{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,25]],"date-time":"2026-08-25T14:25:34Z","timestamp":1787667934059,"version":"build-2736575974"},"reference-count":79,"publisher":"American Society for Microbiology","license":[{"start":{"date-parts":[[2023,7,27]],"date-time":"2023-07-27T00:00:00Z","timestamp":1690416000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2023,7,27]],"date-time":"2023-07-27T00:00:00Z","timestamp":1690416000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"funder":[{"DOI":"10.13039\/100000060","name":"HHS | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"crossref","award":["AI118807"],"award-info":[{"award-number":["AI118807"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000060","name":"HHS | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"crossref","award":["AI166263"],"award-info":[{"award-number":["AI166263"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000060","name":"HHS | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"crossref","award":["AI171537"],"award-info":[{"award-number":["AI171537"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000928","name":"Welch Foundation","doi-asserted-by":"crossref","award":["I-1969-20180324"],"award-info":[{"award-number":["I-1969-20180324"]}],"id":[{"id":"10.13039\/100000928","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000861","name":"Burroughs Wellcome Fund","doi-asserted-by":"crossref","award":["1017880"],"award-info":[{"award-number":["1017880"]}],"id":[{"id":"10.13039\/100000861","id-type":"DOI","asserted-by":"crossref"}]},{"name":"United States - Israel Binational Science Foundation","award":["2021025"],"award-info":[{"award-number":["2021025"]}]},{"name":"National Science Foundation","award":["1000194723"],"award-info":[{"award-number":["1000194723"]}]},{"DOI":"10.13039\/100000060","name":"HHS | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"crossref","award":["AI007520"],"award-info":[{"award-number":["AI007520"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000060","name":"HHS | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"crossref","award":["AI075093"],"award-info":[{"award-number":["AI075093"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["mBio"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    <jats:italic>Salmonella enterica<\/jats:italic>\n                    serovar Typhimurium induces intestinal inflammation to create a niche that fosters the outgrowth of the pathogen over the gut microbiota. Under inflammatory conditions,\n                    <jats:italic>Salmonella<\/jats:italic>\n                    utilizes terminal electron acceptors generated as byproducts of intestinal inflammation to generate cellular energy through respiration. However, the electron donating reactions in these electron transport chains are poorly understood. Here, we investigated how formate utilization through the respiratory formate dehydrogenase-N (FdnGHI) and formate dehydrogenase-O (FdoGHI) contribute to gut colonization of\n                    <jats:italic>Salmonella<\/jats:italic>\n                    . Both enzymes fulfilled redundant roles in enhancing fitness in a mouse model of\n                    <jats:italic>Salmonella<\/jats:italic>\n                    -induced colitis, and coupled to tetrathionate, nitrate, and oxygen respiration. The formic acid utilized by\n                    <jats:italic>Salmonella<\/jats:italic>\n                    during infection was generated by its own pyruvate-formate lyase as well as the gut microbiota. Transcription of formate dehydrogenases and pyruvate-formate lyase was significantly higher in bacteria residing in the mucus layer compared to the lumen. Furthermore, formate utilization conferred a more pronounced fitness advantage in the mucus, indicating that formate production and degradation occurred predominantly in the mucus layer. Our results provide new insights into how\n                    <jats:italic>Salmonella<\/jats:italic>\n                    adapts its energy metabolism to the local microenvironment in the gut.\n                  <\/jats:p>\n                  <jats:sec>\n                    <jats:title>IMPORTANCE<\/jats:title>\n                    <jats:p>\n                      Bacterial pathogens must not only evade immune responses but also adapt their metabolism to successfully colonize their host. The microenvironments encountered by enteric pathogens differ based on anatomical location, such as small versus large intestine, spatial stratification by host factors, such as mucus layer and antimicrobial peptides, and distinct commensal microbial communities that inhabit these microenvironments. Our understanding of how\n                      <jats:italic>Salmonella<\/jats:italic>\n                      populations adapt its metabolism to different environments in the gut is incomplete. In the current study, we discovered that\n                      <jats:italic>Salmonella<\/jats:italic>\n                      utilizes formate as an electron donor to support respiration, and that formate oxidation predominantly occurs in the mucus layer. Our experiments suggest that spatially distinct\n                      <jats:italic>Salmonella<\/jats:italic>\n                      populations in the mucus layer and the lumen differ in their energy metabolism. Our findings enhance our understanding of the spatial nature of microbial metabolism and may have implications for other enteric pathogens as well as commensal host-associated microbial communities.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1128\/mbio.00921-23","type":"journal-article","created":{"date-parts":[[2023,7,27]],"date-time":"2023-07-27T09:00:30Z","timestamp":1690448430000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":14,"title":["Formate oxidation in the intestinal mucus layer enhances fitness of\n                    <i>Salmonella enterica<\/i>\n                    serovar Typhimurium"],"prefix":"10.1128","author":[{"given":"Maria G.","family":"Winter","sequence":"first","affiliation":[{"name":"Department of Internal Medicine, Division of Infectious Diseases, UC Davis School of Medicine , Davis, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth R.","family":"Hughes","sequence":"additional","affiliation":[{"name":"Department of Microbiology, UT Southwestern Medical Center , Dallas, Texas, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew K.","family":"Muramatsu","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, Division of Infectious Diseases, UC Davis School of Medicine , Davis, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angel G.","family":"Jimenez","sequence":"additional","affiliation":[{"name":"Department of Microbiology, UT Southwestern Medical Center , Dallas, Texas, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rachael B.","family":"Chanin","sequence":"additional","affiliation":[{"name":"Department of Microbiology, UT Southwestern Medical Center , Dallas, Texas, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luisella","family":"Spiga","sequence":"additional","affiliation":[{"name":"Department of Microbiology, UT Southwestern Medical Center , Dallas, Texas, USA"},{"name":"Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center , Nashville, Tennessee, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caroline C.","family":"Gillis","sequence":"additional","affiliation":[{"name":"Department of Microbiology, UT Southwestern Medical Center , Dallas, Texas, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"McClelland","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Molecular Genetics, UC Irvine , Irvine, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1818-1335","authenticated-orcid":true,"given":"Helene","family":"Andrews-Polymenis","sequence":"additional","affiliation":[{"name":"Department of Microbial Pathogenesis and Immunology, Texas A&amp;M College of Medicine , College Station, Texas, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1532-9178","authenticated-orcid":true,"given":"Sebastian E.","family":"Winter","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, Division of Infectious Diseases, UC Davis School of Medicine , Davis, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","published-online":{"date-parts":[[2023,7,27]]},"reference":[{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41579-022-00833-7"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-immunol-101819-024945"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.01526-14"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro3050"},{"key":"e_1_3_3_6_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0053957"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2018.07.002"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1084\/jem.20181639"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.15252\/embr.201642282"},{"key":"e_1_3_3_10_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2015.03.005"},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.aam9949"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1218831"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature01520"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1128\/MMBR.00027-19"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1608858113"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.13077"},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.0050244"},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.01432-07"},{"key":"e_1_3_3_19_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature09415"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.00143-12"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2016.03.004"},{"key":"e_1_3_3_22_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2017.07.018"},{"key":"e_1_3_3_23_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1004209"},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1107857108"},{"key":"e_1_3_3_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2017.11.006"},{"key":"e_1_3_3_26_2","doi-asserted-by":"publisher","DOI":"10.1186\/s40168-022-01389-7"},{"key":"e_1_3_3_27_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.00773-18"},{"key":"e_1_3_3_28_2","doi-asserted-by":"publisher","DOI":"10.1128\/ecosal.3.2.5"},{"key":"e_1_3_3_29_2","doi-asserted-by":"publisher","DOI":"10.1128\/ecosalplus.ESP-0011-2016"},{"key":"e_1_3_3_30_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1068186"},{"key":"e_1_3_3_31_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00267258"},{"key":"e_1_3_3_32_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00268147"},{"key":"e_1_3_3_33_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.170.1.213-217.1988"},{"key":"e_1_3_3_34_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.149.2.554-560.1982"},{"key":"e_1_3_3_35_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.01570-08"},{"key":"e_1_3_3_36_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.71.5.2839-2858.2003"},{"key":"e_1_3_3_37_2","doi-asserted-by":"publisher","DOI":"10.1097\/00000478-197912000-00001"},{"key":"e_1_3_3_38_2","doi-asserted-by":"publisher","DOI":"10.7326\/0003-4819-76-5-697"},{"key":"e_1_3_3_39_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2017.01.005"},{"key":"e_1_3_3_40_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.00319-08"},{"key":"e_1_3_3_41_2","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.174.3.1675"},{"key":"e_1_3_3_42_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0602187103"},{"key":"e_1_3_3_43_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature07067"},{"key":"e_1_3_3_44_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tim.2018.11.007"},{"key":"e_1_3_3_45_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1008540"},{"key":"e_1_3_3_46_2","doi-asserted-by":"publisher","DOI":"10.4161\/gmic.27129"},{"key":"e_1_3_3_47_2","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.01832-19"},{"key":"e_1_3_3_48_2","doi-asserted-by":"publisher","DOI":"10.1016\/s0014-5793(03)00389-2"},{"key":"e_1_3_3_49_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1006129"},{"key":"e_1_3_3_50_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.01525-15"},{"key":"e_1_3_3_51_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.83.13.4650"},{"key":"e_1_3_3_52_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(18)54583-X"},{"key":"e_1_3_3_53_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.173.16.4983-4993.1991"},{"key":"e_1_3_3_54_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.00205-08"},{"key":"e_1_3_3_55_2","doi-asserted-by":"publisher","DOI":"10.1128\/mbio.00012-23"},{"key":"e_1_3_3_56_2","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.01777-18"},{"key":"e_1_3_3_57_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1007847"},{"key":"e_1_3_3_58_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2022.04.012"},{"key":"e_1_3_3_59_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-021-03785-9"},{"key":"e_1_3_3_60_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.aag3042"},{"key":"e_1_3_3_61_2","doi-asserted-by":"publisher","DOI":"10.3389\/fvets.2020.00563"},{"key":"e_1_3_3_62_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.psj.2019.12.037"},{"key":"e_1_3_3_63_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.00484-07"},{"key":"e_1_3_3_64_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.05395-11"},{"key":"e_1_3_3_65_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2018.12.003"},{"key":"e_1_3_3_66_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41564-019-0407-8"},{"key":"e_1_3_3_67_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature20557"},{"key":"e_1_3_3_68_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.65.4.1610-1618.1999"},{"key":"e_1_3_3_69_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.str.2008.03.017"},{"key":"e_1_3_3_70_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.187.21.7167-7175.2005"},{"key":"e_1_3_3_71_2","doi-asserted-by":"publisher","DOI":"10.1038\/nbt1183-784"},{"key":"e_1_3_3_72_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.177.5.1357-1366.1995"},{"key":"e_1_3_3_73_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0099820"},{"key":"e_1_3_3_74_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.71.2.629-640.2003"},{"key":"e_1_3_3_75_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.2009.06859.x"},{"key":"e_1_3_3_76_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.170.6.2575-2583.1988"},{"key":"e_1_3_3_77_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00270447"},{"key":"e_1_3_3_78_2","first-page":"234","article-title":"Curing bacterial cells of lysogenic viruses by using UCB indicator plates","volume":"2","author":"Bochner BR","year":"1984","unstructured":"Bochner BR . 1984. Curing bacterial cells of lysogenic viruses by using UCB indicator plates. BioTechniques 2:234\u2013240. doi:https:\/\/eurekamag.com\/research\/005\/075\/005075130.php","journal-title":"BioTechniques"},{"key":"e_1_3_3_79_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(18)65874-0"},{"key":"e_1_3_3_80_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.96.1.215-220.1968"}],"container-title":["mBio"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mbio.00921-23","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mbio.00921-23","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,27]],"date-time":"2023-07-27T09:00:37Z","timestamp":1690448437000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/mbio.00921-23"}},"subtitle":[],"editor":[{"given":"Nina R.","family":"Salama","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]},{"given":"John S.","family":"Gunn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,7,27]]},"references-count":79,"alternative-id":["10.1128\/mbio.00921-23"],"URL":"https:\/\/doi.org\/10.1128\/mbio.00921-23","relation":{},"ISSN":["2150-7511"],"issn-type":[{"value":"2150-7511","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,27]]},"assertion":[{"value":"2023-04-14","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-06-12","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-07-27","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e00921-23"}}