Reductive genome evolution, host-symbiont co-speciation and uterine transmission of endosymbiotic bacteria in bat flies

ISME Journal

Volumn 6, Issue 3, 2012, Pages 577-587

  Hosokawa, Takahiro ^a   Nikoh, Naruo ^b   Koga, Ryuichi ^a   Satô, Masahiko ^c   Tanahashi, Masahiko ^a   Meng, Xian Ying ^a   Fukatsu, Takema ^a  

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

^b OPEN UNIVERSITY OF JAPAN   (Japan)

^c Rishiri Town Museum   (Japan)

Author keywords

adenotrophic viviparity; co evolution; endosymbiont; nycteribiid bat fly; vertical transmission

Indexed keywords

BACTERIAL DNA; RNA 16S;

BACTERIUM; BAT; CLADISTICS; COEVOLUTION; DISEASE TRANSMISSION; ENDOSYMBIONT; FUNCTIONAL MORPHOLOGY; GENOME; HEMOPHAGY; HOST-SYMBIONT INTERACTION; INSECT; MOLECULAR ANALYSIS; PHYLOGENY; SPECIATION (BIOLOGY); VIVIPARITY;

ANIMAL; ARTICLE; BACTERIAL GENOME; BAT; CLASSIFICATION; DNA SEQUENCE; FEMALE; FEMALE GENITAL SYSTEM; FLY; GAMMAPROTEOBACTERIA; GENETICS; MALE; MICROBIOLOGY; MOLECULAR EVOLUTION; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; SPECIES DIFFERENTIATION; SYMBIOSIS;

ANIMALS; CHIROPTERA; DIPTERA; DNA, BACTERIAL; EVOLUTION, MOLECULAR; FEMALE; GAMMAPROTEOBACTERIA; GENETIC SPECIATION; GENITALIA, FEMALE; GENOME, BACTERIAL; MALE; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

JAPAN;

ARSENOPHONUS; BACTERIA (MICROORGANISMS); GAMMAPROTEOBACTERIA; HEXAPODA; NYCTERIBIIDAE; PENICILLIDIA; PHTHIRAPTERA; PRIMATES; STREBLIDAE;

EID: 84857118688     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2011.125     Document Type: Article

References (59)

1. Adams TS. (1999). Hematophagy and hormone release. Ann Entomol Soc Am 92: 1-13. (Pubitemid 29324249)
2. Allen JM, Reed DL, Perotti MA, Braig HR. (2007). Evolutionary relationships of 'Candidatus Riesia spp.,' endosymbiotic enterobacteriaceae living within hematophagous primate lice. Appl Environ Microbiol 75: 1659-1664. (Pubitemid 46417893)
3. Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T, Hattori M et al. (2002). Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet 32: 402-407. (Pubitemid 35266115)
4. Aksoy S. (1995). Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. Int J Syst Bacteriol 45: 848-851.
5. Aksoy S. (2000). Tsetse-a haven for microorganisms. Parasitol Today 16: 114-118.
6. Aksoy S, Rio RVM. (2005). Interactions among multiple genomes: Tsetse, its symbionts and trypanosomes. Insect Biochem Mol Biol 35: 691-698. (Pubitemid 40707632)
7. Aschner M. (1931). Die Bakterienflora der Pupiparen (Diptera). Eine Symbiosestudie an blutsaugenden Insekten. Z Morphol ö kol Tiere 20: 368-442.
8. Aschner M. (1946). The symbiosis of Eucampsipoda aegyptia Mcq. (Diptera, Pupipara: Nycteribiidae). Bull Soc Fouad I Entomol 30: 1-6.
9. 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.
10. Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V, Riley M et al. (1997). The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
11. Bourtzis K, Miller TA. (2003). Insect Symbiosis. CRC Press: Boca Raton, FL.
12. Breznak JA, Brune A. (1994). Role of microorganisms in the digestion of lignocellulose by termites. Annu Rev Entomol 39: 453-487.
13. Buchner P. (1965). Endosymbiosis of Animals with Plant Microorganisms. Interscience: New York.
14. Charleston MA, Page RDM. (2002) TreeMap v2.0. Application for Apple Macintosh (http://sydney.edu.au/ engineering/it/mcharles/software/treemap/ treemap.html).
15. Chen X, Li S, Aksoy S. (1999). Concordant evolution of a symbiont with its host insect species: Molecular phylogeny of genus Glossina and its bacteriomeassociated endosymbiont, Wigglesworthia glossinidia. J Mol Evol 48: 49-58. (Pubitemid 29044250)
16. Conord C, Despres L, Vallier A, Balmand S, Miquel C, Zundel S et al. (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.
17. Dale C, Maudlin I. (1999). Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int J Syst Bacteriol 49: 267-275. (Pubitemid 29225889)
18. Dale C, Beeton M, Harbison C, Jones T, Pontes M. (2006). Isolation, pure clture, and characterization of 'Candidatus Arsenophonus arthropodicus,' an intracellular secondary endosymbiont from the hippoboscid louse fly Pseudolynchia canariensis. Appl Environ Microbiol 72: 2997-3004.
19. Dick CW, Patterson BD. (2006). Bat flies: Obligate ectoparasites of bats. In: Morand S, Krasnov BR, Poulin R (eds), Micromammals and Macroparasites: From Evolutionary Ecology to Management. Springer: Tokyo, pp 179-194.
20. Douglas AE. (1998). Nutritional interactions in insectmicrobial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43: 17-37. (Pubitemid 28091227)
21. Fukatsu T. (1999). Acetone preservation: A practical technique for molecular analysis. Mol Ecol 8: 1935-1945. (Pubitemid 30030939)
22. Fukatsu T, Nikoh N, Kawai R, Koga R. (2000). The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: Homoptera). Appl Environ Microbiol 66: 2748-2758. (Pubitemid 30497577)
23. Grimardi D, Engel MS. (2005). Evolution of the Insects. Cambridge University Press: Cambridge.
24. Guindon S, Gascuel O. (2003). A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704. (Pubitemid 37365050)
25. Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML, Dodson RJ et al. (2000). DNA sequence of both chromosomes of the cholera pathogen Vibrio cholelae. Nature 406: 477-483. (Pubitemid 30625724)
26. 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.
27. Hosokawa T, Koga R, Kikuchi Y, Meng X-Y, Fukatsu T. (2010). Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci USA 107: 769-774.
28. Kadota K, Ishino T, Matsuyama T, Chinzei Y, Yuda M. (2004). Essential role of membrane-attack protein in malarial transmission to mosquito host. Proc Natl Acad Sci USA 101: 16310-16315. (Pubitemid 39552841)
29. 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.
30. Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM et al. (2010). Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci USA 107: 12168-12173.
31. Koga R, Tsuchida T, Fukatsu T. (2009). Quenching autofluorescence of insect tissues for in situ detection of endosymbionts. Appl Entomol Zool 44: 281-291.
32. Lehane M. (2005). The Biology of Blood-Sucking in Insects. Cambridge University Press: Cambridge.
33. McAlpine JF. (1989). Phylogeny and classification of the Muscomorpha. In: McAlpine JF (ed), Manual of Nearctic Diptera, vol. 3, Monograph 32. Agriculture Canada: Ottawa, pp 1397-1518.
34. Moran MA, Munson MA, Baumann P, Ishikawa H. (1993). A molecular clock in endosymbiotic bacteria is calibrated using the insect host. Proc R Soc Lond B 253: 167-171.
35. Moran NA, Tran P, Gerardo NM. (2005). Symbiosis and insect diversification: An ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol 1: 8802-8810. (Pubitemid 41804017)
36. Moran NA, McCutcheon JP, Nakabachi A. (2008). Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190.
37. Nirmala X, Hypša V, urovec M. (2001). Molecular phylogeny of Calyptratae (Diptera: Brachycera): The evolution of 18S and 16S ribosomal rDNAs in higher dipterans and their use in phylogenetic inference. Insect Mol Biol 10: 475-485. (Pubitemid 33011480)
38. Nogge G. (1981). Significance of symbionts for the maintenance of an optimal nutritional state for successful reproduction in haematophagous arthropods. Parasitology 82: 101-104.
39. Nováková E, Hypsa V, Moran NA. (2009). Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol 9: 143.
40. Ohkuma M. (2003). Termite symbiotic systems: Efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 61: 1-9. (Pubitemid 36458047)
41. Petersen FT, Meier R, Kutty SN, Wiegmann BM. (2007). The phylogeny and evolution of host choice in the Hippoboscoidea (Diptera) as reconstructed using four molecular markers. Mol Phylogenet Evol 45: 111-122. (Pubitemid 47380412)
42. Puchta O. (1955). Experimentelle Untersuchungen ü ber die Bedeutung der Symbiose der Kleiderlaus Pediculus vestimenti Burm. Z Parasitenk 17: 1-40.
43. Robinson-Rechavi M, Huchon D. (2000). RRTree: Relativerate tests between groups of sequences on a phylogenetic tree. Bioinformatics 16: 296-297. (Pubitemid 30352860)
44. Roubaud B. (1919). Les particularites de la nutrition et de la vie symbiotique chez les mouches tsetse. Ann Inst Pasteur 33: 489-537.
45. Sasaki-Fukatsu K, Koga R, Nikoh N, Yoshizawa K, Kasai S, Mihara M et al. (2006). Symbiotic bacteria associated with stomach discs of human lice. Appl Environ Microbiol 72: 7349-7352. (Pubitemid 44748453)
46. Sauer C, Stackebrandt E, Gadau J, Holldobler B, Gross R. (2000). Systematic relationships and cospeciation of bacterial endosymbionts and their carpenter ant host species: Proposal of the new taxon Candidatus Blochmannia gen. nov. Int J Syst Evol Microbiol 50: 1877-1886.
47. 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.
48. Swofford DL. (2001). PAUP* Version 4.0b10 [computer program]. In: 4.0b10 edition. Sinauer: Sunderland, MA.
49. Takiya DM, Tran PL, Dietrich CH, Moran NA. (2006). Co-cladogenesis spanning three phyla: Leafhoppers (Insecta: Hemiptera: Cicadellidae) and their dual bacterial symbionts. Mol Ecol 15: 4175-4191. (Pubitemid 44607160)
50. Thao ML, Baumann P. (2004). Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl Environ Microbiol 70: 3401-3406. (Pubitemid 38745884)
51. Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P. (2000). Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol 66: 2898-2905. (Pubitemid 30497597)
52. 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)
53. Toh H, Weiss BL, Perkin SAH, Yamashita A, Oshima K, Hattori M et al. (2006). Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res 16: 149-156. (Pubitemid 43200262)
54. Trowbridge RE, Dittmar K, Whiting MF. (2006). Identification and phylogenetic analysis of Arsenophonus-and Photorhabdus-type bacteria from adult Hippoboscidae and Streblidae (Hippoboscoidea). J Invertebr Pathol 91: 64-68. (Pubitemid 43003833)
55. Wernegreen JJ. (2002). Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet 3: 850-861. (Pubitemid 35303517)
56. Werren JH, Baldo L, Clark ME. (2008). Wolbachia: Master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741-751.
57. Wilkes TE, Darby AC, Choi JH, Colbourne JK, Werren JH, Hurst GDD. (2010). The draft genome sequence of Arsenophonus nasoniae, son-killer bacterium of Nasonia vitripennis, reveals genes associated with virulence and symbiosis. Insect Mol Biol 19(s1): 59-73.
58. Yuda M, Hirai M, Miura K, Matsumura H, Ando K, Chinzei Y. (1996). cDNA cloning, expression and characterization of nitric-oxide synthase from the salivary glands of the blood-sucking insect Rhodnius prolixus. Eur J Biochem 242: 807-812.
59. Zacharias A. (1928). Untersuchungen ü ber die intracellulare Symbiose bei den Pupiparen. Z Morphol ö kol Tiere 10: 676-737.