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      Environmental factors influence cross-talk between a heat shock protein and an oxidative stress protein modification in the lizard Gallotia galloti

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          Abstract

          Better understanding how organisms respond to their abiotic environment, especially at the biochemical level, is critical in predicting population trajectories under climate change. In this study, we measured constitutive stress biomarkers and protein post-translational modifications associated with oxidative stress in Gallotia galloti, an insular lizard species inhabiting highly heterogeneous environments on Tenerife. Tenerife is a small volcanic island in a relatively isolated archipelago off the West coast of Africa. We found that expression of GRP94, a molecular chaperone protein, and levels of protein carbonylation, a marker of cellular stress, change across different environments, depending on solar radiation-related variables and topology. Here, we report in a wild animal population, cross-talk between the baseline levels of the heat shock protein-like GRP94 and oxidative damage (protein carbonylation), which are influenced by a range of available temperatures, quantified through modelled operative temperature. This suggests a dynamic trade-off between cellular homeostasis and oxidative damage in lizards adapted to this thermally and topologically heterogeneous environment.

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          NIH Image to ImageJ: 25 years of image analysis

          For the past twenty five years the NIH family of imaging software, NIH Image and ImageJ have been pioneers as open tools for scientific image analysis. We discuss the origins, challenges and solutions of these two programs, and how their history can serve to advise and inform other software projects.
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            The heat-shock response.

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              Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation.

              Physiological thermal-tolerance limits of terrestrial ectotherms often exceed local air temperatures, implying a high degree of thermal safety (an excess of warm or cold thermal tolerance). However, air temperatures can be very different from the equilibrium body temperature of an individual ectotherm. Here, we compile thermal-tolerance limits of ectotherms across a wide range of latitudes and elevations and compare these thermal limits both to air and to operative body temperatures (theoretically equilibrated body temperatures) of small ectothermic animals during the warmest and coldest times of the year. We show that extreme operative body temperatures in exposed habitats match or exceed the physiological thermal limits of most ectotherms. Therefore, contrary to previous findings using air temperatures, most ectotherms do not have a physiological thermal-safety margin. They must therefore rely on behavior to avoid overheating during the warmest times, especially in the lowland tropics. Likewise, species living at temperate latitudes and in alpine habitats must retreat to avoid lethal cold exposure. Behavioral plasticity of habitat use and the energetic consequences of thermal retreats are therefore critical aspects of species' vulnerability to climate warming and extreme events.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: MethodologyRole: Resources
                Role: InvestigationRole: MethodologyRole: Resources
                Role: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                PLOS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                12 March 2024
                2024
                : 19
                : 3
                : e0300111
                Affiliations
                [1 ] School of Natural Sciences, The University of Hull, Hull, United Kingdom
                [2 ] Energy and Environment Institute, The University of Hull, Hull, United Kingdom
                [3 ] National Institute of Biology, Ljubljana, Slovenia
                [4 ] CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto Campus de Vairão, Vairão, Portugal
                [5 ] Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), La Laguna, Tenerife, Canary Islands, Spain
                [6 ] Universidad de Alcalá (UAH), Biomedicine and Biotechnology, Alcalá de Henares, Madrid, Spain
                [7 ] BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Campus de Vairão, Vairão, Portugal
                [8 ] Biomedical Institute for Multimorbidity, Centre for Biomedicine, Hull York Medical School, The University of Hull, Hull, United Kingdom
                [9 ] Department of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, VA, United States of America
                [10 ] Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Porto, Portugal
                [11 ] School of Biology and Environmental Science, University College Dublin, Belfield Campus, Dublin, Ireland
                Oklahoma State University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                ‡ PBA and KCWV contributed equally as corresponding authors to this work.

                Author information
                https://orcid.org/0000-0003-3273-1986
                https://orcid.org/0000-0002-7611-1298
                https://orcid.org/0000-0002-3556-9796
                https://orcid.org/0000-0002-2335-7198
                https://orcid.org/0000-0001-8136-8963
                https://orcid.org/0000-0001-8858-1804
                Article
                PONE-D-23-22705
                10.1371/journal.pone.0300111
                10931494
                38470891
                2b8b5a21-772f-49c7-a35c-ab7291765aed
                © 2024 Gilbert et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 19 July 2023
                : 21 February 2024
                Page count
                Figures: 4, Tables: 1, Pages: 21
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100010663, H2020 European Research Council;
                Award ID: 101044202
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000270, Natural Environment Research Council;
                Award ID: NE/S007458/1
                Award Recipient :
                Funded by: Slovenian Research and Innovation Agency
                Award ID: P1-0255
                Award Recipient :
                Funded by: Fundação para a Ciência e Tecnologia
                Award ID: 28014 02/SAICT/2017
                Award Recipient :
                Funded by: Slovenian Research and Innovation Agency
                Award ID: J1-2466
                Award Recipient :
                Funded by: MINECO/ERDF
                Award ID: CGL2015-67789-C2-1-P
                Funded by: FCT
                Award ID: CEECIND/04084/2017
                EG, PBA and KWV were supported by the Leeds-York-Hull Natural Environment Research Council (NERC) Doctoral Training Partnership (DTP) Panorama under grant NE/S007458/1 https://panorama-dtp.ac.uk/ KWV acknowledges funding by the European Union (ERC, MolStressH2O, 101044202). https://erc.europa.eu/homepage AZ fieldwork was funded by FCT - Fundação para a Ciência e Tecnologia (project num. 28014 02/SAICT/2017) and by ARIS - Slovenian Research and Innovation Agency (programme P1-0255). This work was also funded by MINECO/ERDF (CGL2015-67789-C2-1-P) and FCT (CEECIND/04084/2017). AZ acknowledges funding by ARIS under project grant J1-2466 during article writing. There was no additional external funding received during this study.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Reptiles
                Squamates
                Lizards
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amniotes
                Reptiles
                Squamates
                Lizards
                Biology and Life Sciences
                Biochemistry
                Biomarkers
                Physical Sciences
                Physics
                Electromagnetic Radiation
                Solar Radiation
                Biology and Life Sciences
                Cell Biology
                Oxidative Stress
                Biology and Life Sciences
                Physiology
                Physiological Parameters
                Body Temperature
                Biology and Life Sciences
                Biochemistry
                Oxidative Damage
                Earth Sciences
                Atmospheric Science
                Meteorology
                Humidity
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cellular Stress Responses
                Heat Shock Response
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files. Data used in analysis and R code is available at: https://github.com/RepTed/Proteins-in-G.-galloti.git.

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