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.
Highlights
Insects lack antibodies, the carriers of immunological memory in vertebrates
It has been shown that an insect mother facing pathogens can prime her offspring’s immune system. It has remained enigmatic how insects achieve specific trans-generational immune priming despite the absence of antibodybased immunity
We show this is made possible via an egg-yolk protein binding to immune elicitors that are carried to eggs
Summary
It has been thought that insects are deprived of acquired immunity and only have innate defense mechanisms against pathogens. Recent research has shown that insects are capable of high specificity in their defense reactions; insect immune defenses can recognize specific pathogens [1] and prime offspring against them [2,3]. Immunity is a major mechanism of survival that carries significant physiological and energetic costs, immune responses must be regulated to maximise fitness [4,5]. In order to maximize the fitness of their offspring in terms of immunity, growth rate and reproductive potential, selection should favour passing on a plastic signal (i.e. presence or absence of pathogens) about the pathogenicity of the environment. It has been observed that many organisms can transfer highly specific immune protection to the generation [6]
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