Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin

Abstract

Insect immune systems can recognize specific pathogens and prime offspring immunity. High specificity of immune priming can be achieved when insect females transfer immune elicitors into developing oocytes. The molecular mechanism behind this transfer has been a mystery. Here, we establish that the egg-yolk protein vitellogenin is the carrier of immune elicitors. Using the honey bee, Apis mellifera, model system, we demonstrate with microscopy and western blotting that vitellogenin binds to bacteria, both Paenibacillus larvae – the gram-positive bacterium causing American foulbrood disease – and to Escherichia coli that represents gram-negative bacteria. Next, we verify that vitellogenin binds to pathogen-associated molecular patterns; lipopolysaccharide, peptidoglycan and zymosan, using surface plasmon resonance. We document that vitellogenin is required for transport of cell-wall pieces of E. coli into eggs by imaging tissue sections. These experiments identify vitellogenin, which is distributed widely in oviparous species, as the carrier of immune-priming signals. This work reveals a molecular explanation for trans-generational immunity in insects and a previously undescribed role for vitellogenin.

Author Summary

Insects lack antibodies, the carriers of immunological memory that vertebrate mothers can transfer to their offspring. Yet, it has been shown that an insect mother facing pathogens can prime her offspring’s immune system. To date, it has remained enigmatic how insects achieve specific trans-generational immune priming despite the absence of antibody-based immunity. Here, we show this is made possible via an egg-yolk protein binding to immune elicitors that are then carried to eggs. This yolk protein, called vitellogenin, is able to bind to different bacteria and pathogenic pattern molecules. We use E. coli fragments as a bait to show how vitellogenin is necessary for the carrying of immune elicitors to eggs. These findings help to understand how insects fight pathogens and can be useful for protection of ecologically and economically important insects, such as the honey bee, that we used as a model species.