{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T01:14:48Z","timestamp":1791422088418,"version":"4.3.3"},"reference-count":42,"publisher":"National Academy of Sciences","issue":"46","license":[{"start":{"date-parts":[[2008,11,12]],"date-time":"2008-11-12T00:00:00Z","timestamp":1226448000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.pnas.org\/site\/misc\/userlicense.xhtml"}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2008,11,18]]},"abstract":"<jats:p>\n                    Quantitative information on the ecophysiology of individual microorganisms is generally limited because it is difficult to assign specific metabolic activities to identified single cells. Here, we develop and apply a method, Halogen In Situ Hybridization-Secondary Ion Mass Spectroscopy (HISH-SIMS), and show that it allows simultaneous phylogenetic identification and quantitation of metabolic activities of single microbial cells in the environment. Using HISH-SIMS, individual cells of the anaerobic, phototropic bacteria\n                    <jats:italic>Chromatium okenii<\/jats:italic>\n                    ,\n                    <jats:italic>Lamprocystis purpurea<\/jats:italic>\n                    , and\n                    <jats:italic>Chlorobium clathratiforme<\/jats:italic>\n                    inhabiting the oligotrophic, meromictic Lake Cadagno were analyzed with respect to H\n                    <jats:sup>13<\/jats:sup>\n                    CO\n                    <jats:sub arrange=\"stack\">3<\/jats:sub>\n                    <jats:sup arrange=\"stack\">\u2212<\/jats:sup>\n                    and\n                    <jats:sup>15<\/jats:sup>\n                    NH\n                    <jats:sub arrange=\"stack\">4<\/jats:sub>\n                    <jats:sup arrange=\"stack\">+<\/jats:sup>\n                    assimilation. Metabolic rates were found to vary greatly between individual cells of the same species, showing that microbial populations in the environment are heterogeneous, being comprised of physiologically distinct individuals. Furthermore,\n                    <jats:italic>C. okenii<\/jats:italic>\n                    , the least abundant species representing \u22480.3% of the total cell number, contributed more than 40% of the total uptake of ammonium and 70% of the total uptake of carbon in the system, thereby emphasizing that numerically inconspicuous microbes can play a significant role in the nitrogen and carbon cycles in the environment. By introducing this quantification method for the ecophysiological roles of individual cells, our study opens a variety of possibilities of research in environmental microbiology, especially by increasing the ability to examine the ecophysiological roles of individual cells, including those of less abundant and less active microbes, and by the capacity to track not only nitrogen and carbon but also phosphorus, sulfur, and other biological element flows within microbial communities.\n                  <\/jats:p>","DOI":"10.1073\/pnas.0809329105","type":"journal-article","created":{"date-parts":[[2008,11,12]],"date-time":"2008-11-12T20:58:35Z","timestamp":1226523515000},"page":"17861-17866","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":404,"title":["A single-cell view on the ecophysiology of anaerobic phototrophic bacteria"],"prefix":"10.1073","volume":"105","author":[{"given":"Niculina","family":"Musat","sequence":"first","affiliation":[{"name":"Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, 28359 Bremen, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hannah","family":"Halm","sequence":"additional","affiliation":[{"name":"Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, 28359 Bremen, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B\u00e4rbel","family":"Winterholler","sequence":"additional","affiliation":[{"name":"Max Planck Institute for Chemistry, Johann-Joachim-Becher Weg 27, 55128 Mainz, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Hoppe","sequence":"additional","affiliation":[{"name":"Max Planck Institute for Chemistry, Johann-Joachim-Becher Weg 27, 55128 Mainz, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandro","family":"Peduzzi","sequence":"additional","affiliation":[{"name":"Cantonal Institute of Microbiology and Alpine Biology Center Foundation Piora, Via Mirasole 22A, CH-6500 Bellinzona, Switzerland; and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francois","family":"Hillion","sequence":"additional","affiliation":[{"name":"Cameca, Quai des Gresillons 29, 92622 Gennevilliers Cedex, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francois","family":"Horreard","sequence":"additional","affiliation":[{"name":"Cameca, Quai des Gresillons 29, 92622 Gennevilliers Cedex, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rudolf","family":"Amann","sequence":"additional","affiliation":[{"name":"Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, 28359 Bremen, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bo B.","family":"J\u00f8rgensen","sequence":"additional","affiliation":[{"name":"Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, 28359 Bremen, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcel M. M.","family":"Kuypers","sequence":"additional","affiliation":[{"name":"Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, 28359 Bremen, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2008,11,18]]},"reference":[{"key":"e_1_3_3_1_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrg820"},{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.micro.57.030502.090759"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature02649"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1369-5274(02)00353-3"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1462-2920.2004.00668.x"},{"key":"e_1_3_3_6_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1061338"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1038\/ismej.2007.30"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.68.8.4067-4073.2002"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1186\/jbiol42"},{"key":"e_1_3_3_10_2","doi-asserted-by":"publisher","DOI":"10.1038\/ismej.2007.44"},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1145557"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1462-2920.2006.01222_5.x"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1462-2920.2007.01478.x"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1007\/PL00001345"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.65.3.1325-1330.1999"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.4081\/jlimnol.2004.161"},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.71.7.3544-3550.2005"},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1007\/0-387-30747-8_13"},{"key":"e_1_3_3_19_2","doi-asserted-by":"publisher","DOI":"10.1007\/0-387-30746-X_31"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1007\/0-306-47954-0_4"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.1007\/PL00001353"},{"key":"e_1_3_3_22_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6941.2003.tb01048.x"},{"key":"e_1_3_3_23_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.83.7.2138"},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00249026"},{"key":"e_1_3_3_25_2","first-page":"26","volume-title":"The Sea","author":"Redfield A","year":"1963","unstructured":"A Redfield, B Ketchum, F Richards, The influence of organisms on the composition of sea-water. The Sea, ed M Hill (Interscience, New York), pp. 26\u201377 (1963)."},{"key":"e_1_3_3_26_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00877431"},{"key":"e_1_3_3_27_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00409947"},{"key":"e_1_3_3_28_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00425577"},{"key":"e_1_3_3_29_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00425181"},{"key":"e_1_3_3_30_2","doi-asserted-by":"publisher","DOI":"10.1128\/aem.55.1.78-85.1989"},{"key":"e_1_3_3_31_2","doi-asserted-by":"publisher","DOI":"10.4319\/lo.1998.43.6.1262"},{"key":"e_1_3_3_32_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6968.1990.tb04073.x"},{"key":"e_1_3_3_33_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-642-74890-5_9"},{"key":"e_1_3_3_34_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6941.2001.tb00794.x"},{"key":"e_1_3_3_35_2","doi-asserted-by":"publisher","DOI":"10.1038\/30965"},{"key":"e_1_3_3_36_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.70.8.4831-4839.2004"},{"key":"e_1_3_3_37_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1106028"},{"key":"e_1_3_3_38_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.68.1.335-345.2002"},{"key":"e_1_3_3_39_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1998.00760.x"},{"key":"e_1_3_3_40_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.70.9.5426-5433.2004"},{"key":"e_1_3_3_41_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.68.6.3094-3101.2002"},{"key":"e_1_3_3_42_2","first-page":"711","volume-title":"Molecular Microbial Ecology Manual","author":"Pernthaler A","year":"2004","unstructured":"A Pernthaler, J Pernthaler, R Amann, Sensitive multi-color fluorescence in situ hybridization for the identification of environmental microorganisms. Molecular Microbial Ecology Manual, eds GA Kowalchuk, FJ de Bruijn, IM Head, ADL Akkermans, JD van Elsas (Kluwer Academic Publishers, Dordrecht\/Boston\/London), pp. 711\u2013726 (2004)."}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.0809329105","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,4,12]],"date-time":"2022-04-12T17:55:56Z","timestamp":1649786156000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/full\/10.1073\/pnas.0809329105"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2008,11,18]]},"references-count":42,"journal-issue":{"issue":"46","published-print":{"date-parts":[[2008,11,18]]}},"alternative-id":["10.1073\/pnas.0809329105"],"URL":"https:\/\/doi.org\/10.1073\/pnas.0809329105","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.1127161.598975","asserted-by":"object"},{"id-type":"doi","id":"10.3410\/f.1127161.584312","asserted-by":"object"},{"id-type":"doi","id":"10.3410\/f.1127161.595047","asserted-by":"object"},{"id-type":"doi","id":"10.3410\/f.1127161.584886","asserted-by":"object"},{"id-type":"doi","id":"10.3410\/f.1127161.592962","asserted-by":"object"}]},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2008,11,18]]},"assertion":[{"value":"2008-04-21","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2008-11-18","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}