, McLaughlin HJ, Sorek R (2009) The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323:379-382.
19. Sasaki T, Aoki T, Hayashi H, Ishikawa H (1990) Amino acid composition of the honeydew of symbiotic and aposymbiotic pea aphids Acyrthosiphon pisum. J Insect Physiol 36:35-40.
20. Akman Gündüz E, Douglas AE (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc Biol Sci 276:987-991.
21. Sasaki T, Ishikawa H (1995) Production of essential amino acids from glutamate by mycetocyte symbionts of the pea aphid, Acyrthosiphon pisum. J Insect Physiol 41:41-46.
22. Sasaki T, Ishikawa H (1993) Nitrogen recycling in the endosymbiotic system of the pea aphid, Acyrthosiphon pisum. Zoolog Sci 10:779-785. (Pubitemid 2006339)
23. Moran NA, Dunbar HE, Wilcox JL (2005) Regulation of transcription in a reduced bacterial genome: Nutrient-provisioning genes of the obligate symbiont Buchnera aphidicola. J Bacteriol 187:4229-4237. (Pubitemid 40827805)
24. Klowden M (2002) Physiological Systems in Insects (Academic, San Diego).
25. Wilkinson TL, Douglas AE (1995) Why aphids lacking symbiotic bacteria have elevated levels of the amino acid glutamine. J Insect Physiol 41:921-927.
26. Buchanan B, Gruissem W, Jones R (2000) Biochemistry and Molecular Biology of Plants, eds American Society of Plant Physiologists (Courier Companies, Inc., Waldorf, MD).
27. Helling R (1998) Pathway choice in glutamate synthesis in Escherichia coli. J Bacteriol 17:4571-4575.
28. Drews M, et al. (2000) Pathways of glutamine metabolism in Spodoptera frugiperda (Sf9) insect cells: Evidence for the presence of the nitrogen assimilation system, and a metabolic switch by 1H/15N NMR. J Biotechnol 78:23-37. (Pubitemid 30084787)
29. Campbell MK, Farrell SO (2006) Biochemistry (Thompson Brooks/Cole, Belmont, CA)5th Ed.
30. Becker A, Schlöder P, Steele JE, Wegener G (1996) The regulation of trehalose metabolism in insects. Experientia 52:433-439. (Pubitemid 26158611)
31. 15N]-labeled compounds and mass spectrometry. Insect Biochem Mol Biol 36:614-622.
32. Scaraffia PY, Zhang Q, Thorson K, Wysocki VH, Miesfeld RL (2010) Differential ammonia metabolism in Aedes aegypti fat body and midgut tissues. J Insect Physiol 56:1040-1049.
33. Shinbo H, Konno K, Hirayama C (1997) The pathway of ammonia assimilation in the silkworm, Bombyx mori. J Insect Physiol 43:959-964. (Pubitemid 27521877)
34. Hirayama C, Saito H, Konno K, Shinbo H (1998) Purification and characterization of NADH-dependent glutamate synthase from the silkworm fat body (Bombyx mori). Insect Biochem Mol Biol 28:473-482. (Pubitemid 28372902)
35. Hirayama C, Nakamura M (2002) Regulation of glutamine metabolism during the development of Bombyx mori larvae. Biochim Biophys Acta 1571:131-137. (Pubitemid 34607371)
36. Scaraffia PY, Isoe J, Murillo A, Wells MA (2005) Ammonia metabolism in Aedes aegypti. Insect Biochem Mol Biol 35:491-503. (Pubitemid 40440940)
37. Gerardo NM, et al. (2010) Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol 11:R21.
38. Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100:1803-1807. (Pubitemid 36254529)
39. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621-628. (Pubitemid 351911867)
40. Kal AJ, et al. (1999) Dynamics of gene expression revealed by comparison of serial analysis of gene expression transcript profiles from yeast grown on two different carbon sources. Mol Biol Cell 10:1859-1872. (Pubitemid 29272637)
41. Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27-30. (Pubitemid 30047706)
42. Chang A, Scheer M, Grote A, Schomburg I, Schomburg D (2009) BRENDA, AMENDA and FRENDA the enzyme information system: New content and tools in 2009. Nucleic Acids Res 37(Database issue):D588-D592.
43. Keseler IM, et al. (2009) EcoCyc: A comprehensive view of Escherichia coli biology. Nucleic Acids Res 37(Database issue):D464-D470.
44. AcypiCyc (2010) AcypiCyc database, NRIA Bamboo team-project. Database is hosted at the Pôle Rhône-Alpes de Bioinformatique (PRABI)Available at http://acypicyc.cycadsys.org/. Accessed June 1, 2010.