Characterization and expression of heat shock and immune genes in natural populations of Prodiamesa olivacea (Diptera) exposed to thermal stress

This paper characterizes the heat stress response (HSR) and explores the impact of temperatures on the immune response of larvae from two chironomid species, Prodiamesa olivacea and Chironomus riparius. Genes involved in crucial metabolic pathways were de novo identified in P. olivacea: Hsp27, Hsp60...

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Main Authors: Lola Llorente, Mónica Aquilino, Óscar Herrero, Eduardo de la Peña, Rosario Planelló
Format: Article
Language:English
Published: Elsevier 2023-09-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651323008631
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author Lola Llorente
Mónica Aquilino
Óscar Herrero
Eduardo de la Peña
Rosario Planelló
author_facet Lola Llorente
Mónica Aquilino
Óscar Herrero
Eduardo de la Peña
Rosario Planelló
author_sort Lola Llorente
collection DOAJ
description This paper characterizes the heat stress response (HSR) and explores the impact of temperatures on the immune response of larvae from two chironomid species, Prodiamesa olivacea and Chironomus riparius. Genes involved in crucial metabolic pathways were de novo identified in P. olivacea: Hsp27, Hsp60, Hsp70, Hsc70, Cdc37, and HSF for the heat stress response (HSR) and TOLL, PGRP, C-type lectin, and JAK/hopscotch for the immune system response (ISR). Quantitative real-time PCR was used to evaluate the expression levels of the selected genes in short-term treatments (up to 120') at high temperatures (35 °C and 39 °C). Exposing P. olivacea to elevated temperatures resulted in HSR induction with increased expression of specific heat shock genes, suggesting the potential of HSPs as early indicators of acute thermal stress. Surprisingly, we found that heat shock represses multiple immune genes, revealing the antagonist relation between the heat shock response and the innate immune response in P. olivacea. Our results also showed species-dependent gene responses, with more significant effects in P. olivacea, for most of the biomarkers studied, demonstrating a higher sensitivity in this species to environmental stress conditions than that of C. riparius. This work shows a multi-species approach that enables a deeper understanding of the effects of heat stress at the molecular level in aquatic dipterans.
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spelling doaj.art-7aa00869bfd3454b87ca61086f53f72a2023-09-16T05:28:32ZengElsevierEcotoxicology and Environmental Safety0147-65132023-09-01263115359Characterization and expression of heat shock and immune genes in natural populations of Prodiamesa olivacea (Diptera) exposed to thermal stressLola Llorente0Mónica Aquilino1Óscar Herrero2Eduardo de la Peña3Rosario Planelló4Biology and Environmental Toxicology Group, Faculty of Science, Universidad Nacional de Educación a Distancia (UNED), 28232, Las Rozas, Madrid, SpainBiology and Environmental Toxicology Group, Faculty of Science, Universidad Nacional de Educación a Distancia (UNED), 28232, Las Rozas, Madrid, Spain; School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UKBiology and Environmental Toxicology Group, Faculty of Science, Universidad Nacional de Educación a Distancia (UNED), 28232, Las Rozas, Madrid, SpainInstitute for Subtropical and Mediterranean Horticulture (IHSM-UMA-CSIC), Spanish National Research Council (CSIC), Finca Experimental La Mayora, Algarrobo-Costa, 29750 Malaga, Spain; Department of Plants and Crops, Faculty of Bio-science Engineering, Ghent University, Coupure Links 653, Ghent 9000, BelgiumBiology and Environmental Toxicology Group, Faculty of Science, Universidad Nacional de Educación a Distancia (UNED), 28232, Las Rozas, Madrid, Spain; Corresponding author.This paper characterizes the heat stress response (HSR) and explores the impact of temperatures on the immune response of larvae from two chironomid species, Prodiamesa olivacea and Chironomus riparius. Genes involved in crucial metabolic pathways were de novo identified in P. olivacea: Hsp27, Hsp60, Hsp70, Hsc70, Cdc37, and HSF for the heat stress response (HSR) and TOLL, PGRP, C-type lectin, and JAK/hopscotch for the immune system response (ISR). Quantitative real-time PCR was used to evaluate the expression levels of the selected genes in short-term treatments (up to 120') at high temperatures (35 °C and 39 °C). Exposing P. olivacea to elevated temperatures resulted in HSR induction with increased expression of specific heat shock genes, suggesting the potential of HSPs as early indicators of acute thermal stress. Surprisingly, we found that heat shock represses multiple immune genes, revealing the antagonist relation between the heat shock response and the innate immune response in P. olivacea. Our results also showed species-dependent gene responses, with more significant effects in P. olivacea, for most of the biomarkers studied, demonstrating a higher sensitivity in this species to environmental stress conditions than that of C. riparius. This work shows a multi-species approach that enables a deeper understanding of the effects of heat stress at the molecular level in aquatic dipterans.http://www.sciencedirect.com/science/article/pii/S0147651323008631ChironomidsTranscriptional biomarkersImmune system responseHeat shock responseGlobal changeSentinel organism
spellingShingle Lola Llorente
Mónica Aquilino
Óscar Herrero
Eduardo de la Peña
Rosario Planelló
Characterization and expression of heat shock and immune genes in natural populations of Prodiamesa olivacea (Diptera) exposed to thermal stress
Ecotoxicology and Environmental Safety
Chironomids
Transcriptional biomarkers
Immune system response
Heat shock response
Global change
Sentinel organism
title Characterization and expression of heat shock and immune genes in natural populations of Prodiamesa olivacea (Diptera) exposed to thermal stress
title_full Characterization and expression of heat shock and immune genes in natural populations of Prodiamesa olivacea (Diptera) exposed to thermal stress
title_fullStr Characterization and expression of heat shock and immune genes in natural populations of Prodiamesa olivacea (Diptera) exposed to thermal stress
title_full_unstemmed Characterization and expression of heat shock and immune genes in natural populations of Prodiamesa olivacea (Diptera) exposed to thermal stress
title_short Characterization and expression of heat shock and immune genes in natural populations of Prodiamesa olivacea (Diptera) exposed to thermal stress
title_sort characterization and expression of heat shock and immune genes in natural populations of prodiamesa olivacea diptera exposed to thermal stress
topic Chironomids
Transcriptional biomarkers
Immune system response
Heat shock response
Global change
Sentinel organism
url http://www.sciencedirect.com/science/article/pii/S0147651323008631
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AT oscarherrero characterizationandexpressionofheatshockandimmunegenesinnaturalpopulationsofprodiamesaolivaceadipteraexposedtothermalstress
AT eduardodelapena characterizationandexpressionofheatshockandimmunegenesinnaturalpopulationsofprodiamesaolivaceadipteraexposedtothermalstress
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