Partner associations across sympatric broad-headed bug species and their environmentally acquired bacterial symbionts

Molecular Ecology

Volumn 23, Issue 6, 2014, Pages 1333-1347

  Garcia, J R ^a   Laughton, A M ^a,b   Malik, Z ^a   Parker, B J ^a   Trincot, C ^a   S L Chiang, S ^a   Chung, E ^a   Gerardo, N M ^a  

^a EMORY UNIVERSITY   (United States)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

alydids; Burkholderia; insects; Lespedeza; mutualism

Indexed keywords

ALYDIDAE; ALYDUS CALCARATUS; BACTERIA (MICROORGANISMS); BURKHOLDERIA; BURKHOLDERIACEAE; ESCHERICHIA COLI; HEXAPODA; LESPEDEZA; MEGALOTOMUS QUINQUESPINOSUS;

BACTERIAL DNA; RNA 16S;

ALYDIDS; ANIMAL; ARTICLE; BACTERIUM IDENTIFICATION; BURKHOLDERIA; CLASSIFICATION; DIGESTIVE SYSTEM; ECOSYSTEM; GENETICS; HETEROPTERA; INSECT; ISOLATION AND PURIFICATION; LESPEDEZA; MICROBIOLOGY; MOLECULAR GENETICS; MULTILOCUS SEQUENCE TYPING; NUCLEOTIDE SEQUENCE; PHYLOGENY; SYMBIOSIS; SYMPATRY;

ALYDIDS; BURKHOLDERIA; INSECTS; LESPEDEZA; MUTUALISM;

ANIMALS; BACTERIAL TYPING TECHNIQUES; BURKHOLDERIA; DIGESTIVE SYSTEM; DNA, BACTERIAL; ECOSYSTEM; HETEROPTERA; MOLECULAR SEQUENCE DATA; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; RNA, RIBOSOMAL, 16S; SOIL MICROBIOLOGY; SYMBIOSIS; SYMPATRY;

EID: 84896399567     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12655     Document Type: Article

References (54)

1. Abràmoff MD, Magalhães PJ, (2004) Image processing with ImageJ. Biophotonics International, 11, 36-42.
2. Baldwin A, Mahenthiralingam E, Thickett KM, et al,. (2005) Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. Journal of Clinical Microbiology, 43, 4665-4673.
3. Baumann P, Baumann L, Lai C-Y, Rouhbakhsh D, (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annual Review of Microbiology, 49, 55-94.
4. Boucias DG, Garcia-Maruniak A, Cherry R, et al,. (2012) Detection and characterization of bacterial symbionts in the Heteropteran, Blissus insularis. FEMS Microbiology Ecology, 82, 629-641.
5. Chen WM, Moulin L, Bontemps C, et al,. (2003) Legume symbiotic nitrogen fixation by Beta-proteobacteria is widespread in nature. Journal of Bacteriology, 185, 7266-7272.
6. Compant S, Nowak J, Coenye T, Clement C, Barka EA, (2008) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiology Reviews, 32, 607-626.
7. Darriba D, Taboada GL, Doallo R, Posada D, (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772-772.
8. Davidson SK, Koropatnick TA, Kossmehl R, Sycuro L, McFall-Ngai MJ, (2004) NO means "yes" in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cellular Microbiology, 6, 1139-1151.
9. DeSantis TZ, Hugenholtz P, Keller K, et al,. (2006a) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Research, 34, W394-W399.
10. DeSantis TZ, Hugenholtz P, Larsen N, et al,. (2006b) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology, 72, 5069-5072.
11. Douglas AE, (2009) The microbial dimension in insect nutritional ecology. Functional Ecology, 23, 38-47.
12. Finney JC, Pettay DT, Sampayo EM, et al,. (2010) The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microbial Ecology, 60, 250-263.
13. Fukatsu T, Hosokawa T, (2002) Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Applied and Environmental Microbiology, 68, 389-396.
14. Gans J, Wolinsky M, (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science, 309, 1387-1390.
15. Goto S, Anbutsu H, Fukatsu T, (2006) Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Applied and Environmental Microbiology, 72, 4805-4810.
16. Haine ER, Pollitt LC, Moret Y, Siva-Jothy MT, Rolff J, (2008) Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor). Journal of Insect Physiology, 54, 1090-1097.
17. Huelsenbeck JP, Ronquist F, (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754-755.
18. Jaenike J, Stahlhut JK, Boelio LM, Unckless RL, (2009) Association between Wolbachia and Spiroplasma within Drosophila neotestacea: an emerging symbiotic mutualism? Molecular Ecology, 19, 414-425.
19. Kikuchi Y, Meng X-Y, Fukatsu T, (2005) Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Applied and Environmental Microbiology, 71, 4035-4043.
20. Kikuchi Y, Hosokawa T, Fukatsu T, (2007) Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Applied and Environmental Microbiology, 73, 4308-4316.
21. Kikuchi Y, Hosokawa T, Fukatsu T, (2011a) Specific developmental window for establishment of an insect-microbe gut symbiosis. Applied and Environmental Microbiology, 77, 4075-4081.
22. Kikuchi Y, Hosokawa T, Fukatsu T, (2011b) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. The ISME Journal, 5, 446-460.
23. Kikuchi Y, Hayatsu M, Hosokawa T, et al,. (2012) Symbiont-mediated insecticide resistance. Proceedings of the National Academy of Sciences, 109, 8618-8622.
24. Kim JK, Kim NH, Jang HA, et al,. (2013a) A specified midgut region controlling the symbiont titer in an insect-microbe gut symbiotic association. Applied and Environmental Microbiology 79, 7229-7233.
25. Kim JK, Lee HJ, Kikuchi Y, et al,. (2013b) The bacterial cell wall synthesis gene uppP is required for Burkholderia colonization of the stinkbug gut. Applied and Environmental Microbiology, 79, 4879-4886.
26. Lane DJ, (1991) 16S/23S rRNA sequencing. In: Nucleic Acid Techniques in Bacterial Systematics (eds, Stackebrandt E, Goodfellow M,), pp. 115-175. Wiley, New York.
27. Lee K-H, Ruby EG, (1992) Detection of the light organ symbiont, Vibrio fischeri, in Hawaiian seawater by using lux gene probes. Applied and Environmental Microbiology, 58, 942-947.
28. Lemaitre B, Hoffmann J, (2007) The host defense of Drosophila melanogaster. Annual Review of Immunology, 25, 697-743.
29. Loutet SA, Valvano MA, (2011) Extreme antimicrobial peptide and polymyxin B resistance in the genus Burkholderia. Frontiers in Microbiology, 2, 1-8.
30. McFall-Ngai M, Hadfield MG, Bosch TCG, et al,. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America, 110, 3229-3236.
31. Mitsuhashi J, (2002) Composition of salt solutions and culture media. In: Invertebrate Tissue Culture Methods (eds, Mitsuhashi J,), pp. 401-420. Springer Lab Manual, Tokyo.
32. Moret Y, Schmid-Hempel P, (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science, 290, 1166-1168.
33. Nyholm SV, Graf J, (2012) Knowing your friends: invertebrate innate immunity fosters beneficial bacterial symbioses. Nature Reviews Microbiology, 10, 815-827.
34. Oksanen J, Guillaume Blanchet F, Kindt R, et al,. (2013) Vegan: Community Ecology Package.
35. Oliver KM, Moran NA, Hunter MS, (2006) Costs and benefits of a superinfection of facultative symbionts in aphids. Proceedings of the Royal Society B: Biological Sciences, 273, 1273-1280.
36. Olivier-Espejel S, Sabree ZL, Noge K, Becerra JX, (2011) Gut microbiota in nymph and adults of the giant mesquite bug (Thasus neocalifornicus) (Heteroptera: Coreidae) is dominated by Burkholderia acquired de novo every generation. Environmental Entomology, 40, 1102-1110.
37. Palaniappan P, Chauhan PS, Saravanan VS, Anandham R, Sa T, (2010) Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp Biology and Fertility of Soils, 46, 807-816.
38. Pinheiro J, Bates D, DebRoy S, Sarvat D, Team RDC, (2013) NLME: Linear and Nonlinear Mixed Effects Model.
39. Porter SS, Rice KJ, (2012) Trade-offs, spatial heterogeneity, and the maintenance of microbial diversity. Evolution, 67, 599-608.
40. Prado SS, Almeida RPP, (2009) Role of symbiotic gut bacteria in the development of Acrosternum hilare and Murgantia histrionica. Entomologia Experimentalis et Applicata, 132, 21-29.
41. R Core Team (2009) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
42. Ruby EG, (2008) Symbiotic conversations are revealed under genetic interrogation. Nature Reviews Microbiology, 6, 752-762.
43. Sachs JL, Kembel SW, Lau AH, Simms EL, (2009) In situ phylogenetic structure and diversity of wild Bradyrhizobium communities. Applied and Environmental Microbiology, 75, 4727-4735.
44. Sachs JL, Russell JE, Lii YE, et al,. (2010) Host control over infection and proliferation of a cheater symbiont. Journal of Evolutionary Biology, 23, 1919-1927.
45. Sakurai M, Koga R, Tsuchida T, Meng XY, Fukatsu T, (2005) Rickettsia symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropism, effect on host fitness, and interaction with the essential symbiont Buchnera. Applied and Environmental Microbiology, 71, 4069-4075.
46. Schaefer CW, (1980) The host plants of the Alydinae, with a note on heterotypic feeding aggregations (Hemiptera: Coreoidea: Alydidae). Journal of the Kansas Entomological Society, 53, 115-122.
47. Schloss PD, Westcott SL, Ryabin T, et al,. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537-7541.
48. Spilker T, Baldwin A, Bumford A, et al,. (2009) Expanded multilocus sequence typing for Burkholderia species. Journal of Clinical Microbiology, 47, 2607-2610.
49. Suárez-Moreno ZR, Caballero-Mellado J, Coutinho BG, et al,. (2011) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microbial Ecology, 63, 249-266.
50. Swofford D, (2002) PAUP*. Phylogenetic Analysis Using Parsimony (and Other Methods). Sinauer Associates, Sunderland, MA.
51. Therneau T, (2013) A Package for Survival Analysis in S. Mayo Foundation, Rochester, MN.
52. Troll JV, Bent EH, Pacquette N, et al,. (2010) Taming the symbiont for coexistence: a host PGRP neutralizes a bacterial symbiont toxin. Environmental Microbiology, 12, 2190-2203.
53. Ventura MU, Silva JJ, Panizzi AR, (2000) Phyophagous Neomegalotomus parvus (Westwood) (Hemiptera: Alydidae) feeding on carrion and feces. Annals of the Society of Entomology Brasil, 29, 839-841.
54. Zwickl DJ, (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD Dissertation. University of Texas at Austin, Austin, Texas.