Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts

Environmental Microbiology

Volumn 14, Issue 5, 2012, Pages 1284-1295

  Toenshoff, Elena R ^a   Gruber, Daniela ^a   Horn, Matthias ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ANIMAL; ARTICLE; BETAPROTEOBACTERIA; CLASSIFICATION; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GAMMAPROTEOBACTERIA; GENETICS; HEMIPTERA; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; SYMBIOSIS; ULTRASTRUCTURE;

ANIMALS; BETAPROTEOBACTERIA; FEMALE; GAMMAPROTEOBACTERIA; HEMIPTERA; IN SITU HYBRIDIZATION, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

ADELGES; ADELGIDAE; APHIDIDAE; BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; CONIFEROPHYTA; GAMMAPROTEOBACTERIA; HEMIPTERA; HEXAPODA; INSECTA;

EID: 84859971372     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02712.x     Document Type: Article

References (64)

1. Allen, D.C., and Dimond, J.B. (1968) A histological study of white pine shoots attacked by exules stage of Pineus pinifoliae. Ann Entomol Soc Am 61: 962-965.
2. Altschul, S., Gish, W., Miller, W., Myers, E., and Lipman, D. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Ashelford, K.E., Chuzhanova, N.A., Fry, J.C., Jones, A.J., and Weightman, A.J. (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71: 7724-7736.
4. Balch, R.E. (1952) Studies of the balsam woolly aphid Adelges piceae (Ratz.) and its effects on balsam fir, Abies balsamea (L.) Mill. Can Dep Agric Pub 867: 1-76.
5. Baumann, L., and Baumann, P. (2005) Cospeciation between the primary endosymbionts of mealybugs and their hosts. Curr Microbiol 50: 84-87.
6. Baumann, P. (2005) Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59: 155-189.
7. Baumann, P., Baumann, L., Lai, C.Y., Rouhbakhsh, D., Moran, N.A., and Clark, M.A. (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol 49: 55-94.
8. Blackman, R.L., and Eastop, V.F. (1994) Aphids of the World's Trees: An Identification and Information Guide. Wallingford, USA: CAB International.
9. Buchner, P. (1953) Endosymbiose Der Tiere Mit Pflanzlichen Mikroorganismen. Basel/Stuttgart: Birkhäuser.
10. Conord, C., Despres, L., Vallier, A., Balmand, S., Miquel, C., Zundel, S., etal. (2008) Long-term evolutionary stability of bacterial endosymbiosis in Curculionoidea: additional evidence of symbiont replacement in the Dryophthoridae family. Mol Biol Evol 25: 859-868.
11. Daims, H., Stoecker, K., and Wagner, M. (2005) Fluorescence in situ hybridization for the detection of prokaryotes. In Advanced Methods in Molecular Microbial Ecology. Osborn, A., and Smith, C. (eds). Abingdon, UK: Bios-Garland, pp. 213-239.
12. Degnan, P., Lazarus, A., Brock, C., and Wernegreen, J. (2004) Host-symbiont stability and fast evolutionary rates in an ant-bacterium association: cospeciation of Camponotus species and their endosymbionts, Candidatus Blochmannia. Syst Biol 53: 95-110.
13. Downie, D.A., and Gullan, P.J. (2005) Phylogenetic congruence of mealybugs and their primary endosymbionts. J Evol Biol 18: 315-324.
14. Felsenstein, J. (1989) PHYLIP - Phylogeny inference package (version 3.2). Cladistics 5: 164-166.
15. Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3: 294-299.
16. Foottit, R.G., Maw, H.E.L., Havill, N.P., Ahern, R.G., and Montgomery, M.E. (2009) DNA barcodes to identify species and explore diversity in the Adelgidae (Insecta: Hemiptera: Aphidoidea). Mol Ecol Resour 9: 188-195.
17. Fukatsu, T., and Ishikawa, H. (1996) Phylogenetic position of yeast-like symbiont of Hamiltonaphis styraci (Homoptera, Aphididae) based on 18S rDNA sequence. Insect Biochem Mol Biol 26: 383-388.
18. Gosalbes, M.J., Lamelas, A., Moya, A., and Latorre, A. (2008) The striking case of tryptophan provision in the cedar aphid Cinara cedri. J Bacteriol 190: 6026-6029.
19. Groot, T.V.M., Janssen, A., Pallini, A., and Breeuwer, J.A.J. (2005) Adaptation in the asexual false spider mite Brevipalpus phoenicis: evidence for frozen niche variation. Exp Appl Acarol 36: 165-176.
20. Gruwell, M.E., Morse, G.E., and Normark, B.B. (2007) Phylogenetic congruence of armored scale insects (Hemiptera: Diaspididae) and their primary endosymbionts from the phylum Bacteroidetes. Mol Phylogenet Evol 44: 267-280.
21. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
22. Guryev, V., Makarevitch, I., Blinov, A., and Martin, J. (2001) Phylogeny of the genus Chironomus (Diptera) inferred from DNA sequences of mitochondrial cytochrome b and cytochrome oxidase I. Mol Phylogenet Evol 19: 9-21.
23. Havill, N.P., and Foottit, R.G. (2007) Biology and evolution of Adelgidae. Annu Rev Entomol 52: 325-349.
24. Havill, N.P., Foottit, R.G., and von Dohlen, C.D. (2007) Evolution of host specialization in the Adelgidae (Insecta: Hemiptera) inferred from molecular phylogenetics. Mol Phylogenet Evol 44: 357-370.
25. Huelsenbeck, J.P., and Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
26. Katoh, K., Kuma, K., Toh, H., and Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511-518.
27. Koga, R., Tsuchida, T., and Fukatsu, T. (2003) Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc R Soc Lond B Biol Sci 270: 2543-2550.
28. Lackner, G., Mobius, N., Scherlach, K., Partida-Martinez, L.P., Winkler, R., Schmitt, I., and Hertweck, C. (2009) Global distribution and evolution of a toxinogenic Burkholderia-Rhizopus symbiosis. Appl Environ Microbiol 75: 2982-2986.
29. Lamelas, A., Gosalbes, M.J., Manzano-Marin, A., Pereto, J., Moya, A., and Latorre, A. (2011) Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet 7: e1002357.
30. Lefevre, C., Charles, H., Vallier, A., Delobel, B., Farrell, B., and Heddi, A. (2004) Endosymbiont phylogenesis in the Dryophthoridae weevils: evidence for bacterial replacement. Mol Biol Evol 21: 965-973.
31. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, etal. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
32. McCutcheon, J.P., and von Dohlen, C.D. (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol 21: 1366-1372.
33. McCutcheon, J.P., and Moran, N.A. (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA 104: 19392-19397.
34. McCutcheon, J.P., and Moran, N.A. (2010) Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol Evol 2: 708-718.
35. McCutcheon, J.P., McDonald, B.R., and Moran, N.A. (2009) Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci USA 106: 15394-15399.
36. Martinez-Torres, D., Buades, C., Latorre, A., and Moya, A. (2001) Molecular systematics of aphids and their primary endosymbionts. Mol Phylogenet Evol 20: 437-449.
37. Moran, N.A., McCutcheon, J.P., and Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190.
38. Moya, A., Pereto, J., Gil, R., and Latorre, A. (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9: 218-229.
39. Munson, M., Baumann, P., Clark, M., Baumann, L., Moran, N., Voegtlin, D., and Campbell, B. (1991a) Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol 173: 6321-6324.
40. Munson, M.A., Baumann, P., and Kinsey, M.G. (1991b) Buchnera gen. nov. and Buchnera aphidicola sp. nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. Int J Syst Bacteriol 41: 566-568.
41. Murray, R.G.E., and Stackebrandt, E. (1995) Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol 45: 186-187.
42. Oliver, K.M., Degnan, P.H., Burke, G.R., and Moran, N.A. (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55: 247-266.
43. Parry, W.H., and Spires, S. (1982) Studies on the factors affecting the population levels of Adelges cooleyi (Gillette) on Douglas fir. J Appl Entomol 94: 253-263.
44. Plumb, G.H. (1953) The formation and development of the Norway spruce gall caused by Adelges abietis L. Bull Conn Agric Exp Stn 566: 1-77.
45. Profft, J. (1936) Beiträge zur Symbiose der Aphiden und Psylliden. Zoomorphology 32: 289-326.
46. Rohfritsch, O., and Anthony, M. (1992) Strategies in Gall Induction by Two Groups of Homopterans. New York, USA; Oxford, England: Oxford University Press.
47. Ronquist, F., and Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
48. Schmidt, H.A., Strimmer, K., Vingron, M., and von Haeseler, A. (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
49. Shields, K.S., and Hirth, R.T. (2005) Bacterial endosymbionts of Adelges tsugae Annand: potential targets for biocontrol? Morgantown USDA, For. Serv.
50. Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y., and Ishikawa, H. (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407: 81-86.
51. Sopow, S.L., Shorthouse, J.D., Strong, W., and Quiring, D.T. (2003) Evidence for long-distance, chemical gall induction by an insect. Ecol Lett 6: 102-105.
52. Steffan, A.W. (1968) Evolution und Systematik der Adelgidae (Homoptera: Aphidina): Eine Verwandtschaftsanalyse auf vorwiegend ethologischer, zytologischer und karyologischer Grundlage. Zoologica 115: 1-139.
53. Stoecker, K., Dorninger, C., Daims, H., and Wagner, M. (2010) Double labeling of oligonucleotide probes for fluorescence in situ hybridization (DOPE-FISH) improves signal intensity and increases rRNA accessibility. Appl Environ Microbiol 76: 922-926.
54. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
55. Thao, M.L., and Baumann, P. (2004) Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl Environ Microbiol 70: 3401-3406.
56. Thao, M.L., Clark, M.A., Burckhardt, D.H., Moran, N.A., and Baumann, P. (2001) Phylogenetic analysis of vertically transmitted psyllid endosymbionts (Candidatus Carsonella ruddii) based on atpAGD and rpoC: comparisons with 16S-23S rDNA-derived phylogeny. Curr Microbiol 42: 419-421.
57. Thomas, G., Zucker, J., Macdonald, S., Sorokin, A., Goryanin, I., and Douglas, A. (2009) A fragile metabolic network adapted for cooperation in the symbiotic bacterium Buchnera aphidicola. BMC Syst Biol 3: 24.
58. Toenshoff, E.R., Penz, T., Narzt, T., Collingro, A., Schmitz-Esser, S., Pfeiffer, S., etal. (2011) Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae). ISME J 6: 384-396.
59. Tsuchida, T., Koga, R., and Fukatsu, T. (2004) Host plant specialization governed by facultative symbiont. Science 303: 1989.
60. Tsuchida, T., Koga, R., Horikawa, M., Tsunoda, T., Maoka, T., Matsumoto, S., etal. (2010) Symbiotic bacterium modifies aphid body color. Science 330: 1102-1104.
61. Williams, K., Gillespie, J., Sobral, B., Nordberg, E., Snyder, E., Shallom, J., and Dickerman, A. (2010) Phylogeny of Gammaproteobacteria. J Bacteriol 192: 2305-2314.
62. Wu, D., Daugherty, S.C., Aken, S.E., Pai, G.H., Watkins, K.L., Khouri, H., etal. (2006) Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol 4: e188.
63. Young, R.F., Shields, K.S., and Berlyn, G.P. (1995) Hemlock woolly adelgid (Homoptera, Adelgidae) - stylet bundle insertion and feeding sites. Ann Entomol Soc Am 88: 827-835.
64. Zurovcova, M., Havelka, J., Stary, P., Vechtova, P., Chundelova, D., Jarosova, A., and Kucerova, L. (2010) 'DNA barcoding' is of limited value for identifying adelgids (Hemiptera: Adelgidae) but supports traditional morphological taxonomy. Eur J Entomol 107: 147-156.