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.
Highlights
Microbes that associate with hosts span a continuum from mutualism to parasitism and employ disparate transmission strategies [1]
These results were mirrored in analysis of a wider set of core genes, in which the Arsenophonus from honey bees again clustered as sister to A. nasoniae (Supplementary information Fig. 1)
This higher number of unique orthologous genes in A. nasoniae may reflect the difference between draft and polished genomes, in accessory genes carried on plasmids and prophage elements
Summary
Microbes that associate with hosts span a continuum from mutualism to parasitism and employ disparate transmission strategies [1]. Heritable bacterial symbionts, such as Wolbachia and Arsenophonus, transmit vertically (VT) from parent to offspring [2]. A combination of these routes operate, creating a complex transmission landscape [5, 6]. Across this transmission axis lies the impact of the symbiosis on each partner—whether the host and microbe benefit from the interaction, and whether one party requires the other to complete their life cycle. Obligacy may be a component of symbiont or host biology, or in some cases both parties are mutually dependent [2, 7, 8]
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