Previous Article | Next Article 
Applied and Environmental Microbiology, July 2000, p. 2748-2758, Vol. 66, No. 7
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
The Secondary Endosymbiotic Bacterium of the Pea
Aphid Acyrthosiphon pisum (Insecta: Homoptera)
Takema
Fukatsu,1,*
Naruo
Nikoh,1,2
Rena
Kawai,1 and
Ryuichi
Koga1
National Institute of Bioscience and
Human-Technology, Agency of Industrial Science and Technology,
Tsukuba, 305-8566,1 and Bio-Oriented
Technology Research Advancement Institution, Omiya,
331-8537,2 Japan
Received 4 February 2000/Accepted 17 April 2000
The secondary intracellular symbiotic bacterium (S-symbiont) of the
pea aphid Acyrthosiphon pisum was investigated to determine its prevalence among strains, its phylogenetic position, its
localization in the host insect, its ultrastructure, and the cytology
of the endosymbiotic system. A total of 14 aphid strains were examined, and the S-symbiont was detected in 4 Japanese strains by diagnostic PCR. Two types of eubacterial 16S ribosomal DNA sequences were identified in disymbiotic strains; one of these types was obtained from
the primary symbiont Buchnera sp., and the other was
obtained from the S-symbiont. In situ hybridization and electron
microscopy revealed that the S-symbiont was localized not only in the
sheath cells but also in a novel type of cells, the secondary
mycetocytes (S-mycetocytes), which have not been found previously in
A. pisum. The size and shape of the S-symbiont cells were
different when we compared the symbionts in the sheath cells and the
symbionts in the S-mycetocytes, indicating that the S-symbiont is
pleomorphic under different endosymbiotic conditions. Light microscopy,
electron microscopy, and diagnostic PCR revealed unequivocally that the hemocoel is also a normal location for the S-symbiont. Occasional disordered localization of S-symbionts was also observed in adult aphids, suggesting that there has been imperfect host-symbiont coadaptation over the short history of coevolution of these organisms.
*
Corresponding author. Mailing address: National
Institute of Bioscience and Human-Technology, Agency of Industrial
Science and Technology, Tsukuba, 305-8566, Japan. Phone:
81-298-61-6087. Fax: 81-298-61-6080. E-mail:
fukatsu{at}nibh.go.jp.
Applied and Environmental Microbiology, July 2000, p. 2748-2758, Vol. 66, No. 7
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
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
[Abstract]
[Full Text]
-
Lamelas, A., Perez-Brocal, V., Gomez-Valero, L., Gosalbes, M. J., Moya, A., Latorre, A.
(2008). Evolution of the Secondary Symbiont "Candidatus Serratia symbiotica" in Aphid Species of the Subfamily Lachninae. Appl. Environ. Microbiol.
74: 4236-4240
[Abstract]
[Full Text]
-
Oliver, K. M, Campos, J., Moran, N. A, Hunter, M. S
(2008). Population dynamics of defensive symbionts in aphids. Proc R Soc B
275: 293-299
[Abstract]
[Full Text]
-
Wilkinson, T. L., Koga, R., Fukatsu, T.
(2007). Role of Host Nutrition in Symbiont Regulation: Impact of Dietary Nitrogen on Proliferation of Obligate and Facultative Bacterial Endosymbionts of the Pea Aphid Acyrthosiphon pisum. Appl. Environ. Microbiol.
73: 1362-1366
[Abstract]
[Full Text]
-
Kageyama, D., Anbutsu, H., Watada, M., Hosokawa, T., Shimada, M., Fukatsu, T.
(2006). Prevalence of a Non-Male-Killing Spiroplasma in Natural Populations of Drosophila hydei.. Appl. Environ. Microbiol.
72: 6667-6673
[Abstract]
[Full Text]
-
Oliver, K. M, Moran, N. A, Hunter, M. S
(2006). Costs and benefits of a superinfection of facultative symbionts in aphids. Proc R Soc B
273: 1273-1280
[Abstract]
[Full Text]
-
Gottlieb, Y., Ghanim, M., Chiel, E., Gerling, D., Portnoy, V., Steinberg, S., Tzuri, G., Horowitz, A. R., Belausov, E., Mozes-Daube, N., Kontsedalov, S., Gershon, M., Gal, S., Katzir, N., Zchori-Fein, E.
(2006). Identification and Localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae).. Appl. Environ. Microbiol.
72: 3646-3652
[Abstract]
[Full Text]
-
Russell, J. A., Moran, N. A.
(2005). Horizontal Transfer of Bacterial Symbionts: Heritability and Fitness Effects in a Novel Aphid Host. Appl. Environ. Microbiol.
71: 7987-7994
[Abstract]
[Full Text]
-
Oliver, K. M., Moran, N. A., Hunter, M. S.
(2005). Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl. Acad. Sci. USA
102: 12795-12800
[Abstract]
[Full Text]
-
Darby, A. C., Chandler, S. M., Welburn, S. C., Douglas, A. E.
(2005). Aphid-Symbiotic Bacteria Cultured in Insect Cell Lines. Appl. Environ. Microbiol.
71: 4833-4839
[Abstract]
[Full Text]
-
Sakurai, M., Koga, R., Tsuchida, T., Meng, X.-Y., Fukatsu, T.
(2005). Rickettsia Symbiont in the Pea Aphid Acyrthosiphon pisum: Novel Cellular Tropism, Effect on Host Fitness, and Interaction with the Essential Symbiont Buchnera. Appl. Environ. Microbiol.
71: 4069-4075
[Abstract]
[Full Text]
-
Moran, N. A., Russell, J. A., Koga, R., Fukatsu, T.
(2005). Evolutionary Relationships of Three New Species of Enterobacteriaceae Living as Symbionts of Aphids and Other Insects. Appl. Environ. Microbiol.
71: 3302-3310
[Abstract]
[Full Text]
-
Degnan, P. H., Lazarus, A. B., Brock, C. D., Wernegreen, J. J.
(2004). Host-Symbiont Stability and Fast Evolutionary Rates in an Ant-Bacterium Association: Cospeciation of Camponotus Species and Their Endosymbionts, Candidatus Blochmannia. Syst Biol
53: 95-110
[Abstract]
[Full Text]
-
Haynes, S., Darby, A. C., Daniell, T. J., Webster, G., van Veen, F. J. F., Godfray, H.C.J., Prosser, J. I., Douglas, A. E.
(2003). Diversity of Bacteria Associated with Natural Aphid Populations. Appl. Environ. Microbiol.
69: 7216-7223
[Abstract]
[Full Text]
-
Rio, R. V. M., Lefevre, C., Heddi, A., Aksoy, S.
(2003). Comparative Genomics of Insect-Symbiotic Bacteria: Influence of Host Environment on Microbial Genome Composition. Appl. Environ. Microbiol.
69: 6825-6832
[Abstract]
[Full Text]
-
Darby, A. C., Douglas, A. E.
(2003). Elucidation of the Transmission Patterns of an Insect-Borne Bacterium. Appl. Environ. Microbiol.
69: 4403-4407
[Abstract]
[Full Text]
-
Oliver, K. M., Russell, J. A., Moran, N. A., Hunter, M. S.
(2003). Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl. Acad. Sci. USA
100: 1803-1807
[Abstract]
[Full Text]
-
Kikuchi, Y., Fukatsu, T.
(2002). Endosymbiotic Bacteria in the Esophageal Organ of Glossiphoniid Leeches. Appl. Environ. Microbiol.
68: 4637-4641
[Abstract]
[Full Text]
-
Thao, M. L., Gullan, P. J., Baumann, P.
(2002). Secondary ({gamma}-Proteobacteria) Endosymbionts Infect the Primary ({beta}-Proteobacteria) Endosymbionts of Mealybugs Multiple Times and Coevolve with Their Hosts. Appl. Environ. Microbiol.
68: 3190-3197
[Abstract]
[Full Text]
-
Gil, R., Sabater-Munoz, B., Latorre, A., Silva, F. J., Moya, A.
(2002). Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life. Proc. Natl. Acad. Sci. USA
99: 4454-4458
[Abstract]
[Full Text]
-
Kikuchi, Y., Sameshima, S., Kitade, O., Kojima, J., Fukatsu, T.
(2002). Novel Clade of Rickettsia spp. from Leeches. Appl. Environ. Microbiol.
68: 999-1004
[Abstract]
[Full Text]
-
Fukatsu, T., Hosokawa, T.
(2002). Capsule-Transmitted Gut Symbiotic Bacterium of the Japanese Common Plataspid Stinkbug, Megacopta punctatissima. Appl. Environ. Microbiol.
68: 389-396
[Abstract]
[Full Text]
-
Fukatsu, T.
(2001). Secondary Intracellular Symbiotic Bacteria in Aphids of the Genus Yamatocallis (Homoptera: Aphididae: Drepanosiphinae). Appl. Environ. Microbiol.
67: 5315-5320
[Abstract]
[Full Text]
-
Akman, L., Rio, R. V. M., Beard, C. B., Aksoy, S.
(2001). Genome Size Determination and Coding Capacity of Sodalis glossinidius, an Enteric Symbiont of Tsetse Flies, as Revealed by Hybridization to Escherichia coli Gene Arrays. J. Bacteriol.
183: 4517-4525
[Abstract]
[Full Text]
-
Fukatsu, T., Tsuchida, T., Nikoh, N., Koga, R.
(2001). Spiroplasma Symbiont of the Pea Aphid, Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol.
67: 1284-1291
[Abstract]
[Full Text]
-
Dale, C., Young, S. A., Haydon, D. T., Welburn, S. C.
(2001). The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. USA
10.1073/pnas.021450998v1
[Abstract]
[Full Text]
-
Wilkinson, T. L., Adams, D., Minto, L. B., Douglas, A. E.
(2001). The impact of host plant on the abundance and function of symbiotic bacteria in an aphid. J. Exp. Biol.
204: 3027-3038
[Abstract]
[Full Text]
-
Dale, C., Young, S. A., Haydon, D. T., Welburn, S. C.
(2001). From the Cover: The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. USA
98: 1883-1888
[Abstract]
[Full Text]
-
Gil, R., Sabater-Munoz, B., Latorre, A., Silva, F. J., Moya, A.
(2002). Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life. Proc. Natl. Acad. Sci. USA
99: 4454-4458
[Abstract]
[Full Text]