{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T23:25:56Z","timestamp":1792797956853,"version":"4.5.0"},"reference-count":32,"publisher":"Wiley","issue":"2","license":[{"start":{"date-parts":[[2018,2,22]],"date-time":"2018-02-22T00:00:00Z","timestamp":1519257600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"name":"Leopoldina","award":["LPDS 2009-42"],"award-info":[{"award-number":["LPDS 2009-42"]}]},{"name":"Marie-Curie-Intra-European fellowship","award":["FP7-MC-IEF; 271929"],"award-info":[{"award-number":["FP7-MC-IEF; 271929"]}]},{"name":"ETH Zurich Center","id":[{"id":"https:\/\/ror.org\/05a28rw58","id-type":"ROR","asserted-by":"crossref"}]}],"content-domain":{"domain":["enviromicro-journals.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Environ Microbiol Rep"],"published-print":{"date-parts":[[2018,4]]},"abstract":"<jats:title>Summary<\/jats:title>\n                  <jats:p>\n                    Populations of genetically identical cells can display marked variation in phenotypic traits; such variation is termed phenotypic heterogeneity. Here, we investigate the effect of substrate and electron donor limitation on phenotypic heterogeneity in N\n                    <jats:sub>2<\/jats:sub>\n                    and CO\n                    <jats:sub>2<\/jats:sub>\n                    fixation in the green sulphur bacterium\n                    <jats:italic>Chlorobium phaeobacteroides<\/jats:italic>\n                    . We grew populations in chemostats and batch cultures and used stable isotope labelling combined with nanometer\u2010scale secondary ion mass spectrometry (NanoSIMS) to quantify phenotypic heterogeneity. Experiments in H\n                    <jats:sub>2<\/jats:sub>\n                    S (i.e. electron donor) limited chemostats show that varying levels of\n                    <jats:inline-graphic xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" xlink:href=\"graphic\/emi412616-math-0001.png\" xlink:title=\"urn:x-wiley:17582229:media:emi412616:emi412616-math-0001\"\/>\n                    limitation induce heterogeneity in N\n                    <jats:sub>2<\/jats:sub>\n                    fixation. Comparison of phenotypic heterogeneity between chemostats and batch (unlimited for H\n                    <jats:sub>2<\/jats:sub>\n                    S) populations indicates that electron donor limitation drives heterogeneity in N\n                    <jats:sub>2<\/jats:sub>\n                    and CO\n                    <jats:sub>2<\/jats:sub>\n                    fixation. Our results demonstrate that phenotypic heterogeneity in a certain metabolic activity can be driven by different modes of limitation and that heterogeneity can emerge in different metabolic processes upon the same mode of limitation. In conclusion, our data suggest that limitation is a general driver of phenotypic heterogeneity in microbial populations.\n                  <\/jats:p>","DOI":"10.1111\/1758-2229.12616","type":"journal-article","created":{"date-parts":[[2018,2,2]],"date-time":"2018-02-02T06:02:44Z","timestamp":1517551364000},"page":"179-183","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Substrate and electron donor limitation induce phenotypic heterogeneity in different metabolic activities in a green sulphur bacterium"],"prefix":"10.1111","volume":"10","author":[{"given":"M.","family":"Zimmermann","sequence":"first","affiliation":[{"name":"Department of Environmental Systems Science ETH Zurich \u2013 Swiss Federal Institute of Technology Zurich Switzerland"},{"name":"Department of Environmental Microbiology Eawag \u2013 Swiss Federal Institute of Aquatic Science and Technology D\u00fcbendorf Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S.","family":"Escrig","sequence":"additional","affiliation":[{"name":"Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering (ENAC) \u00c9cole Polytechnique F\u00e9d\u00e9rale de Lausanne (EPFL) Lausanne Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"G.","family":"Lavik","sequence":"additional","affiliation":[{"name":"Department of Biogeochemistry Max Planck Institute for Marine Microbiology Bremen Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M. 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M.","family":"Kuypers","sequence":"additional","affiliation":[{"name":"Department of Biogeochemistry Max Planck Institute for Marine Microbiology Bremen Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A.","family":"Meibom","sequence":"additional","affiliation":[{"name":"Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering (ENAC) \u00c9cole Polytechnique F\u00e9d\u00e9rale de Lausanne (EPFL) Lausanne Switzerland"},{"name":"Center for Advanced Surface Analysis Institute of Earth Sciences, University of Lausanne Lausanne Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M.","family":"Ackermann","sequence":"additional","affiliation":[{"name":"Department of Environmental Systems Science ETH Zurich \u2013 Swiss Federal Institute of Technology Zurich Switzerland"},{"name":"Department of Environmental Microbiology Eawag \u2013 Swiss Federal Institute of Aquatic Science and Technology D\u00fcbendorf Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"F.","family":"Schreiber","sequence":"additional","affiliation":[{"name":"Department of Environmental Systems Science ETH Zurich \u2013 Swiss Federal Institute of Technology Zurich Switzerland"},{"name":"Department of Environmental Microbiology Eawag \u2013 Swiss Federal Institute of Aquatic Science and Technology D\u00fcbendorf Switzerland"},{"name":"Division Biodeterioration and Reference Organisms, Department of Materials and Environment Federal Institute for Materials Research and Testing (BAM) Berlin Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2018,2,22]]},"reference":[{"key":"e_1_2_4_2_1","doi-asserted-by":"publisher","DOI":"10.1038\/ng.110"},{"key":"e_1_2_4_3_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro3491"},{"key":"e_1_2_4_4_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature07067"},{"key":"e_1_2_4_5_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1001928"},{"key":"e_1_2_4_6_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1099390"},{"key":"e_1_2_4_7_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature08504"},{"key":"e_1_2_4_8_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0705463105"},{"key":"e_1_2_4_9_1","doi-asserted-by":"publisher","DOI":"10.1038\/ismej.2015.193"},{"key":"e_1_2_4_10_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1462-2920.2009.01917.x"},{"key":"e_1_2_4_11_1","doi-asserted-by":"publisher","DOI":"10.15252\/msb.20167033"},{"key":"e_1_2_4_12_1","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.12243"},{"key":"e_1_2_4_13_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature13582"},{"key":"e_1_2_4_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2009.12.001"},{"key":"e_1_2_4_15_1","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.12752"},{"key":"e_1_2_4_16_1","doi-asserted-by":"crossref","unstructured":"Kopf S.H. 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