Symbiont-mediated immune priming in animals through an evolutionary lens

Hoang, Kim Le Mai; King, Kayla C.

doi:10.1099/mic.0.001181

Cited by 13 publications

(11 citation statements)

References 123 publications

(160 reference statements)

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“…This study resonates with emerging concepts on the impact of environmental signals, either biotic or abiotic, on epigenetic changes responsible for heritable phenotypic outcomes [92][93][94] and on innate immune memory formation (also known as trained immunity) [89,90,95]. 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][97][98][99][100][101][102][103]. These findings are reminiscent of evidence of symbiont-mediated immune priming (reviewed in [104]) showing the impact of beneficial symbionts on immune capacities.…”

Section: The Microbiota Shapes the Oyster Immune Systemsupporting

confidence: 71%

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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Section: The Microbiota Shapes the Oyster Immune Systemsupporting

confidence: 71%

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 stark contrast in evolutionary outcomes with our model emphasises the importance of understanding the mechanism of host protection. Moreover, most studies of defensive symbionts focus on those that confer protection in terms of a reduced parasite load (e.g., due to interference competition) (Hoang and King 2022), and tolerance-conferring symbionts are understudied. Indeed, we are aware of only one study that explicitly shows defensive symbionts conferring tolerance to the host, with Bacteroides fragilis conferring tolerance by inducing the production of anti-inflammatory proteins against an experimental colitis caused by the bacterium Heliobacter hepaticus ((Mazmanian, Round, and Kasper 2008).…”

Section: Discussionmentioning

confidence: 99%

Tolerance-conferring defensive symbionts and the evolution of parasite virulence

Smith

Ashby

2022

Preprint

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Defensive symbionts in the host microbiome can confer protection from infection or reduce the harms of being infected by a parasite. Defensive symbionts are therefore promising agents of biocontrol that could be used to control or ameliorate the impact of infectious diseases. Previous theory has shown how symbionts can evolve along the parasitism-mutualism continuum to confer greater or lesser protection to their hosts, and in turn how hosts may coevolve with their symbionts to potentially form a mutualistic relationship. However, the consequences of introducing a defensive symbiont for parasite evolution and how the symbiont may coevolve with the parasite have yet to be explored theoretically. Here, we investigate the ecological and evolutionary implications of introducing a tolerance-conferring defensive symbiont into an established host-parasite system. We show that while the defensive symbiont may initially have a positive impact on the host population, parasite and symbiont evolution tend to have a net negative effect on the host population in the long-term. This is because the introduction of the defensive symbiont always selects for an increase in parasite virulence and may cause diversification into high- and low-virulence strains. Even if the symbiont experiences selection for greater host protection, this simply increases selection for virulence in the parasite, resulting in a net negative effect on the host population. Our results therefore suggest that tolerance-conferring defensive symbionts may be poor biocontrol agents for population-level infectious disease control.

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“…Owing to their immunomodulatory role, it is possible that host‐associated microbiota might also exhibit correlated changes as host immune functions diverge, although experimental support is lacking (Zheng et al, 2020). Although pathogen resistance is one of the major evolutionary advantages conferred by microbiota (Hoang & King, 2022; McLaren & Callahan, 2020), there are no experiments to test whether or to what extent the role of microbiota varies across divergent forms of host immunity. We thus conducted a proof‐of‐principle study to analyse the impacts of dietary microbiota in replicated experimental evolution lines of the flour beetle Tribolium castaneum, that separately evolved either constitutively expressed higher basal resistance, or inducible immune priming responses against their natural pathogen Bacillus thuringiensis (Bt) (Khan et al, 2017; Prakash et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Alteration of diet microbiota limits the experimentally evolved immune priming response in flour beetles, but not pathogen resistance

Prakash,

Agashe,

Khan

2023

Journal of Evolutionary Biology

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Host‐associated microbiota play a fundamental role in the training and induction of different forms of immunity, including inducible as well as constitutive components. However, direct experiments analysing the relative importance of microbiota on diverse forms of evolved immune functions are missing. We addressed this gap by using experimentally evolved lines of Tribolium castaneum that either produced inducible immune memory‐like responses (immune priming) or constitutively expressed basal resistance (without priming), as divergent counterstrategies against Bacillus thuringiensis infection. We altered the microbial communities present in the diet (i.e. wheat flour) of these evolved lines using UV irradiation and estimated the impact on the beetle's ability to mount a priming response versus basal resistance. Populations that had evolved immune priming lost the ability to mount a priming response upon alteration of diet microbiota. Microbiota manipulation also caused a drastic reduction in their reproductive output and post‐infection longevity. In contrast, in pathogen‐resistant beetles, microbiota manipulation did not affect post‐infection survival or reproduction. The divergent evolution of immune responses across beetle lines was thus associated with divergent reliance on the microbiome. Whether the latter is a direct outcome of differential pathogen exposure during selection or reflects evolved immune functions remains unclear. We hope that our results will motivate further experiments to understand the mechanistic basis of these complex evolutionary associations between microbiota, host immune strategies and fitness outcomes.

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Symbiont-mediated immune priming in animals through an evolutionary lens

Cited by 13 publications

References 123 publications

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

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

Tolerance-conferring defensive symbionts and the evolution of parasite virulence

Alteration of diet microbiota limits the experimentally evolved immune priming response in flour beetles, but not pathogen resistance

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