How conserved are the bacterial communities associated with aphids? A detailed assessment of the brevicoryne brassicae (Hemiptera: Aphididae) using 16S rDNA

Environmental Entomology

Volumn 41, Issue 6, 2012, Pages 1386-1397

  Clark, E L ^a,b,c   Daniell, T J ^a   Wishart, J ^a,d   Hubbard, S F ^a,b,d   Karley, A J ^a  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c ROYAL VETERINARY COLLEGE   (United Kingdom)

^d UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

16S ribosomal DNA; bacterial community; Brevicoryne brassicae; endosymbiont; real time qPCR

Indexed keywords

BACTERIAL DNA; RIBOSOME DNA;

APHID; BACTERIUM; BIOLOGICAL CONTROL; ENDOSYMBIONT; LEAFY VEGETABLE; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; MITOCHONDRIAL DNA; NATURAL ENEMY; PATHOGEN; POLYMERASE CHAIN REACTION; REAL TIME;

ANIMAL; APHID; ARTICLE; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ENTEROBACTERIACEAE; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; PSEUDOMONAS; STATISTICAL MODEL;

ANIMALS; APHIDS; BIODIVERSITY; DNA, BACTERIAL; DNA, RIBOSOMAL; ENTEROBACTERIACEAE; LIKELIHOOD FUNCTIONS; PHYLOGENY; PSEUDOMONAS; SEQUENCE ANALYSIS, DNA;

UNITED KINGDOM;

APHIDIDAE; BACTERIA (MICROORGANISMS); BREVICORYNE BRASSICAE; ENTEROBACTERIACEAE; ENTEROBACTERIALES; HEMIPTERA; HEXAPODA;

EID: 84871555042     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/EN12152     Document Type: Article

References (65)

1. Acinas, S. G., L. A. Marcelino, V. Klepac-Ceraj, and M. F. Polz. 2004. Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J. Bacteriol. 186: 2629-2635.
2. Allen, A. E., M. G. Booth, M. E. Frischer, P. G. Verity, J. P. Zehr, and S. Zani. 2001. Diversity and detection of nitrate assimilation genes in marine bacteria. Appl. Environ. Microbiol. 67: 5343-5348.
3. Anzai, Y., H. Kim, J-Y. Park, H. Wakabayashi, and H. Oyaizu. 2000. Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int. J. Syst. Evol. Microbiol. 50: 1563-1589.
4. Bacci, L., M. C. Picanco, J. F. Rosado, G. A. Silva, A.L.B. Crespo, E.J.G. Pereira, and J. C. Martins. 2009. Conservation of natural enemies in brassica crops: comparative selectivity of insecticides in the management of Brevicoryne brassicae (Hemiptera: Sternorrhyncha: Aphididae). Appl. Entomol. Zool. 44: 103-113.
5. Begon, M., J. L. Harper, and C. R. Townsend. 2006. Ecology: from individuals to ecosystems, 4th ed, pp. 471-472. Blackwell, Oxford, United Kingdom.
6. Bridges, M., A.M.E. Jones, A. M. Bones, C. Hodgson, R. Cole, E. Bartlet, R. Wallsgrove, V. K. Karapapa, N. Watts, and J. T. Rossiter. 2002. Spatial organization of the glucosinolate-myrosinase system in brassica specialist aphids is similar to that of the host plant. Proc. R. Soc. Lond. B. 269: 187-191.
7. Brown, E. W., R. M. Davis, C. Gouk, and T. van der Zwet. 2000. Phylogenetic relationships of necrogenic Erwinia and Brenneria species as revealed by glyceraldehyde-3-phosphate dehydrogenase gene sequences. Int. J. Syst. Evol. Microbiol. 50: 2057-2068.
8. Buchner, P. 1965. Endosymbiosis of animals with plant microorganisms. Interscience, New York, NY.
9. Chen, D-Q., C. B. Montllor, and A. H. Purcell. 2000. Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomol. Exp. Appl. 95: 315-323.
10. Clark, E. L., A. J. Karley, and S. F. Hubbard. 2010. Insect endosymbionts: manipulators of insect herbivore trophic interactions? Protoplasma 244: 25-51.
11. Costello, M. J., and M. A. Altieri. 1995. Abundance, growth rate and parasitism of Brevicoryne brassicae and Myzus persicae (Homoptera: Aphididae) on broccoli grown in living mulches. Agric. Ecosyst. Environ. 52: 187-196.
12. Darby, A. C., and A. E. Douglas. 2003. Elucidation of the transmission patterns of an insect-borne bacterium. Appl. Environ. Microbiol. 69: 4403-4407.
13. Darby, A. C., L. M. Birkle, S. L. Turner, and A. E. Douglas. 2001. An aphid-borne bacterium allied to the secondary symbionts of whitefly. FEMS Microbiol. Ecol. 36: 43-50.
14. D'Argenio, D. A., L. A. Gallagher, C. A. Berg, and C. Manoil. 2001. Drosophila as a model host for Pseudomonas aeruginosa infection. J. Bacteriol. 183: 1466-1471.
15. Douglas, A. E. 1998. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43: 17-37.
16. Douglas, A. E. 2009. The microbial dimension in insect nutritional ecology. Funct. Ecol. 23: 38-47.
17. Douglas, A. E., C.L.M. François, and L. B. Minto. 2006. Facultative ÔsecondaryÕ bacterial symbionts and the nutrition of the pea aphid, Acyrthosiphon pisum. Physiol. Entomol. 31: 262-269.
18. Ewing, B., and P. Green. 1998. Base-calling of automated sequencer traces using Phred. II. Error probabilities. Genome Res. 8: 186-194.
19. Ewing, B., L. Hillier, M. C. Wendl, and P. Green. 1998. Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res. 8: 175-185.
20. Ferrari, J., C. L. Scarborough, and H.C.J. Godfray. 2007. Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia 153: 323-329.
21. Ferrari, J., A. C. Darby, T. J. Daniell, H.C.J. Godfray, and A. E. Douglas. 2004. Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol. Entomol. 29: 60-65.
22. Ferrari, J., J. A. West, S. Via, and H.C.J. Godfray. 2012. Population genetic structure and secondary symbionts in host associated populations of the pea aphid complex. Evolution 66: 375-390.
23. Fukatsu, T. 2001. Secondary intracellular symbiotic bacteria in aphids of the genus Yamatocallis (Homoptera: Aphididae: Drepanosiphinae). Appl. Environ. Microbiol. 67: 5315-5320.
24. Fukatsu, T., N. Nikoh, R. Kawai, and R. Koga. 2000. The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol. 66: 2748-2758.
25. Fukatsu, T., T. Tsuchida, N. Nikoh, and R. Koga. 2001. Spiroplasma symbiont of the pea aphid, Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol. 67: 1284-1291.
26. Gehrer, L., and C. Vorburger. 2012. Parasitoids as vectors of bacterial endosymbionts in aphids. Biol. Lett. (doi: 10.1098/rsbl.2012.0144).
27. Gerardo, N. M., B. Altincicek, C. Anselme, H. Atamian, S. M. Barribeau, M. de Vos, E. J. Duncan, J. D. Evans, T. Gabaldo ́n, M. Ghamin, et al. 2010. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 11: R21.
28. Gotelli, N. J., and R. K. Colwell. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4: 379-391.
29. Gotelli, N. J., and G. L. Entsminger. 2007. EcoSim: null models software for ecology, version 7. Acquired Intelligence Inc. & Kesey-Bear, Jericho, VT. (http://garyentsminger.com/ecosim.htm).
30. Grenier, A-M., C. Nardon, and Y. Rahbé. 1994. Observations onthe micro-organisms occurring in the gut of thepeaaphid Acyrthosiphon pisum. Entomol. Exp. Appl. 70: 91-96.
31. Grenier, A-M., G. Duport, S. Pagès, G. Condemine, and Y. Rahbé. 2006. The phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) is a pathogen of the pea aphid. Appl. Environ. Microbiol. 72: 1956-1965.
32. Griffiths, B. S., S. Donn, R. Neilson, and T. J. Daniell. 2006. Molecular sequencing and morphological analysis of a nematode community. Appl. Soil Ecol. 32: 325-337.
33. Gündüz, E. A., and A. E. Douglas. 2009. Symbiotic bacteria enable insects to use a nutritionally inadequate diet. Proc. R. Soc. Lond. B. 276: 987-991.
34. Harada, H., and H. Ishikawa. 1993. Gut microbe of aphid closely related to its intracellular symbiont. BioSystems 31: 185-191.
35. Harada, H., and H. Ishikawa. 1997. Experimental pathogenicity of Erwinia aphidicola to pea aphid, Acyrthosiphon pisum. J. Gen. Appl. Microbiol. 43: 363-367.
36. Harada, H., H. Oyaizu, and H. Ishikawa. 1996. A consideration about the origin of aphid intracellular symbiont in connection with gut bacterial flora. J. Gen. Appl. Microbiol. 42: 17-26.
37. Harada, H., H. Oyaizu, Y. Kosako, and H. Ishikawa. 1997. Erwinia aphidicola, a new species isolated from pea aphid, Acyrthosiphon pisum. J. Gen. Appl. Microbiol. 43: 349-354.
38. Hauben, L., E.R.B. Moore, L. Vauterin, M. Steenackers, J. Mergaert, L. Verdonck, and J. Swings. 1998. Phylogenetic position of the phytopathogens within the Enterobacteriaceae. Syst. Appl. Microbiol. 21: 384-397.
39. Haynes, S., A. C. Darby, T. J. Daniell, G. Webster, F.J.F. van Veen, H.C.J. Godfray, J. I. Prosser, and A. E. Douglas. 2003. Diversity of bacteria associated with natural aphid populations. Appl. Environ. Microbiol. 69: 7216-7223.
40. Hinde, R. 1971. The fine structure of the mycetome symbiotes of the aphids Brevicoryne brassicae, Myzus persicae, and Macrosiphum rosae. J. Insect Physiol. 17: 2035-2045.
41. Huws, S. A., J. E. Edwards, E. J. Kim, and N. D. Scollan. 2007. Specificity and sensitivity of eubacterial primers utilized for molecular profiling of bacteria within complex microbial ecosystems. J. Microbiol. Methods 70: 565-569.
42. Jones, A.M.E., P. Winge, A. M. Bones, R. Cole, and J. T. Rossiter. 2002. Characterization and evolution of a myrosinase from the cabbage aphid Brevicoryne brassicae. Insect Biochem. Mol. Biol. 32: 275-284.
43. Jones, R. T., A. Bressan, A. M. Greenwell, and N. Fierer. 2011. Bacterial communities of two parthenogenetic aphid species cocolonizing two host plants across the Hawaiian Islands. Appl. Environ. Microbiol. 77: 8345-8349.
44. Kanzana, E., T. W. Pope, L. Tibbles, M. Bridges, J. A. Pickett, A. M. Bones, G. Powell, and J. T. Rossiter. 2007. The cabbage aphid: a walking mustard oil bomb. Proc. R. Soc. Lond. B. 274: 2271-2277.
45. Lane, D. J. 1991. 16S/23S rRNA sequencing, pp. 115-175. In E. Stackebrandt and M. Goodfellow. 1991. Nucleic acid techniques in bacterial systematics. John Wiley, Chichester, United Kingdom.
46. Lee, C., C. Grasso, and M. F. Sharlow. 2002. Multiple sequence alignment using partial order graphs. Bioinformatics 18: 452-464.
47. Milne, I., F. Wright, G. Rowe, D. F. Marshall, D. Husmeier, and G. McGuire. 2004. TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 20: 1806-1807.
48. Montllor, C. B., A. Maxman, and A. H. Purcell. 2002. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27: 189-195.
49. Moran, N. A., J. A. Russell, R. Koga, and T. Fukatsu. 2005. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl. Environ. Microbiol. 71: 3302-3310.
50. Munson, M. A., P. Baumann, M. A. Clark, L. Baumann, N. A. Moran, D. J. Voegtlin, and B. C. Campbell. 1991. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J. Bacteriol. 173: 6321-6324.
51. Nakabachi, A., H. Ishikawa, and T. Kudo. 2003. Extraordinary proliferation of microorganisms in aposymbiotic pea aphids, Acyrthosiphon pisum. J. Invertebr. Pathol. 82: 152-161.
52. Oliver, K. M., N. A. Moran, and M. S. Hunter. 2005. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl. Acad. Sci. U.S.A. 102: 12795-12800.
53. Oliver, K. M., J. A. Russell, N. A. Moran, and M. S. Hunter. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl. Acad. Sci. U.S.A. 100: 1803-1807.
54. Payne, R. W. 2009. GenStat WIREs Comp Stat. 1: 255-258.
55. Randerath, P. F. 1996. Ordination, pp. 251-287. In J. C. Fry (ed.), Biological Data Analysis: A Practical Approach. IRL Press, Oxford, United Kingdom.
56. Russell, J. A., A. Latorre, B. S. Muñ oz, A. Moya, and N. A. Moran. 2003. Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol. Ecol. 12: 1061-1075.
57. Sakurai, M., R. Koga, T. Tsuchida, X-Y. Meng, and T. Fukatsu. 2005. Rickettsia symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropism, effect on host fitness, and interaction with the essential symbiont Buchnera. Appl. Environ. Microbiol. 71: 4069-4075.
58. Sandström, J. P., J. A. Russell, J. P. White, and N. A. Moran. 2001. Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol. Ecol. 10: 217-228.
59. Scarborough, C. L., J. Ferrari, and H.C.J. Godfray. 2005. Aphid protected from pathogen by endosymbiont. Science 310: 1781.
60. Shigenobu, S., H. Watanabe, M. Hattori, Y. Sakaki, and H. Ishikawa. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407: 81-86.
61. Stackebrandt, E., and B. M. Goebel. 1994. A place for DNADNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44: 846-849.
62. Tsuchida, T., R. Koga, H. Shibao, T. Matsumoto, and T. Fukatsu. 2002. Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 11: 2123-2135.
63. von Burg, S., J. Ferrari, C. B.Müller, and C. Vorburger. 2008. Genetic variation and covariation of susceptibility to parasitoids in the aphid Myzus persicae: no evidence for trade-offs. Proc. R. Soc. Lond. B. 275: 1089-1094.
64. Vorburger, C., L. Gehrer, and P. Rodriguez. 2010. A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol. Lett. 6: 109-111.
65. Wilson, A.C.C., P. D. Ashton, F. Calevro, H. Charles, S. Colella, G. Febvay, G. Jander, P. F. Kushlan, S. J. Macdonald, J. F. Schwartz, 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: 249-258.