Four intracellular genomes direct weevil biology: Nuclear, mitochondrial, principal endosymbiont, and Wolbachia - Archive ouverte HAL Accéder directement au contenu
Article Dans Une Revue Proceedings of the National Academy of Sciences of the United States of America Année : 1999

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

Résumé

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).

Dates et versions

hal-03504040 , version 1 (09-01-2022)

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Paternité - Pas d'utilisation commerciale - Pas de modification

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Abdelaziz Heddi, Anne-Marie Grenier, Chaqué Khatchadourian, Hubert Charles, Paul Nardon. Four intracellular genomes direct weevil biology: Nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96, pp.6814-6819. ⟨10.1073/pnas.96.12.6814⟩. ⟨hal-03504040⟩
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