Microbes, the ‘silent third partners’ of bee–angiosperm mutualisms

Authors: Steffan, Shawn; DHARAMPAL, PRARTHANA - University Of Wisconsin; KUENEMAN, JORDAN - Cornell University; KELLER, ALEXANDER - Ludwig-Maximilians University; ARGUETA-GUZMAN, MAGDA - University Of California, Riverside; MCFREDERICK, QUINN - University Of California; BUCHMANN, STEVEN - Northern Arizona University; VANNETTE, RACHEL - University Of California, Davis; EDLUND, ANNA - Bethany College; MEZERA, CELESTE - University Of Wisconsin; AMON, NOLAN - University Of Wisconsin; DANFORTH, BRYAN - Cornell University

Submitted to: Trends in Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/5/2023
Publication Date: 11/6/2023
Citation: Steffan, S.A., Dharampal, P.S., Kueneman, J.G., Keller, A., Argueta-Guzman, M.P., McFrederick, Q., Buchmann, S., Vannette, R., Edlund, A., Mezera, C.C., Amon, N., Danforth, B.N. 2023. Microbes, the ‘silent third partners’ of bee–angiosperm mutualisms. Trends in Ecology and Evolution. 39:65-77. https://doi.org/10.1016/j.tree.2023.09.001.
DOI: https://doi.org/10.1016/j.tree.2023.09.001

Interpretive Summary: Globally, most bee fauna develop by assimilating proteins and lipids directly from microbial and plant sources. In effect, microbial fingerprints are all over bees. Bee-plant-microbe symbioses are well-documented, but much past work has focused on gut-symbionts, and largely on the honey bee model. Most bee fauna are represented by solitary, non-social species, and most solitary bees are associated with symbiotic microbes. Symbiotic microbes can be divided into two discrete groups: endosymbionts (gut-microbes) and exosymbionts (external symbiotic organisms). There are abundant exosymbiotic microbes within fermenting pollen-provisions. Bee larvae eat, digest, and assimilate bacteria and fungi within the pollen-provision. Indeed, many larvae require exosymbiotic microbes to thrive. Here, we review the literature and summarize available data on the impacts of microbial symbioses with bees.

Technical Abstract: Within the brood-cell, young bees rely to varying degrees upon external symbiotic microbes for food, preservation of food, neutralization of plant toxins, defense against pathogens, and supplemental water and oxygen. These exosymbionts appear to represent a life-support system for immature bees, and collectively, these relationships can be characterized as the brood-cell microbiome hypothesis (BCMH). Here, we provide evidence to support the BCMH, focusing on the ecology, roles, and identities of the exosymbionts associated with bees. The significance of the BCMH is that in a true mutualism, all symbionts require the presence and activities of their fellow symbionts to thrive. Thus, to further the goals of bee conservation, bee symbionts will also need to be conserved. To these ends, an improved understanding of bee exosymbionts will be critical.