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      Specific adaptations are selected in opposite sun exposed Antarctic cryptoendolithic communities as revealed by untargeted metabolomics

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          Abstract

          Antarctic cryptoendolithic communities are self-supporting borderline ecosystems spreading across the extreme conditions of the Antarctic desert and represent the predominant life-form in the ice-free areas of McMurdo Dry Valleys, accounted as the closest terrestrial Martian analogue. Components of these communities are highly adapted extremophiles and extreme-tolerant microorganisms, among the most resistant known to date. Recently, studies investigated biodiversity and community composition in these ecosystems but the metabolic activity of the metacommunity has never been investigated. Using an untargeted metabolomics, we explored stress-response of communities spreading in two sites of the same location, subjected to increasing environmental pressure due to opposite sun exposure, accounted as main factor influencing the diversity and composition of these ecosystems. Overall, 331 altered metabolites (206 and 125 unique for north and south, respectively), distinguished the two differently exposed communities. We also selected 10 metabolites and performed two-stage Receiver Operating Characteristic (ROC) analysis to test them as potential biomarkers. We further focused on melanin and allantoin as protective substances; their concentration was highly different in the community in the shadow or in the sun. These results clearly indicate that opposite insolation selected organisms in the communities with different adaptation strategies in terms of key metabolites produced.

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          Untargeted Metabolomics Strategies—Challenges and Emerging Directions

          Metabolites are building blocks of cellular function. These species are involved in enzyme-catalyzed chemical reactions and are essential for cellular function. Upstream biological disruptions result in a series of metabolomic changes, and as such the metabolome holds a wealth of information that is thought to be most predictive of phenotype. Uncovering this knowledge is a work in progress. The field of metabolomics is still maturing; the community has leveraged proteomics experience when applicable and developed a range of sample preparation and instrument methodology along with myriad data processing and analysis approaches. Research focuses have now shifted toward a fundamental understanding of the biology responsible for metabolomic changes. There are several types of metabolomics experiments including both targeted and untargeted analyses. While untargeted, hypothesis generating, workflows exhibit many valuable attributes, challenges inherent to the approach remain. This Critical Insight comments on these challenges, focusing on the identification process of LC-MS based untargeted metabolomics studies – specifically in mammalian systems. Biological interpretation of metabolomics data hinges on the ability to accurately identify metabolites. The range of confidence associated with identifications that is often overlooked is reviewed, and opportunities for advancing the metabolomics field are described.
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            Exploring the temperature-stress metabolome of Arabidopsis.

            Metabolic profiling analyses were performed to determine metabolite temporal dynamics associated with the induction of acquired thermotolerance in response to heat shock and acquired freezing tolerance in response to cold shock. Low-M(r) polar metabolite analyses were performed using gas chromatography-mass spectrometry. Eighty-one identified metabolites and 416 unidentified mass spectral tags, characterized by retention time indices and specific mass fragments, were monitored. Cold shock influenced metabolism far more profoundly than heat shock. The steady-state pool sizes of 143 and 311 metabolites or mass spectral tags were altered in response to heat and cold shock, respectively. Comparison of heat- and cold-shock response patterns revealed that the majority of heat-shock responses were shared with cold-shock responses, a previously unknown relationship. Coordinate increases in the pool sizes of amino acids derived from pyruvate and oxaloacetate, polyamine precursors, and compatible solutes were observed during both heat and cold shock. In addition, many of the metabolites that showed increases in response to both heat and cold shock in this study were previously unlinked with temperature stress. This investigation provides new insight into the mechanisms of plant adaptation to thermal stress at the metabolite level, reveals relationships between heat- and cold-shock responses, and highlights the roles of known signaling molecules and protectants.
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              Psychrophilic microorganisms: challenges for life.

              The ability of psychrophiles to survive and proliferate at low temperatures implies that they have overcome key barriers inherent to permanently cold environments. These challenges include: reduced enzyme activity; decreased membrane fluidity; altered transport of nutrients and waste products; decreased rates of transcription, translation and cell division; protein cold-denaturation; inappropriate protein folding; and intracellular ice formation. Cold-adapted organisms have successfully evolved features, genotypic and/or phenotypic, to surmount the negative effects of low temperatures and to enable growth in these extreme environments. In this review, we discuss the current knowledge of these adaptations as gained from extensive biochemical and biophysical studies and also from genomics and proteomics.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Writing – review & editing
                Role: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                27 May 2020
                2020
                : 15
                : 5
                : e0233805
                Affiliations
                [1 ] Department of Ecological and Biological Sciences, University of Tuscia, Viterbo, Italy
                [2 ] Department of Science and Technology for Agriculture, Forestry, Nature and Energy, University of Tuscia, Viterbo, Italy
                [3 ] Italian National Antarctic Museum (MNA), Mycological Section, Genoa, Italy
                Free University of Bozen-Bolzano, ITALY
                Author notes

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

                Author information
                http://orcid.org/0000-0002-9289-6179
                Article
                PONE-D-20-03835
                10.1371/journal.pone.0233805
                7253227
                32460306
                145ec964-2cb6-4b7e-a00b-81c50ddf87f1
                © 2020 Coleine 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
                : 10 February 2020
                : 12 May 2020
                Page count
                Figures: 5, Tables: 0, Pages: 17
                Funding
                L.S. and C.C. wish to thank the Italian National Program for Antarctic Researches (PNRA) for funding sampling campaigns and researches in Italy in the frame of the PNRA projects. The Italian Antarctic National Museum (MNA) is kindly acknowledged for financial support to the Mycological Section on the MNA for preserving Antarctic rock samples, herein analysed, stored in the Culture Collection of Fungi from Extreme Environments (CCFEE), University of Tuscia, Italy. The authors wish to thank Italian Space Agency (ASI n. 2018-6-U0) for co-funding the BIOSIGN-Microfossils project.
                Categories
                Research Article
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolites
                People and Places
                Geographical Locations
                Antarctica
                Physical Sciences
                Materials Science
                Materials
                Pigments
                Organic Pigments
                Melanin
                Biology and Life Sciences
                Organisms
                Eukaryota
                Fungi
                Biology and Life Sciences
                Biochemistry
                Biomarkers
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolomics
                Biology and Life Sciences
                Plant Science
                Plant Physiology
                Plant Defenses
                Plant Resistance to Abiotic Stress
                Biology and Life Sciences
                Plant Science
                Plant Pathology
                Plant Resistance to Abiotic Stress
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Plant-Environment Interactions
                Plant Resistance to Abiotic Stress
                Ecology and Environmental Sciences
                Ecology
                Plant Ecology
                Plant-Environment Interactions
                Plant Resistance to Abiotic Stress
                Biology and Life Sciences
                Plant Science
                Plant Ecology
                Plant-Environment Interactions
                Plant Resistance to Abiotic Stress
                Earth Sciences
                Geomorphology
                Topography
                Landforms
                Valleys
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Uncategorized
                Uncategorized

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