Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera

Annual Review of Entomology

Volumn 43, Issue , 1998, Pages 17-37

  Douglas, A E ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Amino acids; Arthropod; Endosymbiosis; Mycetocyte; Nutrition

Indexed keywords

EID: 0031933648     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.ento.43.1.17     Document Type: Review

References (106)

1. Adams D. 1996. Host plant effects on an aphid-bacterial symbiosis. PhD thesis. Univ. York, United Kingdom, 102 pp.
2. Adams D, Douglas AE. 1997. How symbiotic bacteria influence plant utilization by the polyphagous aphid, Aphis fabae. Oecologia. In press
3. Aksoy S, Pourhosseini AA, Chow A. 1995. Mycetome endosymbionts of tsetse flies constitute a distinct lineage related to Enterobacteriaceae. Insect Mol. Biol. 4:15-22
4. Deleted in proof
5. Ball BV, Bailey L. 1978. The symbiotes of Myzus persicae (Sulz.) in strains resistant and susceptible to demeton-S-methyl. Pest. Sci. 9:522-24
6. Bandi C, Damiani G, Magrassi L, Grigolo A, Fani R, Sacchi L. 1994. Flavobacteria as intracellular symbionts in cockroaches. Proc. R. Soc. Lond. B 257:43-48
7. Barbosa P, Krischik VA, Jones CG, eds. 1991. Microbial Mediation of Plant-Herbivore Interactions. New York: Wiley & Sons
8. Baumann L, Baumann P. 1994. Growth kinetics of the endosymbiont Buchnera aphidicola in the aphid Schizaphis graminum. Appl. Environ. Microbiol. 60:3440-43
9. Baumann P, Baumann L, Clark MA. 1996. Levels of Buchnera aphidicola chaparonin GroEL during growth of the aphid Schizaphis graminum. Curr. Microbiol. 32:279-85
10. Baumann P, Lai C-Y, Roubakhsh D, Moran NA, Clark MA. 1995. Genetics, physiology, and evolutionary relationships of the genus Buchnera -intracellular symbionts of aphids. Annu. Rev. Microbiol. 49:55-94
11. Bracho AM, Martinez-Torres D, Moya A, Latorre A. 1995. Discovery and molecular characterization of a plasmid localized in Buchnera sp. bacterial endosymbiont of the aphid Rhopalosiphum padi. J. Mol. Evol. 41:67-73
12. Brough CN, Dixon AFG. 1990. Ultrastructural features of egg development in oviparae of the vetch aphid, Megoura viciae Buckton. Tissue Cell 22:51-63
13. Brown KS. 1975. The chemistry of aphids and scale insects. Chem. Soc. Rev. 4:263-88
14. Buchner P. 1965. Endosymbiosis of Animals with Plant Microorganisms. New York: Wiley & Sons
15. Campbell BC. 1990. On the role of microbial symbiotes in herbivorous insects. In Insect-Plant Interactions, ed. EA Bernays, 2:1-43. Boca Raton, FL: CRC Press
16. Campbell BC, Nes WD. 1983. A reappraisal of sterol biosynthesis and metabolism in aphids. J. Insect Physiol. 29:149-56
17. Chen D-Q, Campbell BC, Purcell AH. 1996. A new rickettsia from a herbivorous insect, the pea aphid Acyrthosiphon pisum (Harris). Curr. Microbiol. 33:123-28
18. Clark MA, Baumann L, Munson MA, Baumann P, Campbell BC. 1992. The eubacterial endosymbionts of whiteflies (Homoptera: Aleyrodoidea) constitute a lineage distinct from the endosymbionts of aphids and mealybugs. Curr. Microbiol. 25:119-23
19. Cochran DG. 1985. Nitrogen excretion in cockroaches. Annu. Rev. Entomol. 30:29-49
20. Dadd RH. 1985. Nutrition: organisms. In Comprehensive Insect Physiology Biochemistry and Pharmacology, ed. GA Kerkut, LI Gilbert, 4:313-91. Oxford: Pergamon
21. Dadd RH, Krieger DL. 1968. Dietary requirements of the aphid Myzus persicae. J. Insect Physiol. 14:741-64
22. Dadd RH, Krieger DL, Mittler TE. 1967. Studies on the artificial feeding of the aphid Myzus persicae. IV. Requirements for water-soluble vitamins and ascorbic acid. J. Insect Physiol. 13:249-72
23. de Renobles M, Cripps C, Stanley-Samuelson DW, Jurenka RA, Blomquist GJ. 1987. Biosynthesis of linoleic acid in insects. Trends Biochem. Sci. 12:364-66
24. de Renobles M, Ryan RO, Heisler CR, McLean DL, Blomquist GJ. 1986. Linoleic acid biosynthesis in the pea aphid, Acyrthosiphon pisum (Harris). Arch. Insect Biochem. Physiol. 3:193-203
25. Douglas AE. 1988. Sulphate utilisation in an aphid symbiosis. Insect Biochem. 18:599-605
26. Douglas AE. 1988. On the source of sterols in the green peach aphid, Myzus persicae, reared on holidic diets. Insect Biochem. 34:403-8
27. Douglas AE. 1988. Experimental studies on the mycetome symbiosis in the leafhopper Euscelis incisus. J. Insect Physiol. 34:1043-53
28. Douglas AE. 1989. Mycetocyte symbiosis in insects. Biol. Rev. 69:409-34
29. Douglas AE. 1990. Nutritional interactions between Myzus persicae and its symbionts. In Aphid-Plant Genotype Interactions, ed. RK Campbell, RD Eikenbary, pp. 319-27. Amsterdam: Elsevier
30. Douglas AE. 1992. Requirement of pea aphids (Acyrthosiphon pisum) for their symbiotic bacteria. Entomol. Exp. Appl. 65:195-98
31. Douglas AE. 1993. The nutritional quality of phloem sap utilized by natural aphid populations. Ecol. Entomol. 18:31-38
32. Douglas AE. 1994. Symbiotic Interactions. Cambridge: Oxford Univ. Press
33. Douglas AE. 1996. Reproductive failure and the amino acid pools in pea aphids (Acyrthosiphon pisum) lacking symbiotic bacteria. J. Insect Physiol. 42:247-55
34. Douglas AE. 1997. Parallels and contrasts between symbiotic bacteria and bacterial-derived organelles: evidence from Buchnera, the bacterial symbiont of aphids. FEMS Microbiol. Ecol. In press
35. Douglas AE, Dixon AFG. 1987. The mycetocyte symbiosis in aphids: variation with age and morph in virginoparae of Megoura viciae and Acyrthosiphon pisum. J. Insect Physiol. 33:109-13
36. Douglas AE, Prosser WA. 1992. Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. J. Insect Physiol. 38:565-8
37. Dreyer DL, Campbell BC. 1987. Chemical basis of host-plant resistance to aphids. Plant Cell Environ. 10:353-61
38. Ehrhardt P. 1968. Die Wirking verscheidener Spurenelemente auf Wachstum. Reproduktion und Symionten von Neomyzus circumflexus Buckt. (Aphidae Homoptera: Insecta) bei kunstlicher Ernahrung. Z. Vgl. Physiol. 58:47-75
39. 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
40. Fukatsu T, Aoki S, Kurosu U, Ishikawa H. 1994. Phylogeny of Cerataphidini aphids revealed by their symbiotic microorganisms and basic structure of their galls: implications for host-symbiont coevolution and evolution of sterile soldier castes. Zool. Sci. 11:613-23
41. Fukatsu T, Ishikawa H. 1992. Soldier and male of an eusocial aphid Colophina arma lack endosymbiont: implications for physiological and evolutionary interaction between host and symbiont. J. Insect Physiol. 38:1033-42
42. Fukatsu T, Ishikawa H. 1996. Phylogenetic position of yeast-like symbiont of Hamiltonaphis styraci (Homoptera, Aphididae) based on 18S rDNA sequence. Insect Biochem. Mol. Biol. 26:383-88
43. Grenier A-M, Nardon C, Rahbe Y. 1994. Observations on the microorganisms occurring in the gut of the pea aphid Acyrthosiphon pisum. Entomol. Exp. Appl. 70:91-96
44. Griffiths GW, Beck SD. 1974. Effects of antibiotics on intracellular symbiotes in the pea aphid Acyrthosiphon pisum. Cell Tissue Res. 48:287-300
45. Guldemond JA. 1990. Evolutionary genetics of the aphid Cryptomyzus with a preliminary analysis of host plant preference, reproductive performance and host alternation. Entomol. Exp. Appl. 57:65-76
46. Harada H, Ishikawa H. 1993. Gut microbe of aphid closely related to its intracellular symbiont. BioSystems 31:185-91
47. Harada H, Oyaizu H, Ishikawa H. 1996. A consideration about the origin of aphid intracellular symbiont in connection with gut bacterial flora. J. Gen. Appl. Microbiol. 42:17-26
48. Harrison CP, Douglas AE, Dixon AFG. 1989. A rapid method to isolate symbiotic bacteria from aphids. J. Invert. Pathol. 53:427-28
49. Heie OE. 1980. The Aphidoidea of Fennoscandia and Denmark. I. Introduction and the families Mindarideae, Hormaphididae, Thelaxidae, Anoeciidae, and Pemphigidae. Fauna Entomol. Scand. 9:1-236
50. Hinde R. 1971. The control of the my cetocyte symbiotes of the aphids Brevicoryne brassicae, Myzus persicae and Macrosiphum rosae. J. Insect Physiol. 17:1791-800
51. Hinde R. 1971. Maintenance of aphid cells and the intracellular symbiotes of aphids in vitro. J. Invert. Pathol. 17:333-38
52. Hongoh Y, Ishikawa H. 1994. Changes in the mycetocyte symbiosis in response to flying behaviour of alatiform aphid (Acyrthosiphon pisum) Zool. Sci. 11:731-35
53. Houk EJ, Griffiths GW. 1980. Intracellular symbiotes of the Homoptera. Annu. Rev. Entomol. 25:161-87
54. Houk EJ, McLean DL. 1974. Isolation of the primary intracellular symbiote in the pea aphid, Acyrthosiphon pisum. J. Invert. Pathol. 23:237-41
55. Humphreys NJ. 1996. Symbiosis and embryo production in the aphid symbiosis. PhD thesis. Univ. York, United Kingdom. 162 pp.
56. Iimura Y, Sasaki T, Fukatsu T, Ishikawa H. 1995. Diminution of intracellular symbiont of aphid maintained on artificial diet - a morphological study. Zool. Sci. 12:795-99
57. Ishikawa H. 1981. Isolation of the intracellular symbionts and partial characterisation of their RNA species of the elder aphid Acyrthosiphon pisum. Comp. Biochem. Physiol. 72B:239-47
58. Ishikawa H. 1984. Characterization of the protein species synthesized in vivo and in vitro by an aphid endosymbiont. Insect Biochem. 14:417-25
59. Ishikawa H, Yamaji M. 1985. Symbionin, an aphid endosymbiont-specific protein - I. Production of insects deficient in symbiont. Insect Biochem. 16:155-63
60. Jones CG. 1984. Microorganisms as mediators of plant resource exploitation by insect herbivores. In A New Ecology: Novel Approaches to Interactive Systems, ed. PW Price, CN Slobodchikoff, WS Gand, pp. 53-99. New York: Wiley & Sons
61. Kolibachuk D, Baumann P. 1995. Armonatic amino acid biosynthesis in Buchnera aphidicola (endosymbiont of aphids): cloning and sequencing of a DNA fragment containing aroH-thrS-infC-rpmL-rplT. Curr. Microbiol. 30:313-16
62. Lai C-Y, Baumann L, Baumann P. 1994. Amplification of trpEG; adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. Proc. Natl. Acad. Sci. USA 91:3819-23
63. Lai C-Y, Baumann P, Moran NA. 1995. Genetics of the tryptophan biosynthetic pathway of the prokaryotic endosymbiont (Buchnera) of the aphid Schlechtendalia chinensis. Insect Mol. Biol. 4:47-59
64. Lai C-Y, Baumann P, Moran NA. 1996. The endosymbiont (Buchnera sp.) of the aphid Diuraphis noxia contains plasmids consisting of trpEG and tandem repeats of trpEG pseudogenes. Appl. Environ. Microbiol. 62:332-39
65. Liadouze I, Febvay G, Guillaud J, Bonnot G. 1995. Effect of diet on the free amino acid pools of symbiotic and aposymbiotic pea aphids, Acyrthosiphon pisum. J. Insect Physiol. 41:33-40
66. Mittler TE. 1971. Dietary amino acid requirement of the aphid Myzus persicae affected by antibiotic uptake. J. Nutr. 101:1023-28
67. Montllor CB. 1991. The influence of plant chemistry on aphid feeding behavior. In Insect-Plant Interactions, ed. EA Bernays, 3:125-73. Boca Raton, FL: CRC Press
68. Moran NA. 1992. Evolution of aphid life cycles. Annu. Rev. Entomol. 37:321-28
69. Moran NA, Baumann P. 1994. Phylogenetics of cytoplasmically-inherited microorganisms of arthropods. Trends Ecol. Evol. 9:15-20
70. Moran NA, Munson MA, Baumann P, Ishikawa H. 1993. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc. R. Soc. Lond. B 253:167-71
71. Munderloh UG, Kurtti TJ. 1995. Cellular and molecular interrelationships between ticks and prokaryotic tick-borne pathogens. Annu. Rev. Entomol. 40:221-43
72. Munson MA, Baumann P. 1993. Molecular cloning and nucleotide sequence of a putative trpDC(F)BA operon in Buchnera aphidicola (endosymbiont of the aphid Schizaphis graminum. J. Bacteriol. 175:6426-32
73. Munson MA, Baumann P, Clark MA, Baumann L, Moran NA, et al. 1991. Evidence for the establishment of aphideubacterium endosymbiosis in an ancestor of four aphid families. J. Bacteriol. 173:6321-24
74. Munson MA, Baumann P, Kinsey MG. 1991. Buchnera gen. nov. and Buchnera aphidicola sp. nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. Int. J. Syst. Bacteriol. 41:566-68
75. Munson MA, Baumann P, Moran NA. 1992. Phylogenetic relationships of the endosymbionts of mealybugs (Homoptera: Pseudococcidae) based on 16S rDNA sequences. Mol. Phylogen. Evol. 1:26-30
76. Noda H, Kodama K. 1996. Phylogenetic position of yeastlike endosymbionts of anobiid beetles. Appl. Environ. Microbiol. 62:162-67
77. Noda H, Nakashima N, Koizumi M. 1995. Phylogenetic position of yeastlike symbiotes of rice planthoppers based on partial 18S rDNA sequences. Insect Biochem. Mol. Biol. 25:639-36
78. Potrikus CJ, Breznak JA. 1981. Gut bacteria recycle uric acid nitrogen in termites: a strategy for nutrient conservation. Proc. Natl. Acad. Sci USA 78:4601-5
79. Prosser WA, Douglas AE. 1991. The aposymbiotic aphid: an analysis of chlortetracycline-treated pea aphid, Acyrthosiphan pisum. J. Insect Physiol. 37:713-19
80. Prosser WA, Douglas AE. 1992. A test of the hypotheses that nitrogen is upgraded and recycled in an aphid (Acyrthosiphon pisum) symbiosis. J. Insect Physiol. 38:93-99
81. Prosser WA, Simpson SJ, Douglas AE. 1992. How an aphid (Acyrthosiphon pisum) symbiosis responds to variation in dietary nitrogen. J. Insect Physiol. 38:301-7
82. Rahbe Y, Delobel B, Febvay G, Chantegrel B. 1994. Aphid-specific triglycerides in symbiotic and aposymbiotic Acyrthosiphon pisum. Insect Biochem. Mol. Biol. 24:95-101
83. Rouhbakhsh D, Lai C-Y, von Dohlen C, Clark MA, Baumann L, et al. 1996. Thr tryptophan biosynthetic pathway of aphid endosymbionts (Buchnera): genetics and evolution of plasmid-associated anthranilate synthase (trpEG) within the Aphididae. J. Mol. Evol. 42:414-21
84. Roubakhsh D, Moran NA, Baumann L, Voegtlin DJ, Baumann P. 1994. Polymerase chain reaction-based identification of Buchnera: the primary prokaryotic endosymbiont of aphids. Insect Mol. Biol. 3:213-17
85. Ruby EG. 1996. Lessons from a cooperative bacterial-animal association: the Vibrio fischeri-Euprymna scolopes light organ symbiosis. Annu. Rev. Microbiol. 50:591-624
86. Sander K. 1977. Anomalien der Oogenese und Embryogenese symbiontenfuhrender Kleinzikaden unter Tetracyclin-Einfluss. Verhand. Deutsch. Zool. Gesell. 1977:306
87. 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
88. Sasaki T, Hayashi H, Ishikawa H. 1991. Growth and reproduction of the symbiotic and aposymbiotic pea aphids, Acyrthosiphon pisum maintained on artificial diets. J. Insect Physiol. 37:749-56
89. 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
90. Sasaki T, Kawamura M, Ishikawa H. 1996. Nitrogen recycling in the brown planthopper, Nilaparvata lugens: involvement of yeast-like endosymbionts in uric acid metabolism. J. Insect Physiol. 42:125-30
91. Schroeder D, Deppisch H, Obermayer M, Krohne G, Stackbrandt E, et al. 1996. Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Mol. Microbiol. 21:479-89
92. Schwemmler W, Duthoit JJ, Kuhl G, Vago C. 1974. Endosymbionts: factors of egg pattern formation. J. Insect Physiol. 20:1467-74
93. Srivastava PN, Gao Y, Levesque J, Auclair JL. 1985. Differences in amino acid requirement between two biotypes of the pea aphid, Acyrthosiphon pisum. Can. J. Zool. 63:603-6
94. Tjallingii WF. 1995. Regulation of phloem feeding by aphids. In Regulatory Mechanisms in Insect Feeding, ed. RF Chapman, G de Boer, pp. 190-209. New York: Chapman & Hall
95. Unterman BM, Baumann P, McLean DL. 1989. Pea aphid symbiont relationships established by analysis of 16S rRNAs. J. Bacteriol. 171:2970-74
96. van den Heuvel JFJM, Verbeek M, van der Wilk F. 1994. Endosymbiotic bacteria associated with circulative transmission of potato virus by Myzus persicae. J. Gen. Virol. 75:2559-65
97. van Rhijn P, Vanderleyden J. 1995. The Rhizobium-plant symbiosis. Microbiol. Rev. 59:124-42
98. von Amiressami M, Petzold H. 1976. Symbioseforschung und Insektizidresistenz. Ein licht-und elektronenmikroscopisher Beitrag zur Klarung der Insektizidresistenz von Aphiden unter Berucksichtigung der Mycetom-Symbionten bei Myzus persicae Sulz. Angew. Entomol. 82:252-59
99. Walters FS, Mullin CA. 1994. Biosynthetic alternatives for acetogenic production of sorbic acid in the potato aphid (Homoptera: Aphididae). Arch. Insect Biochem. Physiol. 27:249-64
100. Walters FS, Mullin CA, Gildow FE. 1994. Biosynthesis of sorbic acid in aphids: an investigation into symbiont involvement and potential relationships with aphid pigments. Arch. Insect Biochem. Physiol. 26:49-67
101. Whitehead LF, Douglas AE. 1993. Populations of symbiotic bacteria in the parthenogenetic pea aphid (Acyrthosiphon pisum) symbiosis. Proc. R. Soc. Lond. B 254:29-32
102. Whitehead LF, Douglas AE. 1993. A metabolic study of Buchnera, the intracellular bacterial symbionts of the pea aphid, Acyrthosiphon pisum. J. Gen. Microbiol. 139:821-26
103. Whitehead LF, Wilkinson TL, Douglas AE. 1992. Nitrogen recycling in the pea aphid (Acyrthosiphon pisum) symbiosis. Proc. R. Soc. Lond. B 250:115-17
104. Wilkinson TL, Douglas AE. 1995. Aphid feeding, as influenced by the disruption of the symbiotic bacteria. J. Insect Physiol. 41:635-40
105. Wilkinson TL, Douglas AE. 1995. Why aphids lacking symbiotic bacteria have elevated levels of the amino acid glutamine. J. Insect Physiol. 41:921-27
106. Wilkinson TL, Douglas AE. 1996. The impact of aposymbiosis on amino acid metabolism of pea aphids. Entomol. Exp. Appl. 80:279-82