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Research Article

Genome-wide Annotation, Identification, and Global Transcriptomic Analysis of Regulatory or Small RNA Gene Expression in Staphylococcus aureus

Ronan K. Carroll, Andy Weiss, William H. Broach, Richard E. Wiemels, Austin B. Mogen, Kelly C. Rice, Lindsey N. Shaw
Paul Dunman, Invited Editor, Gerald B. Pier, Editor
Ronan K. Carroll
aDepartment of Biological Sciences, Ohio University, Athens, Ohio, USA
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Andy Weiss
bDepartment of Cell Biology, Microbiology and Molecular Biology, University of South Florida, Tampa, Florida, USA
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William H. Broach
bDepartment of Cell Biology, Microbiology and Molecular Biology, University of South Florida, Tampa, Florida, USA
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Richard E. Wiemels
aDepartment of Biological Sciences, Ohio University, Athens, Ohio, USA
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Austin B. Mogen
cDepartment of Microbiology and Cell Science, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, Florida, USA
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Kelly C. Rice
cDepartment of Microbiology and Cell Science, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, Florida, USA
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Lindsey N. Shaw
bDepartment of Cell Biology, Microbiology and Molecular Biology, University of South Florida, Tampa, Florida, USA
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Paul Dunman
University of Rochester
Roles: Invited Editor
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Gerald B. Pier
Harvard Medical School
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DOI: 10.1128/mBio.01990-15
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  • FIG 1 
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    FIG 1 

    Northern blot analysis of tsr transcripts. Northern blotting was performed using oligonucleotide probes specific for the tsr transcripts (tsr8, tsr25, tsr26, tsr31, and tsr33). RNA-seq read alignments for each corresponding chromosomal location are shown, as are CDS genes (black arrows), and sRNAs (red arrows). The depth of read coverage on the genome is shown by the blue histograms.

  • FIG 2 
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    FIG 2 

    Variation in genome annotation of the tsr12 locus. RNA-seq read alignment data are shown for strains USA300 (A), MRSA252 (B), and NCTC 8325 (C). Annotations for CDS genes are shown by black arrows, and the depth of coverage is shown by the blue histograms. The location of tsr12 is shown by a red arrow. (A) There is no CDS annotation at the tsr12 locus in strain USA300. (B) In strain MRSA252, a gene (SAR0432) is annotated in the forward direction at the tsr12 locus. (C) In strain NCTC 8325, a gene (SAOUHSC_00396) is annotated in the reverse direction at the tsr12 locus.

  • FIG 3 
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    FIG 3 

    Analysis of the Teg23 locus. (A) Teg23 locus in S. aureus strains N315, USA300, NCTC 8325, and MRSA252. Annotated CDS genes are shown in gray. The previously reported location of Teg23 is shown in white. (B) Northern blot analysis of Teg23. The Teg23 transcript was detected by Northern blot analysis with a strand-specific oligonucleotide probe. Two bands were detected and were designated Teg23.1 (approximately 215 nt) and Teg23.2 (approximately 310 nt). (C) Alignment of Teg23 DNA sequence in strains USA300, NCTC 8325, and MRSA252. Sequence corresponding to the SAOUHSC_02572 and SAR2384 CDS genes is highlighted in red and blue, respectively. Sequence potentially encoding an 80-amino-acid protein (Teg23P) in strain USA300 is highlighted in green. (D) Western blot to detect histidine-tagged Teg23P. No Teg23P protein was detected in S. aureus expressing the Teg23P-his plasmid (lane 1) or in a wild-type S. aureus strain without the plasmid (lane 2). Histidine-tagged RpoE was detected as a positive control (lane 3). (E) Quantitative RT-PCR analysis of Teg23 expression. Expression of Teg23 was analyzed in the wild-type S. aureus strain with or without the Teg23P-his plasmid. Approximately 3-fold-higher expression of Teg23 was detected in the strain expressing the Teg23P-his plasmid. Statistical significance was determined using Student's t-test. *, P < 0.05. (F) RNA-seq read alignment at the Teg23 locus in strain NCTC 8325. RNA-seq reads aligned to the NCTC 8325 genome are shown in blue. The locations of annotated genes are shown in gray. The locations of primers used for RT-PCR are shown in red. The predicted size and location of the Teg23.1 and Teg23.2 transcripts are shown by red arrows. (G) RT-PCR analysis of Teg23 transcript. PCR was performed using the primer pairs indicated and S. aureus genomic DNA (gDNA) (lane 1), cDNA from S. aureus containing the Teg23P-his plasmid (lane 2), cDNA from wild-type S. aureus (lane 3), or no DNA (lane 4). No PCR product was detected using primers 1 and 3 with S. aureus cDNA as the template.

  • FIG 4 
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    FIG 4 

    Location and comparative expression analysis of the 303 S. aureus USA300 sRNAs. The black outer ring shows the chromosomal locations of 303 sRNAs in strain USA300 (the outer circle shows the forward strand, while the inner circle shows the reverse strand). The inner rings show sRNA gene expression profile in TSB (outside, blue), human serum (inside, red), and heat map (middle) showing differences in expression. The heights of the blue or red bars are proportional to the expression values (the maximum displayed expression value was 1,000).

  • FIG 5 
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    FIG 5 

    Northern blot analysis of serum-regulated sRNAs in strain USA300. (A) Analysis of sRNAs demonstrating upregulation in human serum. RNA-seq read alignment data and Northern blot analysis are shown for SAUSA300s289 (tsr25) and SAUSA300s046 (rsaOG) during growth in TSB (T) or human serum (S). (B) Analysis of RNAIII expression in human serum and TSB. RNA-seq read alignment data are shown for the entire agr locus. Northern blot analysis was performed using an oligonucleotide probe specific for the RNAIII transcript. Annotations for CDS genes are shown by black arrows, annotations for sRNAs are shown by red arrows, and depth of read coverage on the genome is shown by the blue histograms.

Tables

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  • TABLE 1 

    Novel sRNAs identified in strain USA300

    sRNA designationsRNA geneStrandaLocationSize (nt)Chromosomal location of tsr gene in strain:
    USA300bMRSA252bNCTC 8325b
    SAUSA300s265tsr1>52438−53094656IG−−
    SAUSA300s266tsr2<57712−5780492IG−−
    SAUSA300s267tsr3<61388−61550162IG−−
    SAUSA300s268tsr4>73511−74139628ASASAS
    SAUSA300s269tsr5<79346−7942579AS−−
    SAUSA300s270tsr6>120785−120897112IGIGIG
    SAUSA300s271tsr7>169903−170079176IG−IG
    SAUSA300s272tsr8<170013−170214201IG−IG
    SAUSA300s273tsr9<228412−228796384IGCDSCDS
    SAUSA300s274tsr10>349895−350058163IGOLOL
    SAUSA300s275tsr11<356689−35678293OLOLOL
    SAUSA300s276tsr12>457272−45733361IGOLAS
    SAUSA300s277tsr13>484942−48502583OLOLOL
    SAUSA300s278tsr14>834340−834885545IGIGAS
    SAUSA300s279tsr15>896563−897379816ASASAS
    SAUSA300s280tsr16<911246−911364118ASOLOL
    SAUSA300s281tsr17<973559−973971412IGCDSCDS
    SAUSA300s282tsr18<1074292−1074484192IGCDSCDS
    SAUSA300s283tsr19<1080302−108039492IGIGIG
    SAUSA300s284tsr20<1154300−1154753453IG−IG
    SAUSA300s285tsr21<1154827−11560011174CDSCDS3CDS3
    SAUSA300s286tsr22>1165484−1165865381IGCDSCDS
    SAUSA300s287tsr23>1256521−125654524IGIGIG
    SAUSA300s288tsr24>1429517−1429754237IG−IG
    SAUSA300s289tsr25>1442862−1443042180IGASAS
    SAUSA300s290tsr26>1641611−1641732121IGIG−
    SAUSA300s291tsr27<1642820−1642923103IGIG−
    SAUSA300s292tsr28<1715900−171597575OLOLOL
    SAUSA300s293tsr29<1954961−1955091130IG−IG
    SAUSA300s294tsr30>2126434−2126545111IG−−
    SAUSA300s295tsr31<2244964−224503571IGIGIG
    SAUSA300s296tsr32>2337922−2338072150IGIGCDS
    SAUSA300s297tsr33<2410564−241064884IGIGIG
    SAUSA300s298tsr34>2591032−259113199IGIGIG
    SAUSA300s299tsr35>2608047−2608594547IGCDSCDS
    SAUSA300s300tsr36<2608120−2608645525IGASAS
    SAUSA300s301tsr37>2620285−2620621336IGCDSCDS
    SAUSA300s302tsr38<2664856−266494589IGIGIG
    SAUSA300s303tsr39<2811278−281133052IGIGIG
    • ↵a >, forward strand; <, reverse strand.

    • ↵b Characteristics of the chromosomal location of the tsr gene. IG, located in the intergenic region; −, absent, deleted, or no homologue; AS, antisense to the annotated gene; CDS, located within an existing annotated CDS; OL, partially overlaps CDS gene; CDS3, the corresponding locus contains three annotated CDSs.

  • TABLE 2 

    42 sRNAs that are upregulated in human serum versus TSB

    sRNA designationsRNA gene name or featureTSB expression value (RPKM)bSerum expression value (RPKM)Fold change
    SAUSA300s289tsr2560.6735,374.06583.02
    SAUSA300s046rsaOG90.9934,267.77376.61
    SAUSA300s053RsaG80.853,463.0942.83
    SAUSA300s119ssr24130.783,217.8624.6
    SAUSA300s153Teg1671.051,174.0116.52
    SAUSA300s066Sau-63104.991,690.9516.11
    SAUSA300s030sprC149.582,144.3214.34
    SAUSA300s026ssrS2,991.1637,212.8112.44
    SAUSA300s005ffs929.7411,188.0012.03
    SAUSA300s148Teg23256.62,950.5911.5
    SAUSA300s050RsaD2,737.9130,473.5911.13
    SAUSA300s226JKD6008sRNA17350.05539.7910.78
    SAUSA300s013Lysine riboswitch659.936,917.8410.48
    SAUSA300s260JKD6008sRNA39616.13150.269.31
    SAUSA300s294tsr30470.644,383.009.31
    SAUSA300s027sprA11,097.349,306.358.48
    SAUSA300s233JKD6008sRNA20596.96717.537.4
    SAUSA300s003T-box riboswitch158.51,156.137.29
    SAUSA300s094Teg10819.39132.546.83
    SAUSA300s099Teg12437.1245.196.61
    SAUSA300s110sprA336.05233.316.47
    SAUSA300s282tsr18105.4653.56.2
    SAUSA300s024GlmS ribozyme185.531,064.955.74
    SAUSA300s117ssr812.1367.95.6
    SAUSA300s038sprG3191.041,049.335.49
    SAUSA300s120ssr28188.031,012.535.39
    SAUSA300s028sprA299.08504.625.09
    SAUSA300s210JKD6008sRNA071136.39691.135.07
    SAUSA300s100Teg124469.392,313.984.93
    SAUSA300s002SAMa riboswitch56.06268.44.79
    SAUSA300s031sprD804.113,810.914.74
    SAUSA300s021SAM riboswitch239.09941.213.94
    SAUSA300s075rsaOL273.51,010.423.69
    SAUSA300s091Teg6095.9350.093.65
    SAUSA300s034sprF31,227.974,261.303.47
    SAUSA300s016T-box riboswitch316.761,059.283.34
    SAUSA300s084Teg2715,788.2252,571.033.33
    SAUSA300s042rsaOC26.7588.893.32
    SAUSA300s135ssr100322.651,050.223.26
    SAUSA300s163Teg28as46.74149.533.2
    SAUSA300s079rsaOU085.01∞
    SAUSA300s151Teg1340204.13∞
    • ↵a SAM, S-adenosylmethionine.

    • ↵b RPKM, reads per kilobase of transcript per million mapped reads.

  • TABLE 3 

    41 sRNAs that are downregulated in human serum versus TSB

    sRNA designationsRNA gene name or featureTSB expression value (RPKM)aSerum expression value (RPKM)Fold change
    SAUSA300s277tsr13509.650.43−1,187.67
    SAUSA300s113sbrC1,834.126.3−291.07
    SAUSA300s266tsr2122.440.42−290.6
    SAUSA300s296tsr3292.330.44−210.63
    SAUSA300s171Sau-656941,077.46250.83−163.77
    SAUSA300s049RsaC8,079.7277.42−104.37
    SAUSA300s004Purine riboswitch2,277.9045.36−50.22
    SAUSA300s303tsr393,132.5164.48−48.58
    SAUSA300s162Teg25as6,668.30191.51−34.82
    SAUSA300s125ssr476,272.84256.03−24.5
    SAUSA300s052RsaF35,374.061,713.79−20.64
    SAUSA300s275tsr11398.9320.01−19.94
    SAUSA300s301tsr37390.3923.36−16.72
    SAUSA300s292tsr28513.0631.91−16.08
    SAUSA300s297tsr338,987.32592.2−15.18
    SAUSA300s062Sau-31141.329.7−14.57
    SAUSA300s022RNAIII66,968.705,178.15−12.93
    SAUSA300s283tsr19162.0413.93−11.63
    SAUSA300s118ssr16478.4749.19−9.73
    SAUSA300s302tsr38251.1727.55−9.12
    SAUSA300s280tsr16254.4230.88−8.24
    SAUSA300s095Teg1161,149.05155.21−7.4
    SAUSA300s211JKD6008sRNA07359.068−7.38
    SAUSA300s287tsr23970.48133.71−7.26
    SAUSA300s054RsaH4,110.36629.99−6.52
    SAUSA300s087Teg41481.0174.55−6.45
    SAUSA300s078rsaOT17,890.112,790.22−6.41
    SAUSA300s127ssr543,245.19584.15−5.56
    SAUSA300s051RsaE2,929.20534.76−5.48
    SAUSA300s074rsaOI721.93135.52−5.33
    SAUSA300s237JKD6008sRNA258100.8920.87−4.83
    SAUSA300s298tsr34200.1741.54−4.82
    SAUSA300s267tsr385.0119.21−4.43
    SAUSA300s114sbrE424.58102.21−4.15
    SAUSA300s073Sau-6072265.8264.27−4.14
    SAUSA300s276tsr12295.2973.2−4.03
    SAUSA300s291tsr27135.2234.48−3.92
    SAUSA300s204RsaX04265.5870.09−3.79
    SAUSA300s086Teg3950.3913.67−3.69
    SAUSA300s141ssr15374.6921.06−3.54
    SAUSA300s010T-box riboswitch487.82149.37−3.27
    • ↵a RPKM, reads per kilobase of transcript per million mapped reads.

  • TABLE 4 

    Bacterial strains, plasmids, and primers used in this study

    Bacterial strain, plasmid, or primerCharacteristic(s) or sequenceReference or sourceCommenta
    S. aureus strains
        USA300 HoustonCommunity-associated MRSA clinical isolate26
        SH1000Laboratory strain; rsbU functional29
        UAMS-1Osteomyelitis clinical isolate30
        RN4220Restriction-deficient transformation recipient31
        AW2192USA300 pMK4::teg23p-his6This study
    E. coli strain
        DH5αRoutine cloning strainInvitrogen
    Plasmids
        pMK4Shuttle vector; Cmr32
        pAW105pMK4::teg23P-his6This study
    Primers
        OL11845′ TCTGGACCGTGTCTCAGTTCC 3′27
        OL11855′ AGCCGACCTGAGAGGGTGA 3′27
        OL27015′ CCAAATTTAGGCATGTCAAATCGGC 3′teg23 probe
        OL32015′ GGATTCCCAATTTCTACAGACAATGCA 3′tsr8 probe
        OL32085′ ACGGGCATATAAAAGGGGAATATTTGAAAA 3′tsr25 probe
        OU01215′ GTGTTAAAAAAATAACTGGGATGTG 3′tsr26 probe
        OL32165′ CTCACAAATTCTGTAAGGGGAGCGTAT 3′tsr31 probe
        OL32175′ TTATGTCCCAATGCTGAATAAATAACTTC 3′tsr33 probe
        OL32225′ ACGCGTCGACGCGCTTGTATTCGCTGCAGG 3′teg23P F
        OL32235′ CGGGATCCTTAGTGGTGGTGGTGGTGGTGCGCCAACAAGGTTTCAAGAGC 3′teg23P-his6 R
        OL32325′ CGCCAACAAGGTTTCAAGAGC 3′teg23 OL1
        OL32815′ TAAACAACATACAGCCATTG 3′teg23 OL2
        OL32825′ GAGAATTTGAAGGCAAGTAT 3′teg23 OL3
        OL38805′ GCCAGGATAATGTAGTCTTAA 3′tsr1 F
        OL38825′ CCATTAATTTACTCAAACCG 3′tsr1 R
        OL38855′ GCTTCTGTTCGATCTC 3′tsr2 F
        OL38865′ CACGTCTTCTGATTAAAC 3′tsr2 R
        OL39165′ CATACCTCTTTAACAACAG 3′tsr18 F
        OL39175′ GGAGGAATTAATCATGTC 3′tsr18 R
        OL39355′ GAAGGGATCCAACACA 3′tsr24 F
        OL39375′ GTCTCGCCATTAATACTAC 3′tsr24 R
        OL39465′ GTCTTTTCACAACCAAAG 3′tsr29 F
        OL39485′ GGTTTTATCTTTGGAAAAAG 3′tsr29 R
        OL39565′ GATGCGGAAAATTTGG 3′tsr32 F
        OL39575′ GTGCGCAATGAATATTATG 3′tsr32 R
    • ↵a F, forward; R, reverse.

Supplemental Material

  • Figures
  • Tables
  • Additional Files
  • Figure S1

    Schematic outlining the procedure used to locate and annotate sRNAs in S. aureus. (A) Using information provided in previous studies, the approximate locations of reported sRNAs were identified. (B) RNA-seq was performed, and reads were aligned to the relevant S. aureus genome. (C) The locations of aligned reads were used to precisely locate and annotate sRNAs (blue arrow). Download Figure S1, TIF file, 2 MB.

    Copyright © 2016 Carroll et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Table S1 

    25 miscellaneous RNAs from S. aureus MRSA252 genome. Table S1, DOCX file, 0.1 MB.

    Copyright © 2016 Carroll et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Table S2 

    Names and designations for 953 previously identified and 39 newly identified sRNAs in S. aureus strains USA300, MRSA252, and NCTC 8325. Table S2, XLSX file, 0.1 MB.

    Copyright © 2016 Carroll et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Text S1 

    Supplemental methods. Download Text S1, DOCX file, 0.2 MB.

    Copyright © 2016 Carroll et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Figure S2

    Distribution of tsr genes in strains USA300, NCTC 8325, and MRSA252. Five tsr genes are unique to strain USA300. An additional five are found in strains USA300 and NCTC 8325 (but not MRSA252), while two are found in USA300 and MRSA252 (but not NCTC 8325). Twenty-seven tsr genes are found in all three strains. Download Figure S2, TIF file, 0.5 MB.

    Copyright © 2016 Carroll et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Figure S3 

    RNA-seq read alignment data for sarR and tsr33 during growth in human serum. Annotations for CDS genes are shown by black arrows, and the annotation for sRNA is shown by a red arrow. The depth of read coverage on the genome is shown by blue histogram. Greater depth of read coverage for tsr33 suggests that a sarR-independent tsr33 exists under these conditions. Download Figure S3, TIF file, 0.4 MB.

    Copyright © 2016 Carroll et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Table S3 

    Expression values for 303 S. aureus USA300 sRNA genes in TSB and human serum. Table S3, XLSX file, 0.1 MB.

    Copyright © 2016 Carroll et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Figure S4 

    Reverse transcriptase PCR-based detection of newly identified sRNAs in S. aureus. PCRs were performed with primers specific to newly identified sRNA genes. DNA-depleted RNA, DNA, and H2O were employed as the templates to verify the complete removal of DNA from RNA samples, the correct sizes of the respective amplicons, and the absence of DNA contaminations. Successful, size-specific amplification of a target from cDNA suggests the presence of transcript at the position where a novel sRNA annotation was added to the genome file. Download Figure S4, TIF file, 0.5 MB.

    Copyright © 2016 Carroll et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Additional Files

  • Figures
  • Tables
  • Supplemental Material
  • Supplementary Data

    Supplementary Data

    • Text s1, DOCX - Text s1, DOCX
    • Figure sf1, TIF - Figure sf1, TIF
    • Figure sf2, TIF - Figure sf2, TIF
    • Figure sf3, TIF - Figure sf3, TIF
    • Figure sf4, TIF - Figure sf4, TIF
    • Table st1, DOCX - Table st1, DOCX
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Genome-wide Annotation, Identification, and Global Transcriptomic Analysis of Regulatory or Small RNA Gene Expression in Staphylococcus aureus
Ronan K. Carroll, Andy Weiss, William H. Broach, Richard E. Wiemels, Austin B. Mogen, Kelly C. Rice, Lindsey N. Shaw
mBio Feb 2016, 7 (1) e01990-15; DOI: 10.1128/mBio.01990-15

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Genome-wide Annotation, Identification, and Global Transcriptomic Analysis of Regulatory or Small RNA Gene Expression in Staphylococcus aureus
Ronan K. Carroll, Andy Weiss, William H. Broach, Richard E. Wiemels, Austin B. Mogen, Kelly C. Rice, Lindsey N. Shaw
mBio Feb 2016, 7 (1) e01990-15; DOI: 10.1128/mBio.01990-15
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