Bacterial feeding induces changes in immune-related gene expression and has trans-generational impacts in the cabbage looper (Trichoplusia ni)

Abstract

Background: Poly-and oligophagous insects are able to feed on various host plants with a wide range of defense strategies. However, diverse food plants are also inhabited by microbiota differing in quality and quantity, posing a potential challenge for immune system mediated homeostasis in the herbivore. Recent studies highlight the complex interactions between environmentally encountered microorganisms and herbivorous insects, pointing to a potential adaptational alteration of the insects' physiology. We performed a differential gene expression analysis in whole larvae and eggs laid by parents grown on different diets to identify potential novel genes related to elevated microbial content in the caterpillars' food.

The maternal transfer of bacteria can mediate trans-generational immune priming in insects

“…9 Our data confirm the occurrence of such trans-generational immune priming in G. mellonella, which was detectable when E. coli and M. luteus were added to the diet but was more pronounced when the larvae were fed with S. entomophila. In agreement with Moret 23 and Freitak et al 9,10 we observed the strong induction of prophenoloxidases and the antimicrobial protein gloverin.…”

“…5,6 Later it was also shown to occur in beetles such as the mealworm beetle Tenebrio molitor 7 and the red flour beetle Tribolium castaneum. 8 Evidence for trans-generational immune priming among the Lepidoptera was first reported by Freitak et al, 9,10 who added bacteria to the diet of the cabbage looper larvae (Trichoplusia ni) resulting in the induction of immunityrelated genes associated with trans-generational effects. Maternal effects have been well documented in the context of trans-generational priming, and are thought to play a central role e.g., in the induction of offspring immunocompetence, but significant paternal effects have only been observed in a few studies.…”

“…18 We added bacteria to the G. mellonella larval diet to experimentally mimic the most common routes of natural exposure to microbes. 9,10 In the first part of our investigation, we addressed whether specific trans-generational immune priming occurs in G. mellonella by supplementing the larval diet with either non-pathogenic or entomopathogenic bacteria followed by the Parents invest in their offspring by preparing them for defense against pathogens and parasites that only the parents have encountered, a phenomenon known as trans-generational immune priming. We investigated the underlying mechanism using the established lepidopteran model host Galleria mellonella.…”

Endogenous egg immune defenses in the yellow mealworm beetle (Tenebrio molitor)

“…This transgenerational immune priming (TGIP) increases immune activity in eggs laid by immune challenged parents, even in the absence of egg infection (Little and Kraaijeveld, 2004). Priming prepares the eggs for the impending danger by triggering differential expression of immune-related genes in eggs and/or via the direct transmission of immune factors into eggs (Freitak et al, 2014(Freitak et al, , 2009Knorr et al, 2015;Trauer-Kizilelma and Hilker, 2015;Trauer and Hilker, 2013;Zanchi et al, 2011).…”

Transgenerational effects modulate density-dependent prophylactic resistance to viral infection in a lepidopteran pest

“…A number of recent studies have shown that invertebrates surviving disease exposure may produce offspring with enhanced disease resistance; a phenomenon known as 'transgenerational immune priming' [1][2][3][4]. This acquired protection against infection in invertebrates may follow an initial exposure to the same parasite, a different parasite or an immune response elicitor.…”