Symbiosis in the green leafhopper, Cicadella viridis (Hemiptera, Cicadellidae): Association in statu nascendi?

Arthropod Structure and Development

Volumn 43, Issue 6, 2014, Pages 579-587

  Michalik, Anna ^a   Jankowska, Władysława ^a   Kot, Marta ^a   Gołas, Aniela ^a   Szklarzewicz, Teresa ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Endosymbiotic microorganisms; Sodalis like bacteria; Sulcia; Transovarial transmission of endosymbionts

Indexed keywords

DNA 16S; RNA 16S;

ARTICLE; BACTEROIDETES; CICADELLA VIRIDIS; CYTOPLASM; DNA SEQUENCE; ENDOSYMBIONT; FEMALE; LEAFHOPPER; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; PECTOBACTERIUM; PHYLOGENY; POLYMERASE CHAIN REACTION; SODALIS; SULCIA MUELLERI; SYMBIOSIS; ANIMAL; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; CLASSIFICATION; GENETICS; HEMIPTERA; MICROBIOLOGY; OVARY; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; FEMALE; HEMIPTERA; MICROSCOPY, ELECTRON, TRANSMISSION; OVARY; PHYLOGENY; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

EID: 84908503380     PISSN: 14678039     EISSN: 18735495     Source Type: Journal    
DOI: 10.1016/j.asd.2014.07.005     Document Type: Article

References (50)

1. Baumann P. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Ann. Rev. Microbiol. 2005, 59:155-189.
2. Bressan A., Arneodo J., Simonato M., Haines W.P., Boudon-Padieu E. Characterization and evolution of two bacteriome-inhabiting symbionts in cixiid planthoppers (Hemiptera: Fulgoromorpha: Pentastirini). Environ. Microbiol. 2009, 11:3265-3279.
3. Buchner P. Endosymbiosis of Animals with Plant Microorganisms 1965, Interscience Publishers, New York, London, Sydney.
4. Cheung W.K., Purcell A.H. Invasion of bacteroids and BEV bacterium into oocytes of the leafhopper Euscelidius variegatus Kirschbaum (Homoptera: Cicadellidae): an electron microscopic study. Zool. Stud. 1999, 38:69-75.
5. Chrudimský T., Husník F., Nováková E., Hypša V. Candidatus Sodalis melophagi sp. nov.: phylogenetically independent comparative model to the tsetse fly symbiont Sodalis glossinidius. PLoS One 2012, 7:e40354.
6. Dale C., Maudlin I. Sodalis gen. nov. and Sodalis glossinidius sp. nov., microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. I. J.Syst. Bacteriol. 1999, 49:267-275.
7. Dale C., Young S.A., Haydon D.T., Welburn S.C. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:1883-1888.
8. Dietrich C.H. Keys to the families of Cicadomorpha and subfamilies and tribes of Cicadellidae (Hemiptera: Auchenorrhyncha). Florida Entomol. 2005, 88:502-517.
9. von Dohlen C.D., Kohler S., Alsop S.T., McManus W.R. Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature 2001, 412:433-435.
10. Douglas A.E. Nutritional interactions in insect - microbial symbioses: aphids and their symbiotic bacteria Buchnera. Ann. Rev. Entomol. 1998, 43:17-37.
11. Eberle M.W., McLean D.L. Initiation and orientation of the symbiote migration in the human body louse Pediculus humanus L. J.Ins. Physiol. 1982, 28:417-422.
12. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
13. Fukatsu T., Koga R., Smith W.A., Tanaka K., Nikoh N., Sasaki-Fukatsu K., Yoshizawa K., Dale C., Clayton D.H. Bacterial endosymbiont of the slender pigeon louse, Columbicola columbae, allied to endosymbionts of grain weevils and tsetse flies. Appl. Environ. Microbiol. 2007, 73:6660-6668.
14. Gatehouse L.N., Sutherland P., Forgie S.A., Kaji R., Christeller J.T. Molecular and histological characterization of primary (Betaproteobacteria) and secondary (Gammaproteobacteria) endosymbionts of three mealybug species. Appl. Environ. Microbiol. 2011, 78:1187-1197.
15. Hall T.A. BIOEDIT: an user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
16. Ishii Y., Matsuura Y., Kakizawa S., Nikoh N., Fukatsu T. Diversity of bacterial endosymbionts associated with Macrosteles leafhoppers vectoring phytopathogenic phytoplasmas. Appl. Environ. Microbiol. 2013, 79:5013-5022.
17. Kaiwa N., Hosokawa T., Kikuchi Y., Nikoh N., Meng X.Y., Kimura N., Ito M., Fukatsu T. Primary gut symbiont and secondary, Sodalis-allied symbiont of the scutellerid stinkbug Cantao ocellatus. Appl. Environ. Microbiol. 2010, 76:3486-3494.
18. Koga R., Bennett G.M., Cryan J.R., Moran N.A. Evolutionary replacement of symbionts in an ancient and diverse insect lineage. Environ. Microbiol. 2013, 15:2073-2081.
19. Kono M., Koga R., Shimada M., Fukatsu T. Infection dynamics of coexisting β and γ-proteobacteria in the nested endosymbiotic system of mealybugs. Appl. Environ. Microbiol. 2008, 74:4175-4184.
20. Kuechler S.M., Dettner K., Kehl S. Molecular characterization and localization of the obligate endosymbiotic bacterium in the birch catkin bug Kleidocerys resedae (Heteroptera: Lygaeidae, Ischnorhynchinae). FEMS Microbiol. Ecol. 2010, 73:408-418.
21. Kuechler S.M., Dettner K., Kehl S. Characterization of an obligate intracellular bacterium in the midgut epithelium of the bulrush bug Chilacis typhae (Heteroptera, Lygaeidae, Artheneinae). Appl. Environ. Microbiol. 2011, 77:2869-2876.
22. Kuechler S.M., Renz P., Dettner K., Kehl S. Diversity of symbiotic organs and bacterial endosymbionts of lygaeoid bugs of the families Blissidae and Lygaeidae (Hemiptera: Heteroptera: Lygaeoidea). Appl. Environ. Microbiol. 2012, 78:2648-2659.
23. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
24. Matsuura Y., Kikuchi Y., Hosokawa T., Koga R., Meng X.-Y., Kamagata Y., Nikoh N., Fukatsu T. Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs. ISME 2012, 6:397-409.
25. McCutcheon J.P., Moran N.A. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:19392-19397.
26. McCutcheon J.P., McDonald B.R., Moran N.A. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:15394-15399.
27. McCutcheon J.P., von Dohlen C.D. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr. Biol. 2011, 21:1366-1372.
28. Michalik A., Jankowska W., Szklarzewicz T. Ultrastructure and transovarial transmission of endosymbiotic microorganisms in Conomelus anceps and Metcalfa pruinosa (Insecta, Hemiptera, Fulgoromorpha). Folia Biol. (Kraków) 2009, 57:131-137.
29. Michalik A., Gołas A., Kot M., Wieczorek K., Szklarzewicz T. Endosymbiotic microorganisms in Adelges (Sacchiphantes) viridis (Insecta, Hemiptera, Adelgoidea: Adelgidae): molecular characterization, ultrastructure and transovarial transmission. Arthropod Struct. Dev. 2013, 42:531-538.
30. Michalik A., Szklarzewicz T., Jankowska W., Wieczorek K. Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): ultrastructure, distribution and transovarial transmission. Eur. J. Entomol. 2014, 111:91-104.
31. Moran N.A., Dale C., Dunbar H., Smith W., Ochman H. Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environ. Microbiol. 2003, 5:116-126.
32. Moran N.A., Tran P., Gerardo N.M. Symbiosis and insect diversification: an ancient symbiont sap-feeding insects from the bacterial phylum bacteroidetes. Appl. Environ. Microbiol. 2005, 71:8802-8810.
33. Müller H.J. Neuere Vorstellungen über Verbreitung und Phylogenie der Endosymbiosen der Zikaden. Zeitschr. Morphol. Ökol. Tiere 1962, 51:190-210.
34. Noda H. Histological and histochemical observation of intracellular yeast-like symbiotes in the fat body of the small brown planthopper, Laodelphax striatellus (Homoptera: Delphacidae). Appl. Entomol. Zool. 1977, 12:134-141.
35. Noda H., Watanabe K., Kawai S., Yukuhiro F., Miyoshi T., Tomizawa M., Koizumi Y., Nikoh N., Fukatsu T. Bacteriome-associated endosymbionts of the green rice leafhopper Nephotettix cincticeps (Hemiptera: Cicadellidae). Appl. Entomol. Zool. 2012, 47:217-225.
36. Oliver K.M., Dergan P.H., Burke G.R., Moran N.A. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Ann. Rev. Entomol. 2010, 55:247-266.
37. Posada D., Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 1998, 1:817-818.
38. Sacchi L., Genchi M., Clementi E., Bigliardi E., Avanzatti A.M., Pajoroi M., Negri I., Marzorati M., Gonella E., Alma A., Daffonchio D., Bandi C. Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera: Cicadellidae): details of transovarial transmission of Cardinium sp. and yeast-like endosymbionts. Tiss. Cell 2008, 40:231-242.
39. Szklarzewicz T., Moskal A. Ultrastructure, distribution, and transmission of endosymbionts in the whitefly Aleurochiton aceris Modeer (Insecta, Hemiptera, Aleyrodinea). Protoplasma 2001, 218:45-53.
40. Szklarzewicz T., Kedra K., Niznik S. Ultrastructure and transovarial transmission of endosymbiotic microorganisms in Palaeococcus fuscipennis (Burmeister) (Insecta, Hemiptera, Coccinea: Monophlebidae). Folia Biol. (Kraków) 2006, 54:69-74.
41. Szklarzewicz T., Kalandyk-Kołodziejczyk M., Kot M., Michalik A. Ovary structure and transovarial transmission of endosymbiotic microorganisms in Marchalina hellenica (Insecta, Hemiptera, Coccomorpha: Marchalinidae). Acta Zool. (Stockholm) 2013, 94:184-192.
42. Swiatoniowska M., Ogorzalek A., Golas A., Michalik A., Szklarzewicz T. Ultrastructure, distribution and transovarial transmission of symbiotic microorganisms in Nysius ericae and Nithecus jacobaeae (Heteroptera: Lygaeidae: Orsillinae). Protoplasma 2013, 250:325-332.
43. Takiya D.M., Tran P., Dietrich C.H., Moran N.A. Co-cladogenesis spanning three phyla: leafhoppers (Insecta: Hemiptera: Cicadellidae) and their dual bacterial symbionts. Mol. Ecol. 2006, 15:4175-4191.
44. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA 6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013, 30:2725-2729.
45. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
46. Thao M.L., Gullan P.J., Baumann P. Secondary (γ-proteobacteria) endosymbionts infect the primary (β-proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their host. Appl. Environ. Microbiol. 2002, 68:3190-3197.
47. Toh H., Weiss B.L., Perkin S.A., Yamashita A., Oshima K., Hattori M., Aksoy S. Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res. 2006, 16:149-156.
48. Toju H., Fukatsu T. Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol. Ecol. 2011, 20:853-868.
49. Urban J., Cryan J. Two ancient bacterial endosymbionts have coevolved with the planthoppers (Insecta: Hemiptera: Fulgoroidea). BMC Evol. Biol. 2012, 12:87.
50. Wu D., Daugherty S.C., Van Aken S.E., Pai G.H., Watkins K.L., Khouri H. Metabolic complementarity and genomics of the dual symbiosis of sharpshooters. PLoS Biol. 2006, 4:e188.