Integrated Analysis of Gene Expression, Protein Synthesis, and Epigenetic Modifications in Alcanivorax borkumensis SK2 Under Iron Limitation

This study aimed to understand the genetic and molecular mechanisms enabling Alcanivorax borkumensis SK2, a hydrocarbonoclastic marine bacterium, to thrive under iron-limited conditions. Using SMRT PacBio whole-genome sequencing, Illumina total RNA sequencing, and proteomics analysis, we examined th...

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Autores: Francesco Smedile, Renata Denaro, Francesca Crisafi, Domenico Giosa, Giuseppe D'Auria, Manuel Ferrer, Riccardo Rosselli, Martin S. Staege, Michail M. Yakimov, Laura Giuliano, Oleg N. Reva
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/391065
Acceso en línea:http://hdl.handle.net/10261/391065
Access Level:acceso abierto
Palabra clave:http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
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spelling Integrated Analysis of Gene Expression, Protein Synthesis, and Epigenetic Modifications in Alcanivorax borkumensis SK2 Under Iron LimitationFrancesco SmedileRenata DenaroFrancesca CrisafiDomenico GiosaGiuseppe D'AuriaManuel FerrerRiccardo RosselliMartin S. StaegeMichail M. YakimovLaura GiulianoOleg N. Revahttp://metadata.un.org/sdg/14Conserve and sustainably use the oceans, seas and marine resources for sustainable developmentThis study aimed to understand the genetic and molecular mechanisms enabling Alcanivorax borkumensis SK2, a hydrocarbonoclastic marine bacterium, to thrive under iron-limited conditions. Using SMRT PacBio whole-genome sequencing, Illumina total RNA sequencing, and proteomics analysis, we examined the strain's response to iron-rich and iron-depleted media. Despite minimal impact on growth, significant changes in gene expression were observed when using n-tetradecane or acetate under iron limitation. Iron scarcity, depending on the carbon source, affects energy metabolism, membrane transport, lipid metabolism, stress-adaptive responses, and siderophore synthesis. We identified several methyltransferases (MTases) in the studied genome, including RS14230, which is a part of a fully functional restriction-modification (RM) system causing bipartite cytosine methylation and DNA cleavage at AgGCcT sites. Another MTase, RS09425, controls bipartite adenine methylation at GaTNNNNNGtGG motifs; however, no restriction activity at these motifs has been detected. Many epigenetically modified nucleotides lacked canonical motifs, possibly due to MTase byproducts. Notably, non-canonical modifications were statistically associated with transcriptional start sites and gene regulation, suggesting an indirect role in transcription via DNA conformation changes and its accessibility to MTases near actively transcribed genes.Peer reviewedJohn Wiley & SonsEuropean CommissionMinistero dell'Università e della RicercaSmedile, Francesco [0000-0002-8385-564X]Denaro, Renata [0000-0003-4341-197X]Crisafi, Francesca [0000-0002-4917-893X]Giosa, Domenico [0000-0002-3893-5296]D'Auria, Guiseppe [0000-0003-0672-2541]Ferrer, Manuel [0000-0003-4962-4714]Yakimov, Michail M [0000-0003-1418-363X]Giuliano, Laura [0000-0001-7407-9696]Reva, Oleg N [0000-0002-5459-2772]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/391065reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttps://zenodo.org/records/13254283Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3910652026-05-22T06:33:51Z
dc.title.none.fl_str_mv Integrated Analysis of Gene Expression, Protein Synthesis, and Epigenetic Modifications in Alcanivorax borkumensis SK2 Under Iron Limitation
title Integrated Analysis of Gene Expression, Protein Synthesis, and Epigenetic Modifications in Alcanivorax borkumensis SK2 Under Iron Limitation
spellingShingle Integrated Analysis of Gene Expression, Protein Synthesis, and Epigenetic Modifications in Alcanivorax borkumensis SK2 Under Iron Limitation
Francesco Smedile
http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
title_short Integrated Analysis of Gene Expression, Protein Synthesis, and Epigenetic Modifications in Alcanivorax borkumensis SK2 Under Iron Limitation
title_full Integrated Analysis of Gene Expression, Protein Synthesis, and Epigenetic Modifications in Alcanivorax borkumensis SK2 Under Iron Limitation
title_fullStr Integrated Analysis of Gene Expression, Protein Synthesis, and Epigenetic Modifications in Alcanivorax borkumensis SK2 Under Iron Limitation
title_full_unstemmed Integrated Analysis of Gene Expression, Protein Synthesis, and Epigenetic Modifications in Alcanivorax borkumensis SK2 Under Iron Limitation
title_sort Integrated Analysis of Gene Expression, Protein Synthesis, and Epigenetic Modifications in Alcanivorax borkumensis SK2 Under Iron Limitation
dc.creator.none.fl_str_mv Francesco Smedile
Renata Denaro
Francesca Crisafi
Domenico Giosa
Giuseppe D'Auria
Manuel Ferrer
Riccardo Rosselli
Martin S. Staege
Michail M. Yakimov
Laura Giuliano
Oleg N. Reva
author Francesco Smedile
author_facet Francesco Smedile
Renata Denaro
Francesca Crisafi
Domenico Giosa
Giuseppe D'Auria
Manuel Ferrer
Riccardo Rosselli
Martin S. Staege
Michail M. Yakimov
Laura Giuliano
Oleg N. Reva
author_role author
author2 Renata Denaro
Francesca Crisafi
Domenico Giosa
Giuseppe D'Auria
Manuel Ferrer
Riccardo Rosselli
Martin S. Staege
Michail M. Yakimov
Laura Giuliano
Oleg N. Reva
author2_role author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv European Commission
Ministero dell'Università e della Ricerca
Smedile, Francesco [0000-0002-8385-564X]
Denaro, Renata [0000-0003-4341-197X]
Crisafi, Francesca [0000-0002-4917-893X]
Giosa, Domenico [0000-0002-3893-5296]
D'Auria, Guiseppe [0000-0003-0672-2541]
Ferrer, Manuel [0000-0003-4962-4714]
Yakimov, Michail M [0000-0003-1418-363X]
Giuliano, Laura [0000-0001-7407-9696]
Reva, Oleg N [0000-0002-5459-2772]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
topic http://metadata.un.org/sdg/14
Conserve and sustainably use the oceans, seas and marine resources for sustainable development
description This study aimed to understand the genetic and molecular mechanisms enabling Alcanivorax borkumensis SK2, a hydrocarbonoclastic marine bacterium, to thrive under iron-limited conditions. Using SMRT PacBio whole-genome sequencing, Illumina total RNA sequencing, and proteomics analysis, we examined the strain's response to iron-rich and iron-depleted media. Despite minimal impact on growth, significant changes in gene expression were observed when using n-tetradecane or acetate under iron limitation. Iron scarcity, depending on the carbon source, affects energy metabolism, membrane transport, lipid metabolism, stress-adaptive responses, and siderophore synthesis. We identified several methyltransferases (MTases) in the studied genome, including RS14230, which is a part of a fully functional restriction-modification (RM) system causing bipartite cytosine methylation and DNA cleavage at AgGCcT sites. Another MTase, RS09425, controls bipartite adenine methylation at GaTNNNNNGtGG motifs; however, no restriction activity at these motifs has been detected. Many epigenetically modified nucleotides lacked canonical motifs, possibly due to MTase byproducts. Notably, non-canonical modifications were statistically associated with transcriptional start sites and gene regulation, suggesting an indirect role in transcription via DNA conformation changes and its accessibility to MTases near actively transcribed genes.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/391065
url http://hdl.handle.net/10261/391065
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv https://zenodo.org/records/13254283
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv John Wiley & Sons
publisher.none.fl_str_mv John Wiley & Sons
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,812455

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