The earthworm—Verminephrobacter symbiosis: an emerging experimental system to study extracellular symbiosis

Abstract

Almost all Lumbricid earthworms (Oligochaeta: Lumbricidae) harbor extracellular species-specific bacterial symbionts of the genus Verminephrobacter (Betaproteobacteria) in their nephridia. The symbionts have a beneficial effect on host reproduction and likely live on their host's waste products. They are vertically transmitted and presumably associated with earthworms already at the origin of Lumbricidae 62–136 million years ago. The Verminephrobacter genomes carry signs of bottleneck-induced genetic drift, such as accelerated evolutionary rates, low codon usage bias, and extensive genome shuffling, which are characteristic of vertically transmitted intracellular symbionts. However, the Verminephrobacter genomes lack AT bias, size reduction, and pseudogenization, which are also common genomic hallmarks of vertically transmitted, intracellular symbionts. We propose that the opportunity for genetic mixing during part of the host—symbiont life cycle is the key to evade drift-induced genome erosion. Furthermore, we suggest the earthworm-Verminephrobacter association as a new experimental system for investigating host-microbe interactions, and especially for understanding genome evolution of vertically transmitted symbionts in the presence of genetic mixing.

Insights into regeneration from the genome, transcriptome and metagenome analysis ofEisenia fetida

“…Vertical transmission of metagenome in E. fetida was known previously and stands reaffirmed in our study 15 . The inability to restore the obligate symbiont nephridial microbiome post-regeneration is an unexpected finding.…”

“…Earthworms also show intriguing behaviors like the ability to distinguish light of different wavelengths 6,11 and respond to tactile stimuli 12 , vibrations 13 and dragging objects along directions that offer least resistance 14 . They harbor a large and diverse microbiome in their gut and inherit certain bacteria as part of their nephridial metagenome 15 . They work in close proximity to microbial decomposers to reduce organic matter both depending on microbes and inducing changes in the microbiome favouring some species over others through the production of secondary metabolites and anti-microbial agents 1 .…”

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

“…This point is illustrated by the nephridial symbioses of earthworms. The ancient vertically transmitted symbiont, Verminephrobacter, is inherited biparentally, continues to incorporate foreign DNA, and does not undergo genome reduction (106,107). Conversely, entrance to the symbiosis rabbit hole does not require that symbionts be intracellular: Genome decay is observed in maternally transmitted extracellular symbionts, exemplified by Ishikawaella capsulata in plataspid stinkbugs (108).…”

Genome Evolution and Nitrogen Fixation in Bacterial Ectosymbionts of a Protist Inhabiting Wood-Feeding Cockroaches

“…These symbionts are deposited in egg capsules and transmitted to the nephridia of developing worms through a recruitment canal (76). Due to this vertical transmission, they have likely undergone population bottlenecks similarly to endosymbionts, as shown by their accelerated evolutionary rates, but genome reduction has not evolved (75,77). These symbionts also have dynamic genomes where an expansion of mobile elements appears to have mediated genome rearrangements.…”

“…Diverse and fluctuating environments may select against the loss of genes that are required for survival under these conditions and provide a milieu for genetic exchange and recombination with other microbes, which would counteract the deleterious effects of bottleneck-induced genetic drift (77).…”