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

Drew, Georgia C, Budge, Giles E, Frost, Crystal L, Neumann, Peter, Siozios, Stefanos, Yanez, Orlando and Hurst, Gregory DD ORCID: 0000-0002-7163-7784
(2021) Transitions in symbiosis: evidence for environmental acquisition and social transmission within a clade of heritable symbionts. ISME JOURNAL, 15 (10). pp. 2956-2968.

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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.

Item Type: Article
Uncontrolled Keywords: Animals, Bees, Bacteria, Enterobacteriaceae, Gammaproteobacteria, Phylogeny, Symbiosis, Male
Divisions: Faculty of Health and Life Sciences
Faculty of Health and Life Sciences > Institute of Infection, Veterinary and Ecological Sciences
Depositing User: Symplectic Admin
Date Deposited: 10 May 2021 10:30
Last Modified: 08 Jan 2024 12:03
DOI: 10.1038/s41396-021-00977-z
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