Iron Starvation Conditions Upregulate Ehrlichia ruminantium Type IV Secretion System, tr1 Transcription Factor and map1 Genes Family through the Master Regulatory Protein ErxR
Ehrlichia ruminantium is an obligatory intracellular bacterium that causes heartwater, a fatal disease in ruminants. Due to its intracellular nature, E. ruminantium requires a set of specific virulence factors, such as the type IV secretion system (T4SS), and outer membrane proteins (Map proteins) i...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-01-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fcimb.2017.00535/full |
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| author | Amal Moumène Amal Moumène Amal Moumène Silvina Gonzalez-Rizzo Silvina Gonzalez-Rizzo Thierry Lefrançois Thierry Lefrançois Nathalie Vachiéry Nathalie Vachiéry Damien F. Meyer Damien F. Meyer |
| author_facet | Amal Moumène Amal Moumène Amal Moumène Silvina Gonzalez-Rizzo Silvina Gonzalez-Rizzo Thierry Lefrançois Thierry Lefrançois Nathalie Vachiéry Nathalie Vachiéry Damien F. Meyer Damien F. Meyer |
| author_sort | Amal Moumène |
| collection | DOAJ |
| description | Ehrlichia ruminantium is an obligatory intracellular bacterium that causes heartwater, a fatal disease in ruminants. Due to its intracellular nature, E. ruminantium requires a set of specific virulence factors, such as the type IV secretion system (T4SS), and outer membrane proteins (Map proteins) in order to avoid and subvert the host's immune response. Several studies have been conducted to understand the regulation of the T4SS or outer membrane proteins, in Ehrlichia, but no integrated approach has been used to understand the regulation of Ehrlichia pathogenicity determinants in response to environmental cues. Iron is known to be a key nutrient for bacterial growth both in the environment and within hosts. In this study, we experimentally demonstrated the regulation of virB, map1, and tr1 genes by the newly identified master regulator ErxR (for Ehrlichia ruminantium expression regulator). We also analyzed the effect of iron depletion on the expression of erxR gene, tr1 transcription factor, T4SS and map1 genes clusters in E. ruminantium. We show that exposure of E. ruminantium to iron starvation induces erxR and subsequently tr1, virB, and map1 genes. Our results reveal tight co-regulation of T4SS and map1 genes via the ErxR regulatory protein at the transcriptional level, and, for the first time link map genes to the virulence function sensu stricto, thereby advancing our understanding of Ehrlichia's infection process. These results suggest that Ehrlichia is able to sense changes in iron concentrations in the environment and to regulate the expression of virulence factors accordingly. |
| first_indexed | 2024-12-23T06:03:42Z |
| format | Article |
| id | doaj.art-17d2ec359b4848198397dcfc40e6cb73 |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-12-23T06:03:42Z |
| publishDate | 2018-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-17d2ec359b4848198397dcfc40e6cb732022-12-21T17:57:36ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882018-01-01710.3389/fcimb.2017.00535288207Iron Starvation Conditions Upregulate Ehrlichia ruminantium Type IV Secretion System, tr1 Transcription Factor and map1 Genes Family through the Master Regulatory Protein ErxRAmal Moumène0Amal Moumène1Amal Moumène2Silvina Gonzalez-Rizzo3Silvina Gonzalez-Rizzo4Thierry Lefrançois5Thierry Lefrançois6Nathalie Vachiéry7Nathalie Vachiéry8Damien F. Meyer9Damien F. Meyer10Centre de Coopération Internationale en Recherche Agronomique Pour le Développement, UMR ASTRE, Petit-Bourg, FranceASTRE, Univ Montpellier, Centre de Coopération Internationale en Recherche Agronomique Pour le Développement, Institut National de la Recherche Agronomique, Montpellier, FranceUFR Sciences Exactes et Naturelles, Université des Antilles, Pointe-à-Pitre, FranceInstitut de Biologie Paris Seine (EPS - IBPS), Sorbonne Universités, UPMC Univ Paris 06, Univ Antilles, Univ Nice Sophia Antipolis, Centre National de la Recherche Scientifique Evolution Paris Seine, Paris, FranceEquipe Biologie de la Mangrove, UFR Sciences Exactes et Naturelles, Université des Antilles, Pointe-à-Pitre, FranceCentre de Coopération Internationale en Recherche Agronomique Pour le Développement, UMR ASTRE, Petit-Bourg, FranceASTRE, Univ Montpellier, Centre de Coopération Internationale en Recherche Agronomique Pour le Développement, Institut National de la Recherche Agronomique, Montpellier, FranceCentre de Coopération Internationale en Recherche Agronomique Pour le Développement, UMR ASTRE, Petit-Bourg, FranceASTRE, Univ Montpellier, Centre de Coopération Internationale en Recherche Agronomique Pour le Développement, Institut National de la Recherche Agronomique, Montpellier, FranceCentre de Coopération Internationale en Recherche Agronomique Pour le Développement, UMR ASTRE, Petit-Bourg, FranceASTRE, Univ Montpellier, Centre de Coopération Internationale en Recherche Agronomique Pour le Développement, Institut National de la Recherche Agronomique, Montpellier, FranceEhrlichia ruminantium is an obligatory intracellular bacterium that causes heartwater, a fatal disease in ruminants. Due to its intracellular nature, E. ruminantium requires a set of specific virulence factors, such as the type IV secretion system (T4SS), and outer membrane proteins (Map proteins) in order to avoid and subvert the host's immune response. Several studies have been conducted to understand the regulation of the T4SS or outer membrane proteins, in Ehrlichia, but no integrated approach has been used to understand the regulation of Ehrlichia pathogenicity determinants in response to environmental cues. Iron is known to be a key nutrient for bacterial growth both in the environment and within hosts. In this study, we experimentally demonstrated the regulation of virB, map1, and tr1 genes by the newly identified master regulator ErxR (for Ehrlichia ruminantium expression regulator). We also analyzed the effect of iron depletion on the expression of erxR gene, tr1 transcription factor, T4SS and map1 genes clusters in E. ruminantium. We show that exposure of E. ruminantium to iron starvation induces erxR and subsequently tr1, virB, and map1 genes. Our results reveal tight co-regulation of T4SS and map1 genes via the ErxR regulatory protein at the transcriptional level, and, for the first time link map genes to the virulence function sensu stricto, thereby advancing our understanding of Ehrlichia's infection process. These results suggest that Ehrlichia is able to sense changes in iron concentrations in the environment and to regulate the expression of virulence factors accordingly.http://journal.frontiersin.org/article/10.3389/fcimb.2017.00535/fullEhrlichia ruminantiummaster regulatoriron regulationT4SSmap genestr1 transcription factor |
| spellingShingle | Amal Moumène Amal Moumène Amal Moumène Silvina Gonzalez-Rizzo Silvina Gonzalez-Rizzo Thierry Lefrançois Thierry Lefrançois Nathalie Vachiéry Nathalie Vachiéry Damien F. Meyer Damien F. Meyer Iron Starvation Conditions Upregulate Ehrlichia ruminantium Type IV Secretion System, tr1 Transcription Factor and map1 Genes Family through the Master Regulatory Protein ErxR Frontiers in Cellular and Infection Microbiology Ehrlichia ruminantium master regulator iron regulation T4SS map genes tr1 transcription factor |
| title | Iron Starvation Conditions Upregulate Ehrlichia ruminantium Type IV Secretion System, tr1 Transcription Factor and map1 Genes Family through the Master Regulatory Protein ErxR |
| title_full | Iron Starvation Conditions Upregulate Ehrlichia ruminantium Type IV Secretion System, tr1 Transcription Factor and map1 Genes Family through the Master Regulatory Protein ErxR |
| title_fullStr | Iron Starvation Conditions Upregulate Ehrlichia ruminantium Type IV Secretion System, tr1 Transcription Factor and map1 Genes Family through the Master Regulatory Protein ErxR |
| title_full_unstemmed | Iron Starvation Conditions Upregulate Ehrlichia ruminantium Type IV Secretion System, tr1 Transcription Factor and map1 Genes Family through the Master Regulatory Protein ErxR |
| title_short | Iron Starvation Conditions Upregulate Ehrlichia ruminantium Type IV Secretion System, tr1 Transcription Factor and map1 Genes Family through the Master Regulatory Protein ErxR |
| title_sort | iron starvation conditions upregulate ehrlichia ruminantium type iv secretion system tr1 transcription factor and map1 genes family through the master regulatory protein erxr |
| topic | Ehrlichia ruminantium master regulator iron regulation T4SS map genes tr1 transcription factor |
| url | http://journal.frontiersin.org/article/10.3389/fcimb.2017.00535/full |
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