Why and how do protective symbionts impact immune priming with pathogens in invertebrates?

Prigot-Maurice, Cybèle; Beltran‐Bech, Sophie; Braquart‐Varnier, Christine

doi:10.1016/j.dci.2021.104245

Cited by 22 publications

(14 citation statements)

References 227 publications

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“…However, this would appear to contradict work showing that some Wolbachia strains upregulate the host's immune response and result in a reduction of pathogen growth [83][84][85].…”

Section: Discussionmentioning

confidence: 87%

“…Indeed, if priming is the result of upregulation of AMP expression, this may suggest that Wolbachia may actively be supressing the expression of AMPs, thereby reducing the beneficial effects of priming. However, this would appear to contradict work showing that some Wolbachia strains upregulate the host’s immune response and result in a reduction of pathogen growth [87–89]. Further rigorous experimental work is therefore required to fully dissect this effect of Wolbachia on immune priming.…”

Section: Discussionmentioning

confidence: 96%

“…A subsidiary finding of this work was the effect of the endosymbiont Wolbachia on immune priming. How endosymbionts that are widespread among insects are likely to influence innate immune priming is a topic of considerable interest (Prigot-Maurice et al, 2022). There is abundant evidence that Drosophila carrying the endosymbiont Wolbachia are better able to survive infections, especially viral infections (Hedges et al, 2008; Teixeira et al, 2008; Martinez et al, 2014; Vanika Gupta et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

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IMD-mediated innate immune priming increases Drosophila survival and reduces pathogen transmission

Prakash

Fenner

Shit

et al. 2023

Preprint

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Invertebrates lack the specialized immune-memory cells responsible for vertebrate-like acquired immunity. However, there is increasing evidence that past infection by the same pathogen can "prime" the insect immune response, resulting in improved survival upon reinfection. The mechanisms underlying these phenomenological accounts of priming are diverse, and often not completely clear. Here, we investigated the generality, specificity and mechanistic basis of immune priming in the fruit flyDrosophila melanogasterwhen infected with the gram-negative bacterial pathogenProvidencia rettgeri. We further explore the epidemiological consequences of immune priming and find it has the potential to curtail pathogen transmission by reducing pathogen shedding. We find that priming inDrosophilais a long-lasting, pathogen-specific response, occurring in several fly genetic backgrounds and is particularly stronger in male flies. Mechanistically, we find that the enhanced survival of individuals primed with an initial non-lethal bacterial inoculum coincides with a transient decrease in bacterial loads, and that this is likely driven by the IMD-responsive antimicrobial-peptide Diptericin-B in the fat body. Further, we show that while Diptericins are required as the effector of bacterial clearance, it is not solely sufficient for immune priming, and requires regulation by the peptidoglycan recognition proteins PGRP-LB, PGRP-LC and PGRP-LE. We discuss potential explanations for the observed sex differences in priming, and discuss the epidemiological consequences of innate immune priming in invertebrates.

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“…However, this would appear to contradict work showing that some Wolbachia strains upregulate the host's immune response and result in a reduction of pathogen growth [83][84][85].…”

Section: Discussionmentioning

confidence: 87%

Section: Discussionmentioning

confidence: 96%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

IMD-mediated innate immune priming increases Drosophila survival and reduces pathogen transmission

Prakash

Fenner

Shit

et al. 2023

Preprint

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“…We have not directly demonstrated a mode-of-action for this interaction, but the importance of the microbial community may result from the complementary and synergistic antiparasitic effects of different microbes (Prigot-Maurice et al . 2022 ). The data we collected on the gut microbiome of field-located S. exempta larvae, and data from previous studies (Graham et al .…”

Section: Discussionmentioning

confidence: 99%

Gut microbial community supplementation and reduction modulates African armyworm susceptibility to a baculovirus

Donkersley

Rice

Graham

et al. 2022

FEMS Microbiology Ecology

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Gut microbiota stimulates the immune system and inhibits pathogens, and thus, it is critical for disease prevention. Probiotics represent an effective alternative to antibiotics used for the therapy and prevention of bacterial diseases. Probiotic bacteria are commonly used in vertebrates, although their use in invertebrates is still rare. We manipulated the gut microbiome of the African Armyworm (Spodoptera exempta Walker) using antibiotics and field-collected frass, in an attempt to understand the interactions of the gut microbiome with the nucleopolyhedrovirus, SpexNPV. We found that S. exempta individuals with supplemented gut microbiome were significantly more resistant to SpexNPV, relative to those with a typical laboratory gut microbiome. Illumina MiSeq sequencing revealed the bacterial phyla in the S. exempta gut belonged to 28 different classes. Individuals with an increased abundance of Lactobacillales had a higher probability of surviving viral infection. In contrast, there was an increased abundance of Enterobacteriales and Pseudomonadales in individuals dying from viral infection, corresponding with decreased abundance of these two Orders in surviving caterpillars, suggesting a potential role for them in modulating the interaction between the host and its pathogen. These results have important implications for laboratory studies testing biopesticides.

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“…In mammals and arthropods, commensal microbiota was shown to shape immune capacities, not only at early stages, and to have a systemic effect on the immune response, inducing enhanced resistance towards a vast array of unrelated pathogens [96–103]. These findings are reminiscent of evidence of symbiont-mediated immune priming (reviewed in [104]) showing the impact of beneficial symbionts on immune capacities. In C. gigas , long-term immune priming capacities were evidenced using either non-pathogenic bacteria or viral mimic pre-conditioning [105,106].…”

Section: The Microbiota Shapes the Oyster Immune Systemmentioning

confidence: 99%

Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life

Destoumieux-Garzón,

Montagnani,

Dantan

et al. 2024

Phil. Trans. R. Soc. B

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The Pacific oyster Crassostrea gigas lives in microbe-rich marine coastal systems subjected to rapid environmental changes. It harbours a diversified and fluctuating microbiota that cohabits with immune cells expressing a diversified immune gene repertoire. In the early stages of oyster development, just after fertilization, the microbiota plays a key role in educating the immune system. Exposure to a rich microbial environment at the larval stage leads to an increase in immune competence throughout the life of the oyster, conferring a better protection against pathogenic infections at later juvenile/adult stages. This beneficial effect, which is intergenerational, is associated with epigenetic remodelling. At juvenile stages, the educated immune system participates in the control of the homeostasis. In particular, the microbiota is fine-tuned by oyster antimicrobial peptides acting through specific and synergistic effects. However, this balance is fragile, as illustrated by the Pacific Oyster Mortality Syndrome, a disease causing mass mortalities in oysters worldwide. In this disease, the weakening of oyster immune defences by OsHV-1 µVar virus induces a dysbiosis leading to fatal sepsis. This review illustrates the continuous interaction between the highly diversified oyster immune system and its dynamic microbiota throughout its life, and the importance of this cross-talk for oyster health. This article is part of the theme issue ‘Sculpting the microbiome: how host factors determine and respond to microbial colonization’.

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Why and how do protective symbionts impact immune priming with pathogens in invertebrates?

Cited by 22 publications

References 227 publications

IMD-mediated innate immune priming increases Drosophila survival and reduces pathogen transmission

IMD-mediated innate immune priming increases Drosophila survival and reduces pathogen transmission

Gut microbial community supplementation and reduction modulates African armyworm susceptibility to a baculovirus

Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life

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