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ChicherData-dependent acquisitionMass SpectrometryBottom-up proteomicsnutritional immunitymetal homeostasiszincregulatory rnasStaphylococcus aureusStaphylococcus aureus; metal homeostasis; zinc; regulatory rnas; nutritional immunityhttps://www.ebi.ac.uk/pride/archive/projects/PXD065909WT, Δzur, ΔzinS and Δzur ΔzinS cells grown in NRPMI medium supplemented with 1 mM MgCl2, 100 μM CaCl2, 25 μM MnCl2, 1 μM FeSO4, ± 25 μM ZnCl2 were harvested at OD600nm ≈ 1. Cell pellets were washed 5 times with cold DPBS, resuspended in 200 μL lysis buffer (7 M urea, 2 M thiourea, 4% CHAPS, and 20 mM Tris-HCl pH 7.6, 67 U of Pierce Universal Nuclease (ThermoFisher Scientific) and 1 mM CaCl2), and lysed using Fastprep homogenizer. The Bradford assay was used to determine protein concentrations. For mass spectrometry analysis, 10 μg of purified proteins were precipitated with 0.1 M ammonium acetate in 100% methanol (5 volumes, -20°C). Proteins were reduced (5 mM Dithiothreitol, 95°C, 10 min), alkylated (10 mM Iodoacetamide, room temperature, 20 min) and digested overnight with 1:50 (v/v) of sequencing-grade trypsin (Promega). Peptide mixtures were analyzed by nanoLC-MS/MS on a reversed phase nanoElute 2 coupled to a TIMS-TOF Pro 2 mass spectrometer (Bruker Daltonik Gmbh) using a data-dependent acquisition (DDA). Peptides were separated on the integrated emitter column IonOpticks Aurora Elite (25 cm × 75 μM, 1.7 μm particle size and 120 Å pore size; AUR3–15075C18-CSI) with a 70 min gradient.PrideProteins were identified via comparison to a homemade S. aureus protein database (2623 sequences), analyzed using Mascot algorithm (version 2.8, Matrix Science) with a decoy strategy. Mass error was set to 20 ppm for precursor ions and 30 ppm for fragment ions. Oxidation (M), carbamidomethylation (C), acethylation (protein Nter) and phosphorylation (S, T and Y) were considered as variable modifications. Data were then imported into Proline v2.0 software (3), proteins were validated on Mascot pretty rank equal to 1, a Mascot score threshold set at 25 and 1% FDR on both peptide spectrum matches (PSM score) and protein sets (Protein Set score) and MS1 eXtracted Ion Chromatograms (XIC) were used to quantify each protein. An exhaustive map alignment followed by a median ratio normalisation of the intensities was computed on Proline. A 50s cross assignment was carried out within groups only. Prostar was used for the statistical analyses of the intensities. Partially observed values (POV) and values missing in the entire condition (MEC) were imputed with det quantile 1%. A LIMMA statistical test with a log (FC) threshold of 1 and a Benjamini-Hochberg correction were used to generate log2(FC) and adjusted p-values.ProteomicsDavid LalaounaCOMPLETEUniversité de Strasbourg, CNRS, Architecture et Réactivité de l’ARN, UPR9002, F-67000 Strasbourg, FranceStaphylococcus Aureus42755362 Charbonnier M, Racine H, Probst-Lotze S, Radin JN, Rios-Delgado G, Lyu L, Laster HM, Kohl MP, Mazgaj R, Blum M, Marchand V, Chicher J, Romby P, Marzi S, Caldelari I, Tree JJ, Waldron KJ, Boyd JM, Dutheil JY, Kehl-Fie TE, Lalaouna D. A Zur-dependent regulatory RNA involved in maintaining zinc homeostasis in Staphylococcus aureus. Nucleic Acids Res. 2026 54(17):gkag894 10.1093/nar/gkag894j.chicher@ibmc-cnrs.unistra.frUniversité de Strasbourg, Plateforme Protéomique Strasbourg-Esplanade, Centre National de la Recherche ScientifiqueFrance10.6019/PXD065909Small regulatory RNAs (sRNAs) are key drivers of bacterial adaptation to environmental fluctuations, including iron and manganese restriction imposed by the host. This study explored the repertoire of sRNAs produced by the human pathogen Staphylococcus aureus in response to metal limitation. Two sRNAs were identified, S1077 and ZinS, that were regulated by zinc (Zn) availability. Further investigations revealed that, similar to the cnt operon from which it derives, S1077 synthesis is controlled by the transcription factors Zur and Fur. In contrast, zinS transcription is solely repressed by Zur. RNA affinity purification identified several ZinS-associated mRNAs encoding Zn-dependent enzymes, including the alcohol dehydrogenase Adh, whose synthesis is negatively regulated by ZinS. Loss of ZinS does not alter staphylococcal metal accumulation, suggesting a role in a Zn-sparing response. Remarkably, zinS also encodes a small peptide, ZinP. Genomic analysis shows that the regulatory portion of zinS emerged from the 3' untranslated region of zinP and is conserved in S. aureus and closely related species, whereas zinP is also found in phylogenetically distant organisms. Our findings demonstrate that sRNAs facilitate bacterial adaptation to Zn limitation, and that genetic exchange and subsequent neofunctionalization have enabled S. aureus to adapt to metal-restricted environments.A Zur-dependent regulatory RNA involved in maintaining zinc homeostasis in Staphylococcus aureus.Charbonnier Mathilde M, Racine Hugo H, Probst-Lotze Samuel S, Radin Jana N JN, Rios-Delgado Gustavo G, Lyu Liangyu L, Laster Hannah M HM, Kohl Maximilian P MP, Mazgaj Rafał R, Blum Marion M, Marchand Virginie V, Chicher Johana J, Romby Pascale P, Marzi Stefano S, Caldelari Isabelle I, Tree Jai J JJ, Waldron Kevin J KJ, Boyd Jeffrey M JM, Dutheil Julien Y JY, Kehl-Fie Thomas E TE, Lalaouna David DfalseA Zur-dependent regulatory RNA involved in maintaining zinc homeostasis in Staphylococcus aureusSmall regulatory RNAs (sRNAs) serve as key drivers of bacterial adaptation to environmental fluctuations. They critically control the adaptive response of Staphylococcus aureus and other pathogens to iron and manganese restriction imposed by the host. However, it is unknown if bacterial sRNAs enable adaptation to other metal-limited environments This study examined the repertoire of sRNAs produced by S. aureus in response to metal limitation. This led to the identification of two sRNAs, S1077 and ZinS (RsaX20), which are regulated by zinc (Zn) availability. Further investigations revealed that, similar to the cnt operon from which it derives, S1077 synthesis is controlled by the transcription factors Zur and Fur. In contrast, zinS transcription is solely repressed by Zur. Amongst the ZinS targets are several Zn-dependent enzymes, such as the alcohol dehydrogenase Adh, whose synthesis is negatively regulated by ZinS. Loss of ZinS does not alter staphylococcal metal accumulation, suggesting that this sRNA controls a Zn-sparing response. Remarkably, zinS also encodes a small peptide, ZinP, which is produced in response to Zn limitation. Genomic analysis suggests that the regulatory portion of ZinS emerged from the 3’ untranslated region of ZinP in S. aureus and closely related species after horizontal transfer from phylogenetically distant organisms. All our findings demonstrate that sRNAs facilitate bacterial adaptation to Zn limitation, and that genetic exchange and subsequent neofunctionalization have enabled S. aureus to adapt to metal- restricted environments.2026-09-282025-07-08PXD065909NEWT:6945NEWT:3555NEWT:241368NEWT:2NEWT:157546NEWT:190802NEWT:35554NEWT:9778NEWT:150475NEWT:9417NEWT:7111NEWT:347515NEWT:1216979NEWT:307972NEWT:32046NEWT:544496NEWT:5180NEWT:256737NEWT:2042546NEWT:115104NEWT:1081927NEWT:1238993NEWT:67825NEWT:185579NEWT:43179NEWT:13076NEWT:1249668NEWT:376741NEWT:317NEWT:55153NCBITaxon:10407NEWT:1736309NEWT:7227NEWT:7469NEWT:885318NEWT:1211601NEWT:415540NEWT:4081NEWT:876138NEWT:554NEWT:98334NEWT:426428NEWT:557436NEWT:237561NEWT:6928NEWT:10036NEWT:7574NEWT:1351NEWT:7215NEWT:575412NEWT:29204NEWT:272563NEWT:79220NEWT:507601NCBITaxon:79857NCBITaxon:6157NEWT:95648NEWT:3885NEWT:746360NEWT:6239NEWT:3888NEWT:1589NEWT:470150NEWT:135622NEWT:216257NEWT:6915NEWT:9986NEWT:101510NEWT:4054NEWT:3880NEWT:272559NEWT:226186NEWT:3641NEWT:383379NEWT:8782NEWT:1263854NEWT:1000589NEWT:435590NEWT:1902NEWT:85962NEWT:160488NEWT:28104NEWT:317447NEWT:7955NCBITaxon:2NEWT:985076NEWT:7959NEWT:2261NEWT:623NEWT:4565NEWT:1264690NEWT:515619NEWT:6192NEWT:28532NCBITaxon:38727NEWT:34305NEWT:59729NCBITaxon:183674NEWT:224308NEWT:626528NEWT:216599NEWT:139927NEWT:4558NEWT:209285NEWT:211586NEWT:216595NEWT:243230NEWT:8355NEWT:1283NEWT:931281NEWT:4550NEWT:1000561NEWT:9685NEWT:7029NEWT:1283300NEWT:6183NEWT:6063NEWT:334747NEWT:61235NCBITaxon:79824NEWT:4787NCBITaxon:4563NEWT:5755NEWT:3218NEWT:5759NEWT:1736231NEWT:436486NEWT:6287NEWT:2242NEWT:300641NEWT:4784NEWT:727NEWT:9796NEWT:11320NEWT:725NEWT:360106NEWT:260707NEWT:287NEWT:10117NEWT:10239NCBITaxon:6191NEWT:10116NEWT:1280NEWT:1836NEWT:1735272NEWT:83334NEWT:185431NEWT:83332NEWT:29760NEWT:260704NEWT:703612NEWT:260705NEWT:80863NEWT:44685NEWT:2697049NEWT:1148NEWT:11676NEWT:55571NEWT:100226NCBITaxon:6073NEWT:4530NEWT:4896NEWT:6279NEWT:1123869NEWT:7370NEWT:75058NEWT:83906NEWT:607699NEWT:6282NEWT:426688NEWT:1094343NEWT:208964NEWT:1134506NEWT:575584NEWT:296543NEWT:1773NEWT:38783NEWT:8727NEWT:1895NEWT:4006NEWT:1182590NEWT:8726NEWT:6669NEWT:10090NEWT:935293NEWT:64152NEWT:749200NEWT:4120NEWT:51515NEWT:5693NEWT:8724NEWT:51511NEWT:92867NEWT:8723NEWT:990346NEWT:5334NEWT:145953NEWT:257309NEWT:100816NEWT:230741NEWT:284812NCBITaxon:10359NCBITaxon:1313NEWT:43330NEWT:242619NEWT:44544NEWT:632957NEWT:373995NEWT:5689NEWT:645463NEWT:544404NEWT:3702NEWT:129249NEWT:9925NEWT:8839NEWT:4232NEWT:990119NEWT:2758385NEWT:4113NEWT:837NEWT:11298NEWT:171101NEWT:714NEWT:421932NEWT:196627NEWT:408172NEWT:5691NEWT:408170NEWT:493760NEWT:260710NEWT:627025NEWT:400772NEWT:1097677NEWT:3708NEWT:128161NEWT:242507NEWT:106592NEWT:536231NEWT:61674NEWT:1117957NEWT:9913NEWT:1432138NEWT:10312NEWT:1424507NEWT:4100NEWT:1076NEWT:6763NEWT:3498NEWT:803NEWT:8030NEWT:29722NEWT:380394NEWT:1692259NEWT:1639NEWT:188229NEWT:3818NEWT:480NEWT:4909NEWT:180066NEWT:67767NEWT:46835NEWT:135588NEWT:376686NEWT:1843183NEWT:95486NEWT:58002NEWT:9103NEWT:4577NEWT:1416333NEWT:5664NEWT:2157NEWT:749906NEWT:146479NEWT:10306NCBITaxon:2759NEWT:1911079NEWT:8022NEWT:145943NCBITaxon:4932NEWT:595536NCBITaxon:620NEWT:3635NEWT:5811NEWT:235443NEWT:1480154NEWT:1274414NEWT:27606NEWT:59202NEWT:9975NEWT:3197NEWT:9615NEWT:10299NEWT:2719099NEWT:860688NEWT:411483NEWT:884019NEWT:198215NEWT:411490NEWT:169963NEWT:36329NEWT:1147787NCBITaxon:3044782NEWT:72407NEWT:476272NEWT:349741NEWT:9606NEWT:367830NEWT:157295NEWT:641501NEWT:178616NEWT:410289NEWT:373153NEWT:915099NEWT:74940NEWT:9721NEWT:1450511NEWT:360094NEWT:470NEWT:411901NEWT:1313NEWT:411469NEWT:84023NEWT:9838NEWT:105884NCBITaxon:9615NCBITaxon:5811NEWT:58334NEWT:411464NEWT:1193501NEWT:3055NEWT:6326NEWT:6689NEWT:411460NEWT:2762NEWT:5476NEWT:1174673NEWT:562NEWT:411470NEWT:33952NEWT:2094720NEWT:1274432NEWT:1274426NEWT:1423NEWT:4932NEWT:70448NEWT:9825NEWT:1274423NEWT:3603NEWT:698936NEWT:2759NEWT:3847NEWT:39946NEWT:9823NEWT:178876NEWT:9940NEWT:327160NEWT:573NEWT:521001NEWT:9031NEWT:1274420NEWT:7091NEWT:578458427553620000-0002-4403-7484