A Molecular Aspect of Symbiotic Interactions between the WeevilSitophilus oryzaeand Its Endosymbiotic Bacteria: Over-expression of a Chaperonin

Charles, Hubert; Heddi, Abdelaziz; Guillaud, J.; Nardon, C.; Nardon, P.

doi:10.1006/bbrc.1997.7552

Cited by 45 publications

(28 citation statements)

References 19 publications

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“…All these features indicate that SOPE is greatly integrated in the host physiology. Moreover, the SOPE genome apparently has undergone genetic changes throughout its intracellular life history (20), and its expression is partly controlled by the host (21). We interpret these observations to indicate a long period of microorganism-insect coadaptation.…”

mentioning

confidence: 87%

Four intracellular genomes direct weevil biology: Nuclear, mitochondrial, principal endosymbiont, andWolbachia

Heddi¹,

Grenier²,

Khatchadourian³

et al. 1999

Proc. Natl. Acad. Sci. U.S.A.

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Cell physiology in the weevil Sitophilus oryzae is coordinated by three integrated genomes: nuclear, mitochondrial, and the ''S. oryzae principal endosymbiont'' (SOPE). SOPE, a cytoplasmic bacterium (2 ؋ 10 3 bacteria per specialized bacteriocyte cell and 3 ؋ 10 6 bacteria per weevil) that belongs to the proteobacteria ␥3-subgroup, is present in all weevils studied. We discovered a fourth prokaryotic genome in somatic and germ tissues of 57% of weevil strains of three species, S. oryzae, Sitophilus zeamais, and Sitophilus granarius, distributed worldwide. We assigned this Gramnegative prokaryote to the Wolbachia group (␣-proteobacteria), on the basis of 16S rDNA sequence and f luorescence in situ DNA-RNA hybridization (FISH). Both bacteria, SOPE and Wolbachia, were selectively eliminated by combined heat and antibiotic treatments. Study of bacteria involvement in this insect's genetics and physiology revealed that SOPE, which induces the specific differentiation of the bacteriocytes, increases mitochondrial oxidative phosphorylation through the supply of pantothenic acid and ribof lavin. Elimination of this ␥3-proteobacterium impairs many physiological traits. By contrast, neither the presence nor the absence of Wolbachia significantly affects the weevil's physiology. Wolbachia, disseminated throughout the body cells, is in particularly high density in the germ cells, where it causes nucleocytoplasmic incompatibility. The coexistence of two distinct types of intracellular proteobacteria at different levels of symbiont integration in insects illustrates the genetic complexity of animal tissue. Furthermore, evolutionary timing can be inferred: first nucleocytoplasm, then mitochondria, then SOPE, and finally Wolbachia. Symbiogenesis, the genetic integration of long-term associated members of different species, in the weevil appears to be a mechanism of speciation (with Wolbachia) and provides a means for animals to acquire new genes that permit better adaptation to the environment (with SOPE).

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mentioning

confidence: 87%

Four intracellular genomes direct weevil biology: Nuclear, mitochondrial, principal endosymbiont, andWolbachia

Heddi¹,

Grenier²,

Khatchadourian³

et al. 1999

Proc. Natl. Acad. Sci. U.S.A.

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303

290

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“…Both eukaryotic groEL and groES are essential for mitochondrial biogenesis and in yeast for viability (Rospert et al, 1993). Gro-like proteins also have deserved attention in symbiotic/parasitic bacteria, in which they are supposed to be required for the endosymbiont survival within the host cystosol (Charles et al, 1997). In relation to proteolytic processing, a fungal subtilase was detected among the mycorrhiza-related proteins induced in M. truncatula roots upon colonisation with G. mosseae (spot 19, Table 1).…”

Section: Purine Biosynthesis (7)mentioning

confidence: 99%

Identification of in planta-expressed arbuscular mycorrhizal fungal proteins upon comparison of the root proteomes of Medicago truncatula colonised with two Glomus species

Recorbet

Valot

Robert

et al. 2010

Fungal Genetics and Biology

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“…Endosymbionts complement the insect's diet with metabolic components and contribute considerably to its adaptability and invasive power [1,2]. A symbiotic relationship such as this can be seen in the association of the cereal weevil (Sitophilus oryzae) with the Gram-negative γ-proteobacterium Sodalis pierantonius [3,4,5,6]. Weevil endosymbionts are transmitted maternally to the insect progeny.…”

Section: Introductionmentioning

confidence: 99%

“…The bacteriocytes house endosymbionts and isolate them from the host systemic immune response [7,8]. Endosymbionts are only tolerated inside these specific cells and their externalization from the bacteriocytes results in the activation of a systemic response and the secretion of antimicrobial peptides (AMP) [6]. This suggests that efficient mechanisms have been selected through host-symbiont coevolution that allow bacteriocytes to both protect and maintain the symbionts, and to control their localization, growth and density [9,10].…”

Section: Introductionmentioning

confidence: 99%

Systemic Infection Generates a Local-Like Immune Response of the Bacteriome Organ in Insect Symbiosis

Masson¹,

Vallier²,

Vigneron³

et al. 2015

J Innate Immun

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Endosymbiosis is common in insects thriving in nutritionally unbalanced habitats. The cereal weevil, Sitophilus oryzae, houses Sodalis pierantonius, a Gram-negative intracellular symbiotic bacterium (endosymbiont), within a dedicated organ called a bacteriome. Recent data have shown that the bacteriome expresses certain immune genes that result in local symbiont tolerance and control. Here, we address the question of whether and how the bacteriome responds to insect infections involving exogenous bacteria. We have established an infection model by challenging weevil larvae with the Gram-negative bacterium Dickeya dadantii. We showed that D. dadantii infects host tissues and triggers a systemic immune response. Gene transcript analysis indicated that the bacteriome is also immune responsive, but it expresses immune effector genes to a lesser extent than the systemic and intestinal responses. Most genes putatively involved in immune pathways remain weakly expressed in the bacteriome following D. dadantii infection. Moreover, quantitative PCR experiments showed that the endosymbiont load is not affected by insect infection or the resulting bacteriome immune activation. Thus, the contained immune effector gene expression in the bacteriome may prevent potentially harmful effects of the immune response on endosymbionts, whilst efficiently protecting them from bacterial intruders.

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A Molecular Aspect of Symbiotic Interactions between the WeevilSitophilus oryzaeand Its Endosymbiotic Bacteria: Over-expression of a Chaperonin

Cited by 45 publications

References 19 publications

Four intracellular genomes direct weevil biology: Nuclear, mitochondrial, principal endosymbiont, andWolbachia

Four intracellular genomes direct weevil biology: Nuclear, mitochondrial, principal endosymbiont, andWolbachia

Identification of in planta-expressed arbuscular mycorrhizal fungal proteins upon comparison of the root proteomes of Medicago truncatula colonised with two Glomus species

Systemic Infection Generates a Local-Like Immune Response of the Bacteriome Organ in Insect Symbiosis

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