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

Abstract

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).

A mitochondrial-like aconitase in the bacterium Bacteroides fragilis : Implications for the evolution of the mitochondrial Krebs cycle

“…Like the endosymbiont theory, this theory suggests that the intimate association between a eukaryotic host and an endosymbiont permitted the translocation of several endosymbiont genes to the host genome. The serial endosymbiont theory suggests that these events have occurred successively throughout the history of the eukaryote (40). Some of these events are made obvious by the presence of genomous organelles, whereas other events are marked by genes left behind in the nuclear genome.…”

Diversification of endosymbiosis: replacements, co-speciation and promiscuity of bacteriocyte symbionts in weevils

“…For a long time, Sodalis glossinidius and allied insect symbionts have been known only from Glossina tsetse flies and Sitophilus weevils (Dale and Maudlin, 1999;Heddi et al, 1999). However, recent studies unveiled universal occurrences of Sodalis-allied symbionts in diverse insects such as bird lice , louse flies (Nováková and Hypša, 2007;Chrudimský et al, 2012), weevils (Toju and Fukatsu, 2011), longicorn beetles (Grü nwald et al, 2010) and stinkbugs (Kaiwa et al, 2010(Kaiwa et al, , 2011.…”

From bacteria to mitochondria: Aconitase yields surprises

“…1A). For example, modern-day rice weevils have an endosymbiotic relationship with Sitophilus oryzae principal endosymbiont (called SOPE), which supply the weevils with a variety of vitamins (23,24). At some point in the evolution of mitochondria a pivotal event sealed the fate of the endosymbiont to become an organelle.…”