Transitions in symbiosis: evidence for environmental acquisition and social transmission within a clade of heritable symbionts

Abstract

A dynamic continuum exists from free-living environmental microbes to strict host-associated symbionts that are vertically inherited. However, knowledge of the forces that drive transitions in symbiotic lifestyle and transmission mode is lacking. Arsenophonus is a diverse clade of bacterial symbionts, comprising reproductive parasites to coevolving obligate mutualists, in which the predominant mode of transmission is vertical. We describe a symbiosis between a member of the genus Arsenophonus and the Western honey bee. The symbiont shares common genomic and predicted metabolic properties with the male-killing symbiont Arsenophonus nasoniae, however we present multiple lines of evidence that the bee Arsenophonus deviates from a heritable model of transmission. Field sampling uncovered spatial and seasonal dynamics in symbiont prevalence, and rapid infection loss events were observed in field colonies and laboratory individuals. Fluorescent in situ hybridisation showed Arsenophonus localised in the gut, and detection was rare in screens of early honey bee life stages. We directly show horizontal transmission of Arsenophonus between bees under varying social conditions. We conclude that honey bees acquire Arsenophonus through a combination of environmental exposure and social contacts. These findings uncover a key link in the Arsenophonus clades trajectory from free-living ancestral life to obligate mutualism, and provide a foundation for studying transitions in symbiotic lifestyle.

Arsenophonus apicola sp. nov., isolated from the honeybee Apis mellifera

“…Similar siderophores were identified previously as virulence factors in entomopathogenic bacteria [45]. As we previously shown for ArsBeeCH draft genome, the metabolic potential of the Arsenophonus from honey bees resembles that of Arsenophonus nasoniae [20]. The genome encodes complete biosynthetic pathways for several B vitamins including biotin, riboflavin, folate and pyridoxine.…”

“…Phylogenomic analysis using single-copy orthologues () placed strain ArsBeeUS T as a close affiliate of the uncultured Arsenophonus previously reported from European honey bees ( Apis mellifera ) [20]. The two strains share an ANI of 99.86% with 3 500 Single Nucleotide Polymorphisms across the entire genome confirming they are the same species.…”

“…Infection with Arsenophonus has also been linked to poor bee health [21, 22]; however, further work is required to corroborate this. Whilst Arsenophonus from bees has not previously been isolated to pure culture, a draft genome for a strain from Switzerland was recovered during analysis of pathogens in bee haemolymph [20].…”

Fidelity varies in the symbiosis between a gutless marine worm and its microbial consortium

“…[77][78][79][80] . Rapid advances in high-throughput sequencing combined with substantial reductions in sequencing costs using probabilistic SNP-calling now make such studies feasible, and will contribute to revealing the driving forces that shape the complex and fluid nature of multi-member symbioses 68,[81][82][83] .…”

Inheritance through the cytoplasm

“…The evolution of inheritance for symbionts of multicellular hosts also has its origins in the association of free-living organisms, with a transition from symbiosis where the parties reform symbiosis through environmental association each generation to vertical transmission. Indeed, some symbiont clades include both symbionts acquired through the environment and heritable symbionts (e.g., (Drew et al 2021 )). Vertical transmission may arise passively through spatial structure (symbionts from a parent are more likely to infect progeny of that parent through proximity), actively through selection on the host to ensure passage of a beneficial symbiont (host driven vertical transmission) or actively through selection on the microbe to infect the next generation through the germ line.…”