Biparental transmission of Verminephrobacter symbionts in the earthworm Aporrectodea tuberculata (Lumbricidae).
Most lumbricid earthworms harbor species-specific Verminephrobacter symbionts in their excretory organs (nephridia). These symbionts are vertically transmitted via the cocoon, where they colonize the embryos. Despite cospeciation for >100 million years with their hosts, Verminephrobacter lack genome reduction and AT bias typical of evolutionary old, vertically transmitted symbionts, caused by recurring bottlenecks. We hypothesized that biparental symbiont transmission into the cocoon enabled genetic mixing and relieved the bottleneck, and tested biparental transmission experimentally for V. aporrectodeae subsp. tuberculata, the specific symbiont of the earthworm Aporrectodea tuberculata, for which aposymbiotic worm lines are available. Virgin symbiotic and aposymbiotic adult worms were tagged, mated in pairs, separated before the start of cocoon production and their offspring assessed for Verminephrobacter. Specific PCR detected the symbionts in 41.5% of 188 juveniles produced by 20 aposymbiotic worms; fluorescence in situ hybridization showed a patchy but successful colonization of their nephridia. Symbionts were present in the mucus but absent in feed, soil, and spermatophora/nephridia of the aposymbiotic partner, suggesting symbiont transfer via mucus during mating. These results are consistent with the hypothesis that genome evolution in Verminephrobacter is distinct from other vertical-ly transmitted symbionts due to genetic mixing during transmission, partially facilitated by biparental transmission.
Section for Microbiology, Department of Bioscience, Aarhus University, Ny Munkegade 116, Building 1540, 8000 Aarhus-C, Denmark.
Laura-Carlota
LC
Paz
Section for Microbiology, Department of Bioscience, Aarhus University, Ny Munkegade 116, Building 1540, 8000 Aarhus-C, Denmark.
Andreas
A
Schramm
Section for Microbiology, Department of Bioscience, Aarhus University, Ny Munkegade 116, Building 1540, 8000 Aarhus-C, Denmark.|Aarhus Institute of Advanced Studies, Aarhus University, Høegh-Guldbergs Gade 6B, 8000 Aarhus-C, Denmark.
Marie Braad
MB
Lund
D000818:Animals; D042621:Comamonadaceae / Q000235:genetics* / Q000378:metabolism*; D019143:Evolution, Molecular; D041981:Gastrointestinal Tract / Q000382:microbiology; D016680:Genome, Bacterial / Q000235:genetics*; D017404:In Situ Hybridization, Fluorescence; D009835:Oligochaeta / Q000382:microbiology*; D016133:Polymerase Chain Reaction; D013045:Species Specificity; D013559:Symbiosis / Q000502:physiology*
Verminephrobacter–earthworm symbiosis; genome evolution; mucus; symbiont transmission; vertical parental transmission