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

Freitak, Dalial; Schmidtberg, Henrike; Dickel, Franziska; Lochnit, Günther; Vogel, Heiko; Vilcinskas, Andreas

doi:10.4161/viru.28367

Cited by 154 publications

(155 citation statements)

References 30 publications

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“…Classically, this model host has been used to investigate antifungal efficacy and differences in virulence between strains and species. Finally, our data expands the use of G. mellonella for more "sophisticated" studies, as it has been already shown in the case of some pathogenic bacteria, which demonstrated that this model host can be used to investigate brain infections and maternal transfer of immunity 25,67 (see comment in 68 ).…”

Section: 62supporting

confidence: 61%

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Cryptococcus neoformansinduces antimicrobial responses and behaves as a facultative intracellular pathogen in the non mammalian modelGalleria mellonella

et al. 2014

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Section: 62supporting

confidence: 61%

“…Cryptococcusneoformans induces antimicrobial responses and behaves as a facultative intracellular pathogen in the non mammalian model Galleriamellonella, Virulence, 6:1,[66][67][68][69][70][71][72][73][74]…”

mentioning

confidence: 99%

Cryptococcus neoformansinduces antimicrobial responses and behaves as a facultative intracellular pathogen in the non mammalian modelGalleria mellonella

et al. 2014

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“…In this way, the egg and newly hatched larvae could receive an early supply of the important microbial complement, which indeed seems to be already present in the eggs of Lepidoptera (51). This reasonable speculation is indirectly supported by a recent study reporting the transit of ingested bacteria into the hemolymph and their accumulation in the ovary (52). Given the important role of the gut microbiota in the overall physiological balance (33,42,53), the occurrence of a transmission mechanism would not be surprising.…”

Section: Discussionmentioning

confidence: 91%

Midgut microbiota and host immunocompetence underlieBacillus thuringiensiskilling mechanism

Caccia¹,

Lelio

Storia

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

157

128

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Bacillus thuringiensis is a widely used bacterial entomopathogen producing insecticidal toxins, some of which are expressed in insect-resistant transgenic crops. Surprisingly, the killing mechanism of B. thuringiensis remains controversial. In particular, the importance of the septicemia induced by the host midgut microbiota is still debated as a result of the lack of experimental evidence obtained without drastic manipulation of the midgut and its content. Here this key issue is addressed by RNAi-mediated silencing of an immune gene in a lepidopteran host Spodoptera littoralis, leaving the midgut microbiota unaltered. The resulting cellular immunosuppression was characterized by a reduced nodulation response, which was associated with a significant enhancement of host larvae mortality triggered by B. thuringiensis and a Cry toxin. This was determined by an uncontrolled proliferation of midgut bacteria, after entering the body cavity through toxin-induced epithelial lesions. Consequently, the hemolymphatic microbiota dramatically changed upon treatment with Cry1Ca toxin, showing a remarkable predominance of Serratia and Clostridium species, which switched from asymptomatic gut symbionts to hemocoelic pathogens. These experimental results demonstrate the important contribution of host enteric flora in B. thuringiensis-killing activity and provide a sound foundation for developing new insect control strategies aimed at enhancing the impact of biocontrol agents by reducing the immunocompetence of the host.

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“…Transgenerational immunity has been thus far reported in a dozen invertebrate species [13,14,16 -24]. Although the mechanisms underlying this transgenerational immune protection remain unclear, this work suggests that this form of parental care may be induced by the transfer of pathogen-derived antimicrobial peptides or mRNA-encoding immune effectors [20,25,26].…”

Section: Introductionmentioning

confidence: 88%

Evolution of transgenerational immunity in invertebrates

et al. 2016

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Over a decade ago, the discovery of transgenerational immunity in invertebrates shifted existing paradigms on the lack of sophistication of their immune system. Nonetheless, the prevalence of this trait and the ecological factors driving its evolution in invertebrates remain poorly understood. Here, we develop a theoretical host -parasite model and predict that long lifespan and low dispersal should promote the evolution of transgenerational immunity. We also predict that in species that produce both philopatric and dispersing individuals, it may pay to have a plastic allocation strategy with a higher transgenerational immunity investment in philopatric offspring because they are more likely to encounter locally adapted pathogens. We review all experimental studies published to date, comprising 21 invertebrate species in nine different orders, and we show that, as expected, longevity and dispersal correlate with the transfer of immunity to offspring. The validity of our prediction regarding the plasticity of investment in transgenerational immunity remains to be tested in invertebrates, but also in vertebrate species. We discuss the implications of our work for the study of the evolution of immunity, and we suggest further avenues of research to expand our knowledge of the impact of transgenerational immune protection in host -parasite interactions.

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

Cited by 154 publications

References 30 publications

Cryptococcus neoformansinduces antimicrobial responses and behaves as a facultative intracellular pathogen in the non mammalian modelGalleria mellonella

Cryptococcus neoformansinduces antimicrobial responses and behaves as a facultative intracellular pathogen in the non mammalian modelGalleria mellonella

Midgut microbiota and host immunocompetence underlieBacillus thuringiensiskilling mechanism

Evolution of transgenerational immunity in invertebrates

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