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Insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection

BACKGROUND: Previous exposure to a pathogen can help organisms cope with recurring infection. This is widely recognised in vertebrates, but increasing occasions are also being reported in invertebrates where this phenomenon is referred to as immune priming. However, the mechanisms that allow acquire...

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Autores principales: Mikonranta, Lauri, Mappes, Johanna, Kaukoniitty, Minna, Freitak, Dalial
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3975449/
https://www.ncbi.nlm.nih.gov/pubmed/24602309
http://dx.doi.org/10.1186/1742-9994-11-23
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author Mikonranta, Lauri
Mappes, Johanna
Kaukoniitty, Minna
Freitak, Dalial
author_facet Mikonranta, Lauri
Mappes, Johanna
Kaukoniitty, Minna
Freitak, Dalial
author_sort Mikonranta, Lauri
collection PubMed
description BACKGROUND: Previous exposure to a pathogen can help organisms cope with recurring infection. This is widely recognised in vertebrates, but increasing occasions are also being reported in invertebrates where this phenomenon is referred to as immune priming. However, the mechanisms that allow acquired pathogen resistance in insects remain largely unknown. RESULTS: We studied the priming of bacterial resistance in the larvae of the tiger moth, Parasemia plantaginis using two gram-negative bacteria, a pathogenic Serratia marcescens and a non-pathogenic control, Escherichia coli. A sublethal oral dose of S. marcescens provided the larvae with effective protection against an otherwise lethal septic infection with the same pathogen five days later. At the same time, we assessed three anti-bacterial defence mechanisms from the larvae that had been primarily exposed to the bacteria via contaminated host plant. Results showed that S. marcescens had induced a higher amount of reactive oxygen species (ROS) in the larval haemolymph, possibly protecting the host from the recurring infection. CONCLUSIONS: Our study supports the growing evidence of immune priming in insects. It shows that activation of the protective mechanism requires a specific induction, rather than a sheer exposure to any gram-negative bacteria. The findings indicate that systemic pathogen recognition happens via the gut, and suggest that persistent loitering of immune elicitors or anti-microbial molecules are a possible mechanism for the observed prophylaxis. The self-harming effects of ROS molecules are well known, which indicates a potential cost of increased resistance. Together these findings could have important implications on the ecological and epidemiological processes affecting insect and pathogen populations.
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spelling pubmed-39754492014-04-05 Insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection Mikonranta, Lauri Mappes, Johanna Kaukoniitty, Minna Freitak, Dalial Front Zool Research BACKGROUND: Previous exposure to a pathogen can help organisms cope with recurring infection. This is widely recognised in vertebrates, but increasing occasions are also being reported in invertebrates where this phenomenon is referred to as immune priming. However, the mechanisms that allow acquired pathogen resistance in insects remain largely unknown. RESULTS: We studied the priming of bacterial resistance in the larvae of the tiger moth, Parasemia plantaginis using two gram-negative bacteria, a pathogenic Serratia marcescens and a non-pathogenic control, Escherichia coli. A sublethal oral dose of S. marcescens provided the larvae with effective protection against an otherwise lethal septic infection with the same pathogen five days later. At the same time, we assessed three anti-bacterial defence mechanisms from the larvae that had been primarily exposed to the bacteria via contaminated host plant. Results showed that S. marcescens had induced a higher amount of reactive oxygen species (ROS) in the larval haemolymph, possibly protecting the host from the recurring infection. CONCLUSIONS: Our study supports the growing evidence of immune priming in insects. It shows that activation of the protective mechanism requires a specific induction, rather than a sheer exposure to any gram-negative bacteria. The findings indicate that systemic pathogen recognition happens via the gut, and suggest that persistent loitering of immune elicitors or anti-microbial molecules are a possible mechanism for the observed prophylaxis. The self-harming effects of ROS molecules are well known, which indicates a potential cost of increased resistance. Together these findings could have important implications on the ecological and epidemiological processes affecting insect and pathogen populations. BioMed Central 2014-03-07 /pmc/articles/PMC3975449/ /pubmed/24602309 http://dx.doi.org/10.1186/1742-9994-11-23 Text en Copyright © 2014 Mikonranta et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/4.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Mikonranta, Lauri
Mappes, Johanna
Kaukoniitty, Minna
Freitak, Dalial
Insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection
title Insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection
title_full Insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection
title_fullStr Insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection
title_full_unstemmed Insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection
title_short Insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection
title_sort insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3975449/
https://www.ncbi.nlm.nih.gov/pubmed/24602309
http://dx.doi.org/10.1186/1742-9994-11-23
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