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Increasing temperature-driven changes in life history traits and gene expression of an Antarctic tardigrade species

The Antarctic region has been experiencing some of the planet’s strongest climatic changes, including an expected increase of the land temperature. The potential effects of this warming trend will lead ecosystems to a risk of losing biodiversity. Antarctic mosses and lichens host different microbial...

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Autores principales: Giovannini, Ilaria, Manfrin, Chiara, Greco, Samuele, Vincenzi, Joel, Altiero, Tiziana, Guidetti, Roberto, Giulianini, Piero, Rebecchi, Lorena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10520964/
https://www.ncbi.nlm.nih.gov/pubmed/37766751
http://dx.doi.org/10.3389/fphys.2023.1258932
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author Giovannini, Ilaria
Manfrin, Chiara
Greco, Samuele
Vincenzi, Joel
Altiero, Tiziana
Guidetti, Roberto
Giulianini, Piero
Rebecchi, Lorena
author_facet Giovannini, Ilaria
Manfrin, Chiara
Greco, Samuele
Vincenzi, Joel
Altiero, Tiziana
Guidetti, Roberto
Giulianini, Piero
Rebecchi, Lorena
author_sort Giovannini, Ilaria
collection PubMed
description The Antarctic region has been experiencing some of the planet’s strongest climatic changes, including an expected increase of the land temperature. The potential effects of this warming trend will lead ecosystems to a risk of losing biodiversity. Antarctic mosses and lichens host different microbial groups, micro-arthropods and meiofaunal organisms (e.g., tardigrades, rotifers). The eutardigrade Acutuncus antarcticus is considered a model animal to study the effect of increasing temperature due to global warming on Antarctic terrestrial communities. In this study, life history traits and fitness of this species are analyzed by rearing specimens at two different and increasing temperatures (5°C vs. 15°C). Moreover, the first transcriptome analysis on A. antarcticus is performed, exposing adult animals to a gradual increase of temperature (5°C, 10°C, 15°C, and 20°C) to find differentially expressed genes under short- (1 day) and long-term (15 days) heat stress. Acutuncus antarcticus specimens reared at 5°C live longer (maximum life span: 686 days), reach sexual maturity later, lay more eggs (which hatch in longer time and in lower percentage) compared with animals reared at 15°C. The fitness decreases in animals belonging to the second generation at both rearing temperatures. The short-term heat exposure leads to significant changes at transcriptomic level, with 67 differentially expressed genes. Of these, 23 upregulated genes suggest alterations of mitochondrial activity and oxido-reductive processes, and two intrinsically disordered protein genes confirm their role to cope with heat stress. The long-term exposure induces alterations limited to 14 genes, and only one annotated gene is upregulated in response to both heat stresses. The decline in transcriptomic response after a long-term exposure indicates that the changes observed in the short-term are likely due to an acclimation response. Therefore, A. antarcticus could be able to cope with increasing temperature over time, including the future conditions imposed by global climate change.
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spelling pubmed-105209642023-09-27 Increasing temperature-driven changes in life history traits and gene expression of an Antarctic tardigrade species Giovannini, Ilaria Manfrin, Chiara Greco, Samuele Vincenzi, Joel Altiero, Tiziana Guidetti, Roberto Giulianini, Piero Rebecchi, Lorena Front Physiol Physiology The Antarctic region has been experiencing some of the planet’s strongest climatic changes, including an expected increase of the land temperature. The potential effects of this warming trend will lead ecosystems to a risk of losing biodiversity. Antarctic mosses and lichens host different microbial groups, micro-arthropods and meiofaunal organisms (e.g., tardigrades, rotifers). The eutardigrade Acutuncus antarcticus is considered a model animal to study the effect of increasing temperature due to global warming on Antarctic terrestrial communities. In this study, life history traits and fitness of this species are analyzed by rearing specimens at two different and increasing temperatures (5°C vs. 15°C). Moreover, the first transcriptome analysis on A. antarcticus is performed, exposing adult animals to a gradual increase of temperature (5°C, 10°C, 15°C, and 20°C) to find differentially expressed genes under short- (1 day) and long-term (15 days) heat stress. Acutuncus antarcticus specimens reared at 5°C live longer (maximum life span: 686 days), reach sexual maturity later, lay more eggs (which hatch in longer time and in lower percentage) compared with animals reared at 15°C. The fitness decreases in animals belonging to the second generation at both rearing temperatures. The short-term heat exposure leads to significant changes at transcriptomic level, with 67 differentially expressed genes. Of these, 23 upregulated genes suggest alterations of mitochondrial activity and oxido-reductive processes, and two intrinsically disordered protein genes confirm their role to cope with heat stress. The long-term exposure induces alterations limited to 14 genes, and only one annotated gene is upregulated in response to both heat stresses. The decline in transcriptomic response after a long-term exposure indicates that the changes observed in the short-term are likely due to an acclimation response. Therefore, A. antarcticus could be able to cope with increasing temperature over time, including the future conditions imposed by global climate change. Frontiers Media S.A. 2023-09-12 /pmc/articles/PMC10520964/ /pubmed/37766751 http://dx.doi.org/10.3389/fphys.2023.1258932 Text en Copyright © 2023 Giovannini, Manfrin, Greco, Vincenzi, Altiero, Guidetti, Giulianini and Rebecchi. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Giovannini, Ilaria
Manfrin, Chiara
Greco, Samuele
Vincenzi, Joel
Altiero, Tiziana
Guidetti, Roberto
Giulianini, Piero
Rebecchi, Lorena
Increasing temperature-driven changes in life history traits and gene expression of an Antarctic tardigrade species
title Increasing temperature-driven changes in life history traits and gene expression of an Antarctic tardigrade species
title_full Increasing temperature-driven changes in life history traits and gene expression of an Antarctic tardigrade species
title_fullStr Increasing temperature-driven changes in life history traits and gene expression of an Antarctic tardigrade species
title_full_unstemmed Increasing temperature-driven changes in life history traits and gene expression of an Antarctic tardigrade species
title_short Increasing temperature-driven changes in life history traits and gene expression of an Antarctic tardigrade species
title_sort increasing temperature-driven changes in life history traits and gene expression of an antarctic tardigrade species
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10520964/
https://www.ncbi.nlm.nih.gov/pubmed/37766751
http://dx.doi.org/10.3389/fphys.2023.1258932
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