An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts

ISME Journal

Volumn 5, Issue 3, 2011, Pages 446-460

  Kikuchi, Yoshitomo ^a   Hosokawa, Takahiro ^b   Fukatsu, Takema ^b  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

Burkholderia; environmental symbiont acquisition; gut symbiosis; horizontal and vertical transmission; stinkbugs

Indexed keywords

RNA 16S;

BACTERIUM; CLADISTICS; COEXISTENCE; DEVELOPMENTAL BIOLOGY; DISEASE TRANSMISSION; EGG; FREQUENCY ANALYSIS; FUNCTIONAL MORPHOLOGY; GENOTYPE; HOST-SYMBIONT INTERACTION; HYBRIDIZATION; INFECTIOUS DISEASE; INSECT; MOLECULAR ANALYSIS; PHYLOGENY; POLYMERASE CHAIN REACTION; POPULATION STRUCTURE; SPECIES DIVERSITY; SURVIVAL;

ANIMAL; ARTICLE; BURKHOLDERIA; CLASSIFICATION; GASTROINTESTINAL TRACT; GENETICS; HETEROPTERA; HISTOLOGY; ISOLATION AND PURIFICATION; MICROBIOLOGY; OOCYTE; PHYLOGENY; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; BURKHOLDERIA; GASTROINTESTINAL TRACT; HETEROPTERA; OVUM; PHYLOGENY; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

BURKHOLDERIA; COREOIDEA; HETEROPTERA; HEXAPODA; LYGAEOIDEA; PROTEOBACTERIA;

EID: 79951811830     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2010.150     Document Type: Article

References (65)

1. Abe Y, Mishiro K, Takanashi M. (1995). Symbiont of brown-winged green bug, Plautia stali Scott. Jpn J Appl Entomol Zool 39: 109-115.
2. Attardo GM, Lohs C, Heddi A, Alam UH, Yildirim S, Aksoy S. (2008). Analysis of milk gland structure and function in Glossina morsitans: milk protein production, symbiont populations and fecundity. J Insect Physiol 54: 1236-1242.
3. Baker AC. (2003). Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34: 661-689. (Pubitemid 38171434)
4. Benson DR, Silvester WB. (1993). Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57: 293-319. (Pubitemid 23170094)
5. Bontemps C, Elliott GN, Simon MF, Dos Reis Junior FB, Gross E, Lawton RC et al. (2010). Burkholderia species are ancient symbionts of legumes. Mol Ecol 19: 44-52.
6. Bourtzis K, Miller TA. (2003). Insect symbiosis. CRC press: Boca Raton, FL.
7. Bright M, Bulgheresi S. (2010). A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8: 218-230.
8. Buchner P. (1965). Endosymbiosis of animals with plant microorganisms. Interscience: New York, USA.
9. Bull JJ. (1994). Virulence. Evolution 48: 1423-1437.
10. Denarie J, Debelle F, Rosenberg C. (1992). Signaling and host range variation in nodulation. Annu Rev Microbiol 46: 497-531.
11. Douglas AE. (1998). Nutritional interactions in insectmicrobial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43: 17-37. (Pubitemid 28091227)
12. Dubilier N, Bergin C, Lott C. (2008). Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6: 725-740.
13. Estrada-De P, Bustillos-Cristales R, Caballero-Mellado J. (2001). Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67: 2790-2798. (Pubitemid 33639759)
14. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Marine Biol Biotechnol 3: 294-299.
15. Fukatsu T. (1999). Acetone preservation: a practical technique for molecular analysis. Mol Ecol 8: 1935-1945. (Pubitemid 30030939)
16. Fukatsu T, Nikoh N. (1998). Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl Environ Microbiol 64: 3599-3606. (Pubitemid 28462946)
17. Fukatsu T, Hosokawa T. (2002). Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Appl Environ Microbiol 68: 389-396. (Pubitemid 34031201)
18. Galtier N, Gouy M, Gautier C. (1996). SEAVIEW and PHYLO-WIN: two graphic tools for sequence alignment and molecular phylogeny. Bioinformatics 12: 543-548.
19. Garbeva P, van Veen JA, van Elsas JD. (2004). Microbial diversity in soil: selection microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42: 243-270. (Pubitemid 39308513)
20. Glasgow H. (1914). The gastric caeca and the caecal bacteria of the Heteroptera. Biol Bull 3: 101-171.
21. Hardin G. (1968). The tragedy of the commons. Science 162: 1243-1248.
22. Hasegawa M, Kishino H, Yano T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22: 160-174. (Pubitemid 16227864)
23. Hayatsu M, Hirano M, Tokuda S. (2000). Involvement of two plasmids in fenitrothion degradation by Burkholderia sp. strain NF100. Appl Environ Microbiol 66: 1737-1740. (Pubitemid 30185663)
24. Henry TJ. (1997). Phylogenetic analysis of family groups within the infraorder pentatomomorpha (Hemiptera: Heteroptera), with emphasis on the Lygaeoidea. Ann Entomol Soc Am 90: 275-301. (Pubitemid 127674650)
25. Hosokawa T, Kikuchi Y, Meng XY, Fukatsu T. (2005). The making of symbiont capsule in the plataspid stinkbug Megacopta punctatissima. FEMS Microbiol Ecol 54: 471-477. (Pubitemid 41416862)
26. Hosokawa T, Kikuchi Y, Nikoh N, Meng XY, Hironaka M, Fukatsu T. (2010). Phylogenetic position and peculiar genetic traits of the midgut bacterial symbiont in the stinkbug Parastrachia japonensis. Appl Environ Microbiol 76: 4130-4135.
27. Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T. (2006). Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol 4: e337.
28. Hua J, Li M, Dong P, Cui Y, Xie Q, Bu W. (2008). Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera). BMC Genomics 9: 610.
29. Huber-Schneider L. (1957). Morphologische und physiologische Untersuchungen an der Wanze Mesocerus marginatus L. und ihren Symbionten (Heteroptera). Z Morph Ö kol Tiere 46: 433-480.
30. Kaiwa N, Hosokawa T, Kikuchi Y, Nikoh N, Meng XY, Kimura N et al. (2010). Primary gut symbiont and secondary Sodalis-allied symbiont in the scutellerid stinkbug Cantao ocellatus. Appl Environ Microbiol 76: 3486-3494.
31. Kashima T, Nakamura T, Tojo S. (2006). Uric acid recycling in the shield bug, Parastrachia japonensis (Hemiptera: Parastrachiidae), during diapause. J Insect Physiol 52: 816-825. (Pubitemid 44107943)
32. Kiers ET, Denison RF. (2008). Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu Rev Ecol Evol Syst 39: 215-236.
33. Kiers ET, Rousseau RA, West SA, Denison RF. (2003). Host sanctions and the legume-rhizobium mutualism. Nature 425: 78-81. (Pubitemid 37101720)
34. Kikuchi Y. (2009). Endosymbiotic bacteria in insects: their diversity and culturability. Microbes Environ 24: 195-204.
35. Kikuchi Y, Meng XY, Fukatsu T. (2005). Gut symbiotic bacteria of the genus Burkholderia in the broadheaded bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Appl Environ Microbiol 71: 4035-4043. (Pubitemid 40980576)
36. Kikuchi Y, Hosokawa T, Fukatsu T. (2007). Insect-microbe mutualism without vertical transmission: a stinkbug acquires beneficial gut symbiont from environment every generation. Appl Environ Microbiol 73: 4308-4316. (Pubitemid 47068172)
37. Kikuchi Y, Hosokawa T, Fukatsu T. (2008). Diversity of bacterial symbiosis in stinkbugs. Microbial Ecology Research Trends Dijk, TV (ed). Nova Science Publishers, Inc: New York, USA, pp. 39-63.
38. Kikuchi Y, Hosokawa T, Nikoh N, Meng XY, Kamagata Y, Fukatsu T. (2009). Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol 7: 2.
39. Kimura M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111-120. (Pubitemid 11166431)
40. Koropatnick TA, Engle JT, Apicella MA, Stabb EV, Goldman WE, McFall-Ngai MJ. (2004). Microbial factor-mediated development in a host-bacterial mutualism. Science 306: 1186-1188. (Pubitemid 39488998)
41. Maynard Smith J, Szathmáry E. (1995). The Major Transitions in Evolution. Oxford: Freeman.
42. McFall-Ngai MJ, Ruby EG. (1991). Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 254: 1491-1494. (Pubitemid 21917485)
43. Miura T, Braendle C, Shingleton A, Sisk G, Kambhampati S, Stern DL. (2003). A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). J Exp Zool B 295: 59-81. (Pubitemid 37529157)
44. Miyamoto S. (1961). Comparative morphology of alimentary organs of Heteroptera, with the phylogenetic consideration. Sieboldia 2: 197-259.
45. Moawad M, Schmidt EL. (1987). Occurrence and nature of mixed infections in nodules of field-grown soybeans (Glycine max). Biol Fertil Soils 5: 112-114.
46. Müller HJ (1956) Experimentelle Studien an der Symbiose von Coptosoma scutellatum Geoffr (Hem. Heteropt.). Z Morph Ö kol Tiere, 44:459-482
47. Nyholm SV, McFall-Ngai MJ. (2004). The winnowing: establishing the squid-Vibrio symbiosis. Nat Rev Microbiol 2: 632-642.
48. Oldroyd GE, Downie JA. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59: 519-546. (Pubitemid 351813041)
49. Perret X, Staehelin C, Broughton WJ. (2000). Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64: 180-201. (Pubitemid 30143845)
50. Prado SS, Almeida RP. (2009a). Phylogenetic placement of pentatomid stink bug gut symbionts. Curr Microbiol 58: 64-69.
51. Prado SS, Almeida RP. (2009b). Role of symbiotic gut bacteria in the development of Acrosternum hilare and Murgantia histrionica. Entomol Exp Appl 132: 21-29.
52. Prado SS, Rubinoff D, Almeida RPP. (2006). Vertical transmission of a pentatomid caeca-associated symbiont. Ann Entomol Soc Am 99: 577-585. (Pubitemid 44725197)
53. Rowan R, Knowlton N, Baker A, Jara J. (1997). Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388: 265-269. (Pubitemid 27317968)
54. Schaefer CW. (1993). The Pentatomomorpha (Hemiptera: Heteroptera): an annotated outline of its systematic history. Eur J Entomol 90: 105-122.
55. Schaefer CW, Panizzi AR. (2000). Heteroptera of Economic Importance. CRC Press: Florida, USA.
56. Schorr H. (1957). Zur Verhaltensbiologie und Symbiose von Brachypelta aterrima Fö rst (Cydnidae, Heteroptera). Z Morph Ö kol Tiere 45: 561-602.
57. Schuh RT, Slater JA. (1995). True bugs of the world (Hemiptera: Heteroptera). Cornell University Press: New York, USA.
58. Takenaka S, Okugawa S, Kadowaki M, Murakami S, Aoki K. (2003). The metabolic pathway of 4-aminophenol in Burkholderia sp. strain AK-5 differs from that of aniline and aniline with C-4 substituents. Appl Environ Microbiol 69: 5410-5413. (Pubitemid 37150765)
59. Thompson JD, Higgins DG, Gibson TJ. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680. (Pubitemid 24354800)
60. Van Oevelen S, De Wachter R, Vandamme E, Robbrecht E, Prinsen E. (2002). Identification of the bacterial endosymbionts in leaf galls of Psychotria (Rubiaceae, angiosperms) and proposal of 'Candidatus Burkholderia kirkii' sp. nov. Int J Syst Evol Microbiol 52: 2023-2027. (Pubitemid 36004181)
61. Van Oevelen S, De Wachter R, Vandamme E, Vandamme P, Robbrecht E, Prinsen E. (2004). 'Candidatus Burkholderia calva and 'Candidatus Burkholderia nigropunctata' as leaf gall endosymbionts of African Psychotria. Int J Syst Evol Microbiol 54: 2237-2239. (Pubitemid 39585412)
62. West SA, Kiers ET, Pen I, Denison RF. (2002). Sanctions and mutualism stability: when should less beneficial mutualists be tolerated? J Evol Biol 15: 830-837. (Pubitemid 35016005)
63. Wilkinson DM, Sherratt TN. (2001). Horizontally acquired mutualisms, an unsolved problem in ecology? Oikos 92: 377-384. (Pubitemid 32219088)
64. Xie Q, Bu W, Zheng L. (2005). The Bayesian phylogenetic analysis of the 18S rRNA sequences from the main lineages of Trichophora (Insecta: Heteroptera: Pentatomomorpha). Mol Phylogenet Evol 34: 448-451. (Pubitemid 40033389)
65. Young JPW, Haukka KE. (1996). Diversity and phylogeny of rhizobia. New Phytol 133: 87-94. (Pubitemid 126558385)