Translocation of bacteria from the gut to the eggs triggers maternal transgenerational immune priming in Tribolium castaneum

Abstract

Invertebrates can be primed to enhance their protection against pathogens they have encountered before. This enhanced immunity can be passed maternally or paternally to the offspring and is known as transgenerational immune priming. We challenged larvae of the red flour beetle Tribolium castaneum by feeding them on diets supplemented with Escherichia coli, Micrococcus luteus or Pseudomonas entomophila, thus mimicking natural exposure to pathogens. The oral uptake of bacteria induced immunity-related genes in the offspring, but did not affect the methylation status of the egg DNA. However, we observed the translocation of bacteria or bacterial fragments from the gut to the developing eggs via the female reproductive system. Such translocating microbial elicitors are postulated to trigger bacterial strain-specific immune responses in the offspring and provide an alternative mechanistic explanation for maternal transgenerational immune priming in coleopteran insects.

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).…”

The Microbiome of Spodoptera littoralis: Development, Control and Adaptation to the Insect Host

“…Interestingly, the fluorescent E. mundtii were also detected in the eggs of S. littoralis [14], supporting a direct symbiont transmission from one generation to another. Other studies have shown that fluorescent bacteria were transmitted from the gut to the eggs in Tribolium castaneum [120]. The symbiotic E. mundtii was transmitted to the second-generation progeny, suggesting that the bacteria co-evolve with the insect host ( Figure 4D).…”

Pathogen‐induced maternal effects result in enhanced immune responsiveness across generations

“…There are several putative mechanisms, not necessarily mutually exclusive, that can explain the apparent heightened immune competency of progeny from heat‐killed‐ and live‐ Serratia ‐injected mothers. First, the translocation of bacteria and/or bacterial components from Serratia ‐treated mothers to oocytes could elicit the embryo's own immunological responses in a strain‐specific manner (Freitak et al., ; Knorr et al., ). We found no evidence for this mechanism (Appendix ).…”

“…Both TGI and TGIP have been mostly studied at the phenomenological level in a variety of taxonomic groups and appear to be triggered by diverse pathogenic microbes and immune elicitors (Freitak, Heckel, & Vogel, ; Grindstaff et al., ; Hernández López, Schuehly, Crailsheim, & Riessberger‐Gallé, ; Little, O'Connor, Colegrave, Watt, & Read, ; Lozano & Ydenberg, ; Moret, ; Roth et al., ; Sadd & Schmid‐Hempel, ; Sadd et al., ; Tidbury, Pedersen, & Boots, ; Trauer‐Kizilelma & Hilker, , ; Zanchi, Troussard, Martinaud, Moreau, & Moret, ; Zanchi, Troussard, Moreau, & Moret, ). Although in most of these insect studies the specific molecular mechanisms underlying TGI/TGIP are poorly understood (Freitak et al., ; Salmela et al., ), recent research has addressed some of the mechanisms underlying heightened immune responsiveness across generations: from the incorporation of bacterial constituents into the developing eggs (Freitak et al., ; Knorr, Schmidtberg, Arslan, Bingsohn, & Vilcinskas, ; Salmela et al., ) to the differential regulation of immune‐responsive genes (Barribeau, Schmid‐Hempel, & Sadd, ).…”