Live imaging of symbiosis: Spatiotemporal infection dynamics of a GFP-labelled Burkholderia symbiont in the bean bug Riptortus pedestris

Molecular Ecology

Volumn 23, Issue 6, 2014, Pages 1445-1456

  Kikuchi, Yoshitomo ^a,b   Fukatsu, Takema ^c  

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

^b HOKKAIDO UNIVERSITY   (Japan)

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

Author keywords

green fluorescence protein; gut symbiotic bacteria; insect symbiosis; midgut crypt; population dynamics; stinkbug; symbiont colonization

Indexed keywords

BACTERIA (MICROORGANISMS); BURKHOLDERIA; HEXAPODA; RIPTORTUS;

GREEN FLUORESCENT PROTEIN;

ANIMAL; ARTICLE; BURKHOLDERIA; DIGESTIVE SYSTEM; FABACEAE; FEMALE; FLUORESCENCE MICROSCOPY; GENETICS; GROWTH, DEVELOPMENT AND AGING; GUT SYMBIOTIC BACTERIA; HETEROPTERA; INSECT SYMBIOSIS; METABOLISM; MICROBIOLOGY; MIDGUT CRYPT; NYMPH; PHYSIOLOGY; POPULATION DYNAMICS; REPRODUCTIVE FITNESS; STINKBUG; SYMBIONT COLONIZATION; SYMBIOSIS; TRANSGENIC ORGANISM;

GREEN FLUORESCENCE PROTEIN; GUT SYMBIOTIC BACTERIA; INSECT SYMBIOSIS; MIDGUT CRYPT; POPULATION DYNAMICS; STINKBUG; SYMBIONT COLONIZATION;

ANIMALS; BURKHOLDERIA; DIGESTIVE SYSTEM; FABACEAE; FEMALE; GENETIC FITNESS; GREEN FLUORESCENT PROTEINS; HETEROPTERA; MICROSCOPY, FLUORESCENCE; NYMPH; ORGANISMS, GENETICALLY MODIFIED; SYMBIOSIS;

EID: 84896386109     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12479     Document Type: Article

References (72)

1. Abe Y, Mishiro K, Takanashi M, (1995) Symbiont of brown-winged green bug, Plautia stali Scott. Japanese Journal of Applied Entomology and Zoology, 39, 109-115.
2. Akman L, Yamashita A, Watanabe H, et al,. (2002) Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nature Genetics, 32, 402-407.
3. Attardo GM, Lohs C, Heddi A, et al,. (2008) Analysis of milk gland structure and function in Glossina morsitans: milk protein production, symbiont populations and fecundity. Journal of Insect Physiology, 54, 1236-1242.
4. Bao Y, Lies DP, Fu H, Roberts GP, (1991) An improved Tn7-based system for the single-copy insertion of cloned genes into chromosomes of gram-negative bacteria. Gene, 109, 167-168.
5. Baumann P, (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annual Review of Microbiology, 59, 155-189.
6. 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.
7. Brewin NJ, (1991) Development of the legume root nodule. Annual Review of Cell Biology, 7, 191-226.
8. Bright M, Bulgheresi S, (2010) A complex journey: transmission of microbial symbionts. Nature Reviews Microbiology, 8, 218-230.
9. Buchner P, (1965) Endosymbiosis of Animals with Plant Microorganisms. Interscience, New York, New York.
10. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC, (1994) Green fluorescent protein as a marker for gene expression. Science, 263, 802-805.
11. Choi KH, DeShazer D, Schweizer HP, (2006) mini-Tn7 insertion in bacteria with multiple glmS-linked attTn7 sites: example Burkholderia mallei ATCC 23344. Nature Protocols, 1, 162-169.
12. Ciche TA, Kim KS, Kaufmann-Daszczuk B, Nguyen KC, Hall DH, (2008) Cell Invasion and matricide during Photorhabdus luminescens transmission by Heterorhabditis bacteriophora nematodes. Applied and Environmental Microbiology, 74, 2275-2287.
13. Clark MA, Moran NA, Baumann P, Wernegreen JJ, (2000) Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution; International Journal of Organic Evolution, 54, 517-525.
14. Douglas AE, (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology, 43, 17-37.
15. Dunn AK, Millikan DS, Adin DM, Bose JL, Stabb EV, (2006) New rfp- and pES213-derived tools for analyzing symbiotic Vibrio fischeri reveal patterns of infection and lux expression in situ. Applied and Environmental Microbiology, 72, 802-810.
16. 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.
17. Fukatsu T, Nikoh N, (2000) Endosymbiotic microbiota of the bamboo pseudococcid Antonina crawii (Insecta, Homoptera). Applied and Environmental Microbiology, 66, 643-650.
18. Futahashi R, Tanaka K, Matsuura Y, et al,. (2011) Laccase2 is required for cuticular pigmentation in stinkbugs. Insect Biochemistry and Molecular Biology, 41, 191-196.
19. Futahashi R, Tanaka K, Tanahashi M, et al,. (2013) Gene expression in gut symbiotic organ of stinkbug affected by extracellular bacterial symbiont. PLoS ONE, 8, e64557.
20. Gage DJ, (2002) Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. Journal of Bacteriology, 184, 7042-7046.
21. Goodchild AJP, (1963) Studies on the functional anatomy of the intestines of Heteroptera. Proceedings of the Zoological Society of London, 141, 851-910.
22. Hentschel U, Weis VM, McFall-Ngai MJ, (2012) Biological bulletin virtual symposium: discoveries in animal symbiosis in the "omics" age. The Biological Bulletin, 223, 5-6.
23. Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T, (2006) Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biology, 4, e337.
24. Hosokawa T, Kikuchi Y, Shimada M, Fukatsu T, (2008) Symbiont acquisition alters behaviour of stinkbug nymphs. Biology Letters, 4, 45-48.
25. Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T, (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proceedings of the National Academy of Sciences of the United States of America, 107, 769-774.
26. Hosokawa T, Hironaka M, Mukai H, et al,. (2012) Mothers never miss the moment: a fine-tuned mechanism for vertical symbiont transmission in a subsocial insect. Animal Behaviour, 83, 293-300.
27. Husnik F, Nikoh N, Koga R, et al,. (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell, 153, 1567-1578.
28. Inoue T, Kitade O, Yoshimura T, Yamaoka I, (2000) Symbiotic association with protists. In: Termites: Evolution, Sociality, Symbioses, Ecology (eds, Abe T, Bignell DE, Higashi M,), pp. 275-288. Kluwer Academic Publishers, Dordrecht.
29. International aphid genomics consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biology, 8, e1000313.
30. Kaiwa N, Hosokawa T, Kikuchi Y, et al,. (2010) Primary gut symbiont and secondary, Sodalis-allied symbiont of the scutellerid stinkbug Cantao ocellatus. Applied and Environmental Microbiology, 76, 3486-3494.
31. Kaltenpoth M, Winter SA, Kleinhammer A, (2009) Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs. FEMS Microbiology Ecology, 69, 373-383.
32. Kikuchi Y, (2009) Endosymbiotic bacteria in insects: their diversity and culturability. Microbes and Environments, 24, 195-204.
33. Kikuchi Y, Yumoto I, (2013) Efficient colonization of the bean bug Riptortus pedestris by an environmentally transmitted Burkholderia symbiont. Applied and Environmental Microbiology, 79, 2088-2091.
34. 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). Applied and Environmental Microbiology, 71, 4035-4043.
35. 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.
36. Kikuchi Y, Hosokawa T, Nikoh N, et al,. (2009) Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biology, 7, 2.
37. Kikuchi Y, Hosokawa T, Fukatsu T, (2011a) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. The ISME Journal, 5, 446-460.
38. Kikuchi Y, Hosokawa T, Fukatsu T, (2011b) Specific developmental window for establishment of an insect-microbe gut symbiosis. Applied and Environmental Microbiology, 77, 4075-4081.
39. Kikuchi Y, Hayatsu M, Hosokawa T, et al,. (2012) Symbiont-mediated insecticide resistance. Proceedings of the National Academy of Sciences of the United States of America, 109, 8618-8622.
40. Kim JK, Lee HJ, Kikuchi Y, et al,. (2013a) Bacterial cell wall synthesis gene uppP is required for Burkhoderia colonization of the stinkbug gut. Applied and Environmental Microbiology, 79, 4879-4886.
41. Kim JK, Won YJ, Nikoh N, et al,. (2013b) Polyester synthesis genes associated with stress resistance are involved in an insect-bacterium symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 110, E2381-E2389.
42. Koga R, Meng XY, Tsuchida T, Fukatsu T, (2012) Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. Proceedings of the National Academy of Sciences of the United States of America, 109, E1230-E1237.
43. Margulis L, Fester R, (1991) Symbiosis as a Source of Evolutionary Innovation. MIT Press, Cambridge, Massachusetts.
44. McCutcheon JP, Moran NA, (2012) Extreme genome reduction in symbiotic bacteria. Nature Reviews Microbiology, 10, 13-26.
45. McFall-Ngai M, Hadfield MG, Bosch TC, 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.
46. Miura T, Braendle C, Shingleton A, et al,. (2003) A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Journal of Experimental Zoology Part B, Molecular and Developmental Evolution, 295, 59-81.
47. Moran NA, (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proceedings of the National Academy of Sciences of the United States of America, 104, 8627-8633.
48. Moran NA, Munson MA, Baumann P, Ishikawa H, (1993) A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proceedings of the Royal Society B, 253, 167-171.
49. Moran NA, McCutcheon JP, Nakabachi A, (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics, 42, 165-190.
50. Nyholm SV, McFall-Ngai MJ, (2004) The winnowing: establishing the squid-Vibrio symbiosis. Annual Review of Microbiology, 2, 632-642.
51. Oliver KM, Russell JA, Moran NA, Hunter MS, (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences of the United States of America, 100, 1803-1807.
52. Prado SS, Golden M, Follett PA, Daugherty MP, Almeida RP, (2009) Demography of gut symbiotic and aposymbiotic Nezara viridula L. (Hemiptera: Pentatomidae). Environmental Entomology, 38, 103-109.
53. R development core team (2005) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
54. Rawls JF, Mahowald MA, Goodman AL, Trent CM, Gordon JI, (2007) In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut. Proceedings of the National Academy of Sciences of the United States of America, 104, 7622-7627.
55. Ruby EG, (2008) Symbiotic conversations are revealed under genetic interrogation. Nature Reviews Microbiology, 6, 752-762.
56. Ruby E, Henderson B, McFall-Ngai M, (2004) We get by with a little help from our (little) friends. Science, 303, 1305-1307.
57. Salem H, Kreutzer E, Sudakaran S, Kaltenpoth M, (2013) Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae). Environmental Microbiology, 15, 1956-1968.
58. Sasaki-Fukatsu K, Koga R, Nikoh N, et al,. (2006) Symbiotic bacteria associated with stomach discs of human lice. Applied and Environmental Microbiology, 72, 7349-7352.
59. Scarborough CL, Ferrari J, Godfray HC, (2005) Aphid protected from pathogen by endosymbiont. Science, 310, 1781.
60. Schneider G, (1940) Beiträge zur Kenntnis der symbiontischen Einrichtungen der Heteropteren. Zeitschrift für Morphologie und Ökologie der Tiere, 36, 565-644.
61. Schorr H, (1957) Zur Verhaltensbiologie und Symbiose von Brachypelta aterrima Först (Cydnidae, Heteroptera). Zeitschrift für Morphologie und Ökologie der Tiere, 45, 561-602.
62. Schuh RT, Slater JA, (1995) True Bugs of the World (Hemiptera: Heteroptera). Cornell University Press, New York, New York.
63. Schultze M, Kondorosi A, (1998) Regulation of symbiotic root nodule development. Annual Review of Genetics, 32, 33-57.
64. Shibata TF, Maeda T, Nikoh N, et al,. (2013) Complete genome sequence of Burkholderia sp strain RPE64, bacterial symbiont of the bean bug R. pedestris. Genome Announcements, 1, e00441-e00413.
65. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H, (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp APS. Nature, 407, 81-86.
66. Shimomura O, (2005) The discovery of aequorin and green fluorescent protein. Journal of Microscopy, 217, 1-15.
67. Tada A, Kikuchi Y, Hosokawa T, et al,. (2011) Obligate association with gut bacterial symbiont in Japanese populations of the southern green stinkbug Nezara viridula (Heteroptera: Pentatomidae). Applied and Entomology and Zoology, 46, 483-488.
68. Teal TK, Lies DP, Wold BJ, Newman DK, (2006) Spatiometabolic stratification of Shewanella oneidensis biofilms. Applied and Environmental Microbiology, 72, 7324-7330.
69. Tsuchida T, Koga R, Fukatsu T, (2004) Host plant specialization governed by facultative symbiont. Science, 303, 1989.
70. Tsuchida T, Koga R, Horikawa M, et al,. (2010) Symbiotic bacterium modifies aphid body color. Science, 330, 1102-1104.
71. Weirauch C, Schuh RT, (2011) Systematics and evolution of Heteroptera: 25 years of progress. Annual Review of Entomology, 56, 487-510.
72. Wernegreen JJ, (2002) Genome evolution in bacterial endosymbionts of insects. Nature Reviews Genetics, 3, 850-861. Technology