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Discovery of Staphylococcus aureus small RNAs highly expressed during human chronic infection.

Λεπτομέρειες βιβλιογραφικής εγγραφής
Τίτλος: Discovery of Staphylococcus aureus small RNAs highly expressed during human chronic infection.
Συγγραφείς: Briaud P; School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA.; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, USA., Schumacher J; School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA.; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, USA., Whiteley M; School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA.; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, USA.; Emory-Children's Cystic Fibrosis Center, Atlanta, Georgia, USA.
Πηγή: MBio [mBio] 2026 Sep 09; Vol. 17 (9), pp. e0063726. Date of Electronic Publication: 2026 Aug 07.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: American Society for Microbiology Country of Publication: United States NLM ID: 101519231 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2150-7511 (Electronic) NLM ISO Abbreviation: mBio Subsets: MEDLINE
Imprint Name(s): Original Publication: Washington, D.C. : American Society for Microbiology
Ιατρικοί όροι (MeSH): Staphylococcus aureus*/genetics , Staphylococcus aureus*/metabolism , Staphylococcal Infections*/microbiology , RNA, Bacterial*/genetics , Persistent Infection*/microbiology , RNA, Small Untranslated*/genetics , Gene Expression Regulation, Bacterial*, Zinc/metabolism ; Cystic Fibrosis/microbiology ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Humans ; Gene Expression Profiling ; Transcriptome
Περίληψη: Understanding bacterial gene expression in natural environments remains challenging because most regulatory networks are inferred from in vitro models that poorly capture in situ environmental conditions. Here, we present NEMO (network transcriptomics of microbes in native environments), a generalizable pangenome-based metatranscriptomic framework for extracting microbial transcriptional programs from metatranscriptomes generated from natural samples. We applied NEMO to Staphylococcus aureus metatranscriptomes from human chronic wounds and cystic fibrosis sputum, revealing infection-associated transcriptional states that diverged markedly from in vitro growth conditions. Notably, small RNAs (sRNAs) were key drivers of the transcriptional divergence between human infection-derived and in vitro transcriptomes. Among these, we identify rsaX20 as a previously uncharacterized, zinc-responsive sRNA that also encodes a small peptide. Meta-analysis of more than 2,000 publicly available S. aureus RNA-seq data sets showed that rsaX20 is induced under zinc limitation and host-associated stress and is co-regulated with known metal-responsive sRNAs. Genetic, transcriptomic, and proteomic analyses demonstrated that rsaX20 is repressed by the zinc regulator Zur and functions as a dual-purpose sRNA/small open reading frame, with the RNA and peptide exerting distinct, sometimes opposing, effects on target proteins. Together, these findings establish NEMO as a broadly applicable framework for interrogating microbial gene regulation directly from native metatranscriptomes and identify rsaX20 as a key regulator of zinc homeostasis during chronic human S. aureus infection.
Importance: Most knowledge of bacterial gene regulation comes from laboratory cultures, yet pathogens behave very differently inside the human body. We introduce NEMO, a pangenome-based framework that enables direct analysis of microbial gene expression from natural infection samples. Applying NEMO to human Staphylococcus aureus infections revealed transcriptional programs that differ substantially from standard in vitro models and highlighted small regulatory RNAs as major drivers of this divergence. Using this approach, we discovered rsaX20, a previously uncharacterized zinc-responsive regulatory RNA that also encodes a small peptide with distinct biological functions. These findings demonstrate the power of studying microbes in their native environments and uncover a key regulator of zinc homeostasis during chronic human infection.
Competing Interests: The authors declare no conflict of interest.
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Grant Information: R21 AI190856 United States AI NIAID NIH HHS; R21AI190856 National Institute of Allergy and Infectious Diseases
Contributed Indexing: Keywords: Staphylococcus aureus; chronic infection; chronic wound infection; cystic fibrosis; in vivo gene expression; metatranscriptomic; pangenome; small regulatory RNA (sRNA); zinc; zinc homeostasis
Substance Nomenclature: 0 (RNA, Bacterial)
J41CSQ7QDS (Zinc)
0 (Bacterial Proteins)
0 (RNA, Small Untranslated)
Entry Date(s): Date Created: 20260807 Date Completed: 20260909 Latest Revision: 20260912
Update Code: 20260912
PubMed Central ID: PMC13556194
DOI: 10.1128/mbio.00637-26
PMID: 42565592
Βάση Δεδομένων: MEDLINE
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Items – Name: Title
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  Group: Ti
  Data: Discovery of Staphylococcus aureus small RNAs highly expressed during human chronic infection.
– Name: Author
  Label: Authors
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  Data: <searchLink fieldCode="AU" term="%22Briaud+P%22">Briaud P</searchLink>; School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA.; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, USA.<br /><searchLink fieldCode="AU" term="%22Schumacher+J%22">Schumacher J</searchLink>; School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA.; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, USA.<br /><searchLink fieldCode="AU" term="%22Whiteley+M%22">Whiteley M</searchLink>; School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA.; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, USA.; Emory-Children's Cystic Fibrosis Center, Atlanta, Georgia, USA.
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  Data: <searchLink fieldCode="JN" term="%22101519231%22">MBio</searchLink> [mBio] 2026 Sep 09; Vol. 17 (9), pp. e0063726. <i>Date of Electronic Publication: </i>2026 Aug 07.
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  Data: <i>Publisher: </i><searchLink fieldCode="PB" term="%22American+Society+for+Microbiology%22">American Society for Microbiology </searchLink><i>Country of Publication: </i>United States <i>NLM ID: </i>101519231 <i>Publication Model: </i>Print-Electronic <i>Cited Medium: </i>Internet <i>ISSN: </i>2150-7511 (Electronic) <i>NLM ISO Abbreviation: </i>mBio <i>Subsets: </i>MEDLINE
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  Data: <i>Original Publication</i>: Washington, D.C. : American Society for Microbiology
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  Data: <searchLink fieldCode="MM" term="%22Staphylococcus+aureus%22">Staphylococcus aureus*</searchLink>/<searchLink fieldCode="MM" term="%22Staphylococcus+aureus+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Staphylococcus+aureus%22">Staphylococcus aureus*</searchLink>/<searchLink fieldCode="MM" term="%22Staphylococcus+aureus+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Staphylococcal+Infections%22">Staphylococcal Infections*</searchLink>/<searchLink fieldCode="MM" term="%22Staphylococcal+Infections+microbiology%22">microbiology</searchLink> <br /><searchLink fieldCode="MM" term="%22RNA%2C+Bacterial%22">RNA, Bacterial*</searchLink>/<searchLink fieldCode="MM" term="%22RNA%2C+Bacterial+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Persistent+Infection%22">Persistent Infection*</searchLink>/<searchLink fieldCode="MM" term="%22Persistent+Infection+microbiology%22">microbiology</searchLink> <br /><searchLink fieldCode="MM" term="%22RNA%2C+Small+Untranslated%22">RNA, Small Untranslated*</searchLink>/<searchLink fieldCode="MM" term="%22RNA%2C+Small+Untranslated+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Gene+Expression+Regulation%2C+Bacterial%22">Gene Expression Regulation, Bacterial*</searchLink><br /><searchLink fieldCode="MH" term="%22Zinc%22">Zinc</searchLink>/<searchLink fieldCode="MH" term="%22Zinc+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Cystic+Fibrosis%22">Cystic Fibrosis</searchLink>/<searchLink fieldCode="MH" term="%22Cystic+Fibrosis+microbiology%22">microbiology</searchLink> ; <searchLink fieldCode="MH" term="%22Bacterial+Proteins%22">Bacterial Proteins</searchLink>/<searchLink fieldCode="MH" term="%22Bacterial+Proteins+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Bacterial+Proteins%22">Bacterial Proteins</searchLink>/<searchLink fieldCode="MH" term="%22Bacterial+Proteins+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Humans%22">Humans</searchLink> ; <searchLink fieldCode="MH" term="%22Gene+Expression+Profiling%22">Gene Expression Profiling</searchLink> ; <searchLink fieldCode="MH" term="%22Transcriptome%22">Transcriptome</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Understanding bacterial gene expression in natural environments remains challenging because most regulatory networks are inferred from in vitro models that poorly capture in situ environmental conditions. Here, we present NEMO (network transcriptomics of microbes in native environments), a generalizable pangenome-based metatranscriptomic framework for extracting microbial transcriptional programs from metatranscriptomes generated from natural samples. We applied NEMO to Staphylococcus aureus metatranscriptomes from human chronic wounds and cystic fibrosis sputum, revealing infection-associated transcriptional states that diverged markedly from in vitro growth conditions. Notably, small RNAs (sRNAs) were key drivers of the transcriptional divergence between human infection-derived and in vitro transcriptomes. Among these, we identify rsaX20 as a previously uncharacterized, zinc-responsive sRNA that also encodes a small peptide. Meta-analysis of more than 2,000 publicly available S. aureus RNA-seq data sets showed that rsaX20 is induced under zinc limitation and host-associated stress and is co-regulated with known metal-responsive sRNAs. Genetic, transcriptomic, and proteomic analyses demonstrated that rsaX20 is repressed by the zinc regulator Zur and functions as a dual-purpose sRNA/small open reading frame, with the RNA and peptide exerting distinct, sometimes opposing, effects on target proteins. Together, these findings establish NEMO as a broadly applicable framework for interrogating microbial gene regulation directly from native metatranscriptomes and identify rsaX20 as a key regulator of zinc homeostasis during chronic human S. aureus infection.<br />Importance: Most knowledge of bacterial gene regulation comes from laboratory cultures, yet pathogens behave very differently inside the human body. We introduce NEMO, a pangenome-based framework that enables direct analysis of microbial gene expression from natural infection samples. Applying NEMO to human Staphylococcus aureus infections revealed transcriptional programs that differ substantially from standard in vitro models and highlighted small regulatory RNAs as major drivers of this divergence. Using this approach, we discovered rsaX20, a previously uncharacterized zinc-responsive regulatory RNA that also encodes a small peptide with distinct biological functions. These findings demonstrate the power of studying microbes in their native environments and uncover a key regulator of zinc homeostasis during chronic human infection.
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: The authors declare no conflict of interest.
– Name: Ref
  Label: References
  Group: RefInfo
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  Label: Grant Information
  Group: Grant
  Data: R21 AI190856 United States AI NIAID NIH HHS; R21AI190856 National Institute of Allergy and Infectious Diseases
– Name: SubjectMinor
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  Group:
  Data: <i>Keywords: </i>Staphylococcus aureus; chronic infection; chronic wound infection; cystic fibrosis; in vivo gene expression; metatranscriptomic; pangenome; small regulatory RNA (sRNA); zinc; zinc homeostasis
– Name: NumberCAS
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  Data: 0 (RNA, Bacterial)<br />J41CSQ7QDS (Zinc)<br />0 (Bacterial Proteins)<br />0 (RNA, Small Untranslated)
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  Data: <i>Date Created: </i>20260807 <i>Date Completed: </i>20260909 <i>Latest Revision: </i>20260912
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  Data: 10.1128/mbio.00637-26
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        Value: 10.1128/mbio.00637-26
    Languages:
      – Code: eng
        Text: English
    PhysicalDescription:
      Pagination:
        StartPage: e0063726
    Subjects:
      – SubjectFull: Zinc metabolism
        Type: general
      – SubjectFull: Cystic Fibrosis microbiology
        Type: general
      – SubjectFull: Bacterial Proteins genetics
        Type: general
      – SubjectFull: Bacterial Proteins metabolism
        Type: general
      – SubjectFull: Humans
        Type: general
      – SubjectFull: Gene Expression Profiling
        Type: general
      – SubjectFull: Transcriptome
        Type: general
      – SubjectFull: Staphylococcus aureus genetics
        Type: general
      – SubjectFull: Staphylococcus aureus metabolism
        Type: general
      – SubjectFull: Staphylococcal Infections microbiology
        Type: general
      – SubjectFull: RNA, Bacterial genetics
        Type: general
      – SubjectFull: Persistent Infection microbiology
        Type: general
      – SubjectFull: RNA, Small Untranslated genetics
        Type: general
      – SubjectFull: Gene Expression Regulation, Bacterial
        Type: general
    Titles:
      – TitleFull: Discovery of Staphylococcus aureus small RNAs highly expressed during human chronic infection.
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            – D: 09
              M: 09
              Text: 2026 Sep 09
              Type: published
              Y: 2026
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              Value: 2150-7511
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              Value: 17
            – Type: issue
              Value: 9
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