Purine biosynthesis-deficient Burkholderia mutants are incapable of symbiotic accommodation in the stinkbug

ISME Journal

Volumn 8, Issue 3, 2014, Pages 552-563

  Kim, Jiyeun Kate ^a   Jang, Ho Am ^a   Won, Yeo Jin ^a   Kikuchi, Yoshitomo ^b   Heum Han, Sang ^a   Kim, Chan Hee ^a   Nikoh, Naruo ^c   Fukatsu, Takema ^d   Lee, Bok Luel ^a  

^a Pusan National University   (South Korea)

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

^c OPEN UNIVERSITY OF JAPAN   (Japan)

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

Author keywords

Burkholderia symbiont; infection density; insect gut symbiosis; purine biosynthesis; Riptortus pedestris

Indexed keywords

PURINE; PURINE DERIVATIVE;

ANIMAL; ARTICLE; BIOFILM; BIOSYNTHESIS; BURKHOLDERIA; GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HETEROPTERA; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; BIOFILMS; BURKHOLDERIA; GENES, INSECT; HETEROPTERA; MOLECULAR SEQUENCE DATA; MUTATION; PURINES; SYMBIOSIS;

EID: 84894291315     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.168     Document Type: Article

References (45)

1. An R, Grewal PS. (2010). Molecular mechanisms of persistence of mutualistic bacteria Photorhabdus in the entomopathogenic nematode host. PLoS One 5: e13154.
2. An R, Grewal PS. (2011). purL gene expression affects biofilm formation and symbiotic persistence of Photorhabdus temperata in the nematode Heterorhabditis bacteriophora. Microbiology 157: 2595-2603.
3. Anbutsu H, Goto S, Fukatsu T. (2008). High and low temperatures differently affect infection density and vertical transmission of male-killing Spiroplasma symbionts in Drosophila hosts. Appl Environ Microbiol 74: 6053-6059.
4. Baumann P, Moran NA. (1997). Non-cultivable microorganisms from symbiotic associations of insects and other hosts. Antonie Van Leeuwenhoek 72: 39-48. (Pubitemid 27393873)
5. Buchner P. (1965). Endosymbiosis of animals with plant microorganisms. Interscience Publishers: New York, NY, USA.
6. Buendia-Claveria AM, Moussaid A, Ollero FJ, Vinardell JM, Torres A, Moreno J et al. (2003). A purL mutant of Sinorhizobium fredii HH103 is symbiotically defective and altered in its lipopolysaccharide. Microbiology 149: 1807-1818. (Pubitemid 36874326)
7. Burmølle M, Thomsen TR, Fazli M, Dige I, Christensen L, Homøe P et al. (2010). Biofilms in chronic infections-a matter of opportunity-monospecies biofilms in multispecies infections. FEMS Immunol Med Microbiol 59: 324-336.
8. Costerton W, Veeh R, Shirtliff M, Pasmore M, Post C, Ehrlich G. (2003). The application of biofilm science to the study and control of chronic bacterial infections. J Clin Invest 112: 1466-1477. (Pubitemid 38056271)
9. Engelstadter J, Charlat S, Pomiankowski A, Hurst GD. (2006). The evolution of cytoplasmic incompatibility types: integrating segregation, inbreeding and outbreeding. Genetics 172: 2601-2611.
10. Gage DJ. (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68: 280-300. (Pubitemid 38756866)
11. Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC et al. (2007). Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316: 1307-1312. (Pubitemid 46871646)
12. Goodrich-Blair H, Clarke DJ. (2007). Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Mol Microbiol 64: 260-268. (Pubitemid 46632630)
13. Goto S, Anbutsu H, Fukatsu T. (2006). Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Appl Environ Microbiol 72: 4805-4810. (Pubitemid 44078807)
14. Ikeda T, Ishikawa H, Sasaki T. (2003). Infection density of Wolbachia and level of cytoplasmic incompatibility in the Mediterranean flour moth, Ephestia kuehniella. J Invertebr Pathol 84: 1-5. (Pubitemid 37190018)
15. Kikuchi Y, Fukatsu T. (2013). Live imaging of symbiosis: spatiotemporal infection dynamics of GFP-labeled Burkholderia symbiont in the bean bug Riptortus pedestris. Mol Ecol (in press).
16. Kikuchi Y, Meng XY, Fukatsu T. (2005). Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Appl Environ Microbiol 71: 4035-4043. (Pubitemid 40980576)
17. 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. Appl Environ Microbiol 73: 4308-4316. (Pubitemid 47068172)
18. Kikuchi Y, Hosokawa T, Fukatsu T. (2011a). An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5: 446-460.
19. Kikuchi Y, Hosokawa T, Fukatsu T. (2011b). Specific developmental window for establishment of an insect-microbe gut symbiosis. Appl Environ Microbiol 77: 4075-4081.
20. Kim JK, Lee HJ, Kikuchi Y, Kitagawa W, Nikoh N, Fukatsu T et al. (2013a). Bacterial cell wall synthesis gene uppP is required for Burkholderia colonization of the stinkbug gut. Appl Environ Microbiol 79: 4879-4886.
21. Kim JK, Won YJ, Nikoh N, Nakayama H, Han SH, Kikuchi Y et al. (2013b). Polyester synthesis genes associated with stress resistance are involved in an insect-bacterium symbiosis. Proc Natl Acad Sci USA 110: E2381-2389.
22. Koga R, Tsuchida T, 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 Biol Sci 270: 2543-2550. (Pubitemid 38082940)
23. Kondo N, Shimada M, Fukatsu T. (2005). Infection density of Wolbachia endosymbiont affected by co-infection and host genotype. Biol Lett 1: 488-491. (Pubitemid 41796602)
24. Laemmli UK. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
25. Mahan MJ, Slauch JM, Mekalanos JJ. (1993). Selection of bacterial virulence genes that are specifically induced in host tissues. Science 259: 686-688. (Pubitemid 23066292)
26. Maltz MA, Weiss BL, O'Neill M, Wu Y, Aksoy S. (2012). OmpA-mediated biofilm formation is essential for the commensal bacterium Sodalis glossinidius to colonize the tsetse fly gut. Appl Environ Microbiol 78: 7760-7768.
27. McGraw EA, Merritt DJ, Droller JN, O'Neill SL. (2002). Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci USA 99: 2918-2923. (Pubitemid 34240561)
28. Moran NA, McCutcheon JP, Nakabachi A. (2008). Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190.
29. Morris AR, Visick KL. (2010). Control of biofilm formation and colonization in Vibrio fischeri: a role for partner switching? Environ Microbiol 12: 2051-2059.
30. Mouton L, Henri H, Bouletreau M, Vavre F. (2003). Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol Ecol 12: 3459-3465. (Pubitemid 37496705)
31. Mouton L, Dedeine F, Henri H, Bouletreau M, Profizi N, Vavre F. (2004). Virulence, multiple infections and regulation of symbiotic population in the Wolbachia-Asobara tabida symbiosis. Genetics 168: 181-189. (Pubitemid 39346588)
32. Mouton L, Henri H, Charif D, Bouletreau M, Vavre F. (2007). Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol Lett 3: 210-213. (Pubitemid 351878159)
33. Nyholm SV, McFall-Ngai MJ. (2004). The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2: 632-642.
34. Oliver KM, Degnan PH, Burke GR, Moran NA. (2010). Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55: 247-266.
35. Pontes MH, Dale C. (2006). Culture and manipulation of insect facultative symbionts. Trends Microbiol 14: 406-412. (Pubitemid 44233295)
36. Ramey BE, Koutsoudis M, von Bodman SB, Fuqua C. (2004). Biofilm formation in plant-microbe associations. Curr Opin Microbiol 7: 602-609. (Pubitemid 39536286)
37. Rinaudi LV, Giordano W. (2010). An integrated view of biofilm formation in rhizobia. FEMS Microbiol Lett 304: 1-11.
38. Ruby EG. (2008). Symbiotic conversations are revealed under genetic interrogation. Nat Rev Microbiol 6: 752-762.
39. Sakurai M, Koga R, Tsuchida T, Meng XY, Fukatsu T. (2005). Rickettsia symbiont in the pea aphid Acyrtho-siphon pisum: novel cellular tropism, effect on host fitness, and interaction with the essential symbiont. Buchnera. Appl Environ Microbiol 71: 4069-4075. (Pubitemid 40980580)
40. Schägger H. (2006). Tricine-SDS-PAGE. Nat Protoc 1: 16-22.
41. Vautrin E, Vavre F. (2009). Interactions between vertically transmitted symbionts: cooperation or conflict? Trends Microbiol 17: 95-99.
42. Visick KL. (2009). An intricate network of regulators controls biofilm formation and colonization by Vibrio fischeri. Mol Microbiol 74: 782-789.
43. Werren JH, Baldo L, Clark ME. (2008). Wolbachia: master manipulators of invertebrate biology. Nat Rev Micro-biol 6: 741-751.
44. Xie B, Chen DS, Zhou K, Xie YQ, Li YG, Hu GY et al. (2006). Symbiotic abilities of Sinorhizobium fredii with modified expression of purL. Appl Microbiol Biotechnol 71: 505-514. (Pubitemid 44060954)
45. Xie B, Chen D, Cheng G, Ying Z, Xie F, Li Y et al. (2009). Effects of the purL gene expression level on the competitive nodulation ability of Sinorhizobium fredii. Curr Microbiol 59: 193-198.