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          <full_title>Proceedings of the National Academy of Sciences</full_title>
          <abbrev_title>Proc. Natl. Acad. Sci. U.S.A.</abbrev_title>
          <issn media_type="print">0027-8424</issn>
          <issn media_type="electronic">1091-6490</issn>
        </journal_metadata>
        <journal_issue>
          <publication_date media_type="print">
            <month>03</month>
            <day>13</day>
            <year>2018</year>
          </publication_date>
          <journal_volume>
            <volume>115</volume>
          </journal_volume>
          <issue>11</issue>
        </journal_issue>
        <journal_article publication_type="full_text">
          <titles>
            <title>Transitory microbial habitat in the hyperarid Atacama Desert</title>
          </titles>
          <contributors>
            <person_name contributor_role="author" sequence="first">
              <given_name>Dirk</given_name>
              <surname>Schulze-Makuch</surname>
              <affiliation>Center of Astronomy &amp;amp; Astrophysics, Technical University Berlin, 10623 Berlin, Germany;</affiliation>
              <affiliation>School of the Environment, Washington State University, Pullman, WA 99164;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Dirk</given_name>
              <surname>Wagner</surname>
              <affiliation>Section Geomicrobiology, GFZ German Research Centre for Geosciences, 14473 Potsdam, Germany;</affiliation>
              <affiliation>Institute of Earth and Environmental Science, University of Potsdam, 14476 Potsdam, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Samuel P.</given_name>
              <surname>Kounaves</surname>
              <affiliation>Department of Chemistry, Tufts University, Medford, MA 02153;</affiliation>
              <affiliation>Department of Earth Science &amp;amp; Engineering, Imperial College London, London SW72AZ, United Kingdom;</affiliation>
              <ORCID authenticated="false">https://orcid.org/0000-0002-2629-4831</ORCID>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Kai</given_name>
              <surname>Mangelsdorf</surname>
              <affiliation>Section Organic Geochemistry, GFZ German Research Centre for Geosciences, 14473 Potsdam, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Kevin G.</given_name>
              <surname>Devine</surname>
              <affiliation>School of Human Sciences, London Metropolitan University, London N7 8BD, United Kingdom;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Jean-Pierre</given_name>
              <surname>de Vera</surname>
              <affiliation>Astrobiological Laboratories, Management and Infrastructure, Institute for Planetary Research, German Aerospace Center, 12489 Berlin, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Philippe</given_name>
              <surname>Schmitt-Kopplin</surname>
              <affiliation>Analytical Food Chemistry, Technical University München, 85354 Freising-Weihenstephan, Germany;</affiliation>
              <affiliation>Analytical BioGeoChemistry, Helmholtz Zentrum München, 85764 Oberschleissheim, Germany;</affiliation>
              <ORCID authenticated="false">https://orcid.org/0000-0003-0824-2664</ORCID>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Hans-Peter</given_name>
              <surname>Grossart</surname>
              <affiliation>Department of Experimental Limnology, Leibniz Institute of Freshwater Ecology and Inland Fisheries, 16775 Stechlin, Germany;</affiliation>
              <affiliation>Institute of Biochemistry &amp;amp; Biology, University of Potsdam, 14476 Potsdam, Germany;</affiliation>
              <ORCID authenticated="false">https://orcid.org/0000-0002-9141-0325</ORCID>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Victor</given_name>
              <surname>Parro</surname>
              <affiliation>Molecular Evolution Department, Centro de Astrobiología, Instituto Nacional de Técnica Aeroespacial-Consejo Superior de Investigaciones Científicas (INTA-CSIC), 28850 Madrid, Spain;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Martin</given_name>
              <surname>Kaupenjohann</surname>
              <affiliation>Fachgebiet Bodenkunde, Technical University Berlin, 10623 Berlin, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Albert</given_name>
              <surname>Galy</surname>
              <affiliation>Centre de Recherches Pétrographiques et Géochimiques, CNRS, Université de Lorraine, 54500 Vandoeuvre les Nancy, France;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Beate</given_name>
              <surname>Schneider</surname>
              <affiliation>Center of Astronomy &amp;amp; Astrophysics, Technical University Berlin, 10623 Berlin, Germany;</affiliation>
              <affiliation>Section Geomicrobiology, GFZ German Research Centre for Geosciences, 14473 Potsdam, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Alessandro</given_name>
              <surname>Airo</surname>
              <affiliation>Center of Astronomy &amp;amp; Astrophysics, Technical University Berlin, 10623 Berlin, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Jan</given_name>
              <surname>Frösler</surname>
              <affiliation>Biofilm Centre, University of Duisburg-Essen, 45141 Essen, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Alfonso F.</given_name>
              <surname>Davila</surname>
              <affiliation>Planetary Systems Branch (Code SST), NASA Ames Research Center, Moffett Field, CA 94035;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Felix L.</given_name>
              <surname>Arens</surname>
              <affiliation>Institute for Geological Sciences, Freie University Berlin, 12249 Berlin, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Luis</given_name>
              <surname>Cáceres</surname>
              <affiliation>Laboratorio de Microorganismos Extremófilos, University of Antofagasta, Antofagasta 02800, Chile;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Francisco Solís</given_name>
              <surname>Cornejo</surname>
              <affiliation>Laboratorio de Microorganismos Extremófilos, University of Antofagasta, Antofagasta 02800, Chile;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Daniel</given_name>
              <surname>Carrizo</surname>
              <affiliation>Molecular Evolution Department, Centro de Astrobiología, Instituto Nacional de Técnica Aeroespacial-Consejo Superior de Investigaciones Científicas (INTA-CSIC), 28850 Madrid, Spain;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Lewis</given_name>
              <surname>Dartnell</surname>
              <affiliation>Department of Life Sciences, University of Westminster, London W1W 6UW, United Kingdom;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Jocelyne</given_name>
              <surname>DiRuggiero</surname>
              <affiliation>Department of Biology, The John Hopkins University, Baltimore, MD 21218;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Markus</given_name>
              <surname>Flury</surname>
              <affiliation>Department of Crop &amp;amp; Soil Sciences, Washington State University, Pullman, WA 99164;</affiliation>
              <ORCID authenticated="false">https://orcid.org/0000-0002-3344-3962</ORCID>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Lars</given_name>
              <surname>Ganzert</surname>
              <affiliation>Department of Experimental Limnology, Leibniz Institute of Freshwater Ecology and Inland Fisheries, 16775 Stechlin, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Mark O.</given_name>
              <surname>Gessner</surname>
              <affiliation>Department of Experimental Limnology, Leibniz Institute of Freshwater Ecology and Inland Fisheries, 16775 Stechlin, Germany;</affiliation>
              <affiliation>Department of Ecology, Technical University Berlin, 10587 Berlin, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Peter</given_name>
              <surname>Grathwohl</surname>
              <affiliation>Center for Applied Geosciences, University of Tübingen, 72074 Tübingen, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Lisa</given_name>
              <surname>Guan</surname>
              <affiliation>Comparative Microbiome Analysis, Helmholtz Zentrum München, 85764 Oberschleissheim, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Jacob</given_name>
              <surname>Heinz</surname>
              <affiliation>Center of Astronomy &amp;amp; Astrophysics, Technical University Berlin, 10623 Berlin, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Matthias</given_name>
              <surname>Hess</surname>
              <affiliation>Systems Microbiology &amp;amp; Natural Products Laboratory, University of California, Davis, CA 95616;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Frank</given_name>
              <surname>Keppler</surname>
              <affiliation>Institute of Earth Sciences, Heidelberg University, 69120 Heidelberg, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Deborah</given_name>
              <surname>Maus</surname>
              <affiliation>Center of Astronomy &amp;amp; Astrophysics, Technical University Berlin, 10623 Berlin, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Christopher P.</given_name>
              <surname>McKay</surname>
              <affiliation>Planetary Systems Branch (Code SST), NASA Ames Research Center, Moffett Field, CA 94035;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Rainer U.</given_name>
              <surname>Meckenstock</surname>
              <affiliation>Biofilm Centre, University of Duisburg-Essen, 45141 Essen, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Wren</given_name>
              <surname>Montgomery</surname>
              <affiliation>Department of Earth Science &amp;amp; Engineering, Imperial College London, London SW72AZ, United Kingdom;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Elizabeth A.</given_name>
              <surname>Oberlin</surname>
              <affiliation>Department of Chemistry, Tufts University, Medford, MA 02153;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Alexander J.</given_name>
              <surname>Probst</surname>
              <affiliation>Biofilm Centre, University of Duisburg-Essen, 45141 Essen, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Johan S.</given_name>
              <surname>Sáenz</surname>
              <affiliation>Comparative Microbiome Analysis, Helmholtz Zentrum München, 85764 Oberschleissheim, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Tobias</given_name>
              <surname>Sattler</surname>
              <affiliation>Institute of Earth Sciences, Heidelberg University, 69120 Heidelberg, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Janosch</given_name>
              <surname>Schirmack</surname>
              <affiliation>Center of Astronomy &amp;amp; Astrophysics, Technical University Berlin, 10623 Berlin, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Mark A.</given_name>
              <surname>Sephton</surname>
              <affiliation>Department of Earth Science &amp;amp; Engineering, Imperial College London, London SW72AZ, United Kingdom;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Michael</given_name>
              <surname>Schloter</surname>
              <affiliation>Comparative Microbiome Analysis, Helmholtz Zentrum München, 85764 Oberschleissheim, Germany;</affiliation>
              <affiliation>Soil Science, Technical University München, 85354 Freising-Weihenstephan, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Jenny</given_name>
              <surname>Uhl</surname>
              <affiliation>Analytical BioGeoChemistry, Helmholtz Zentrum München, 85764 Oberschleissheim, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Bernardita</given_name>
              <surname>Valenzuela</surname>
              <affiliation>Laboratorio de Microorganismos Extremófilos, University of Antofagasta, Antofagasta 02800, Chile;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Gisle</given_name>
              <surname>Vestergaard</surname>
              <affiliation>Comparative Microbiome Analysis, Helmholtz Zentrum München, 85764 Oberschleissheim, Germany;</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Lars</given_name>
              <surname>Wörmer</surname>
              <affiliation>Center for Marine Environmental Sciences (MARUM), University of Bremen, 28359 Bremen, Germany</affiliation>
            </person_name>
            <person_name contributor_role="author" sequence="additional">
              <given_name>Pedro</given_name>
              <surname>Zamorano</surname>
              <affiliation>Laboratorio de Microorganismos Extremófilos, University of Antofagasta, Antofagasta 02800, Chile;</affiliation>
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          <abstract abstract-type="executive-summary">
            <title>Significance</title>
            <p>It has remained an unresolved question whether microorganisms recovered from the most arid environments on Earth are thriving under such extreme conditions or are just dead or dying vestiges of viable cells fortuitously deposited by atmospheric processes. Based on multiple lines of evidence, we show that indigenous microbial communities are present and temporally active even in the hyperarid soils of the Atacama Desert (Chile). Following extremely rare precipitation events in the driest parts of this desert, where rainfall often occurs only once per decade, we were able to detect episodic incidences of biological activity. Our findings expand the range of hyperarid environments temporarily habitable for terrestrial life, which by extension also applies to other planetary bodies like Mars.</p>
          </abstract>
          <abstract>
            <p>
              Traces of life are nearly ubiquitous on Earth. However, a central unresolved question is whether these traces always indicate an active microbial community or whether, in extreme environments, such as hyperarid deserts, they instead reflect just dormant or dead cells. Although microbial biomass and diversity decrease with increasing aridity in the Atacama Desert, we provide multiple lines of evidence for the presence of an at times metabolically active, microbial community in one of the driest places on Earth. We base this observation on four major lines of evidence: (
              <italic>i</italic>
              ) a physico-chemical characterization of the soil habitability after an exceptional rain event, (
              <italic>ii</italic>
              ) identified biomolecules indicative of potentially active cells [e.g., presence of ATP, phospholipid fatty acids (PLFAs), metabolites, and enzymatic activity], (
              <italic>iii</italic>
              ) measurements of in situ replication rates of genomes of uncultivated bacteria reconstructed from selected samples, and (
              <italic>iv</italic>
              ) microbial community patterns specific to soil parameters and depths. We infer that the microbial populations have undergone selection and adaptation in response to their specific soil microenvironment and in particular to the degree of aridity. Collectively, our results highlight that even the hyperarid Atacama Desert can provide a habitable environment for microorganisms that allows them to become metabolically active following an episodic increase in moisture and that once it decreases, so does the activity of the microbiota. These results have implications for the prospect of life on other planets such as Mars, which has transitioned from an earlier wetter environment to today’s extreme hyperaridity.
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            <month>02</month>
            <day>26</day>
            <year>2018</year>
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            <month>03</month>
            <day>13</day>
            <year>2018</year>
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          <pages>
            <first_page>2670</first_page>
            <last_page>2675</last_page>
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