Alternative σ Factors Regulate Overlapping as Well as Distinct Stress Response and Metabolic Functions in <i>Listeria monocytogenes</i> under Stationary Phase Stress Condition
<i>Listeria monocytogenes</i> can regulate and fine-tune gene expression, to adapt to diverse stress conditions encountered during foodborne transmission. To further understand the contributions of alternative sigma (σ) factors to the regulation of <i>L. monocytogenes</i> gen...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2021-04-01
|
| Series: | Pathogens |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2076-0817/10/4/411 |
| _version_ | 1797539303324123136 |
|---|---|
| author | Renato H. Orsi Soraya Chaturongakul Haley F. Oliver Lalit Ponnala Ahmed Gaballa Martin Wiedmann |
| author_facet | Renato H. Orsi Soraya Chaturongakul Haley F. Oliver Lalit Ponnala Ahmed Gaballa Martin Wiedmann |
| author_sort | Renato H. Orsi |
| collection | DOAJ |
| description | <i>Listeria monocytogenes</i> can regulate and fine-tune gene expression, to adapt to diverse stress conditions encountered during foodborne transmission. To further understand the contributions of alternative sigma (σ) factors to the regulation of <i>L. monocytogenes</i> gene expression, RNA-Seq was performed on <i>L. monocytogenes</i> strain 10403S and five isogenic mutants (four strains bearing in-frame null mutations in three out of four alternative σ factor genes, ΔCHL, ΔBHL, ΔBCL, and ΔBCH, and one strain bearing null mutations in all four genes, ΔBCHL), grown to stationary phase. Our data showed that 184, 35, 34, and 20 genes were positively regulated by σ<sup>B</sup>, σ<sup>L</sup>, σ<sup>H</sup>, and σ<sup>C</sup> (posterior probability > 0.9 and Fold Change (FC) > 5.0), respectively. Moreover, σ<sup>B</sup>-dependent genes showed the highest FC (based on comparisons between the ΔCHL and the ΔBCHL strain), with 44 genes showing an FC > 100; only four σ<sup>L</sup>-dependent, and no σ<sup>H</sup>- or σ<sup>C</sup>-dependent genes showed FC >100. While σ<sup>B</sup>-regulated genes identified in this study are involved in stress-associated functions and metabolic pathways, σ<sup>L</sup> appears to largely regulate genes involved in a few specific metabolic pathways, including positive regulation of operons encoding phosphoenolpyruvate (PEP)-dependent phosphotransferase systems (PTSs). Overall, our data show that (i) σ<sup>B</sup> and σ<sup>L</sup> directly and indirectly regulate genes involved in several energy metabolism-related functions; (ii) alternative σ factors are involved in complex regulatory networks and appear to have epistatic effects in stationary phase cells; and (iii) σ<sup>B</sup> regulates multiple stress response pathways, while σ<sup>L</sup> and σ<sup>H</sup> positively regulate a smaller number of specific pathways. |
| first_indexed | 2024-03-10T12:44:04Z |
| format | Article |
| id | doaj.art-fdf1c61d042944668e92aa0ea506df97 |
| institution | Directory Open Access Journal |
| issn | 2076-0817 |
| language | English |
| last_indexed | 2024-03-10T12:44:04Z |
| publishDate | 2021-04-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Pathogens |
| spelling | doaj.art-fdf1c61d042944668e92aa0ea506df972023-11-21T13:42:55ZengMDPI AGPathogens2076-08172021-04-0110441110.3390/pathogens10040411Alternative σ Factors Regulate Overlapping as Well as Distinct Stress Response and Metabolic Functions in <i>Listeria monocytogenes</i> under Stationary Phase Stress ConditionRenato H. Orsi0Soraya Chaturongakul1Haley F. Oliver2Lalit Ponnala3Ahmed Gaballa4Martin Wiedmann5Department of Food Science, Cornell University, Ithaca, NY 14853, USADepartment of Microbiology, Faculty of Science, Mahidol University, Bangkok 10400, ThailandDepartment of Food Science, Cornell University, Ithaca, NY 14853, USAComputational Biology Service Unit, Cornell University, Ithaca, NY 14853, USADepartment of Food Science, Cornell University, Ithaca, NY 14853, USADepartment of Food Science, Cornell University, Ithaca, NY 14853, USA<i>Listeria monocytogenes</i> can regulate and fine-tune gene expression, to adapt to diverse stress conditions encountered during foodborne transmission. To further understand the contributions of alternative sigma (σ) factors to the regulation of <i>L. monocytogenes</i> gene expression, RNA-Seq was performed on <i>L. monocytogenes</i> strain 10403S and five isogenic mutants (four strains bearing in-frame null mutations in three out of four alternative σ factor genes, ΔCHL, ΔBHL, ΔBCL, and ΔBCH, and one strain bearing null mutations in all four genes, ΔBCHL), grown to stationary phase. Our data showed that 184, 35, 34, and 20 genes were positively regulated by σ<sup>B</sup>, σ<sup>L</sup>, σ<sup>H</sup>, and σ<sup>C</sup> (posterior probability > 0.9 and Fold Change (FC) > 5.0), respectively. Moreover, σ<sup>B</sup>-dependent genes showed the highest FC (based on comparisons between the ΔCHL and the ΔBCHL strain), with 44 genes showing an FC > 100; only four σ<sup>L</sup>-dependent, and no σ<sup>H</sup>- or σ<sup>C</sup>-dependent genes showed FC >100. While σ<sup>B</sup>-regulated genes identified in this study are involved in stress-associated functions and metabolic pathways, σ<sup>L</sup> appears to largely regulate genes involved in a few specific metabolic pathways, including positive regulation of operons encoding phosphoenolpyruvate (PEP)-dependent phosphotransferase systems (PTSs). Overall, our data show that (i) σ<sup>B</sup> and σ<sup>L</sup> directly and indirectly regulate genes involved in several energy metabolism-related functions; (ii) alternative σ factors are involved in complex regulatory networks and appear to have epistatic effects in stationary phase cells; and (iii) σ<sup>B</sup> regulates multiple stress response pathways, while σ<sup>L</sup> and σ<sup>H</sup> positively regulate a smaller number of specific pathways.https://www.mdpi.com/2076-0817/10/4/411<i>Listeria monocytogenes</i>stress responsealternative sigma factorsSigmaBSigmaCSigmaH |
| spellingShingle | Renato H. Orsi Soraya Chaturongakul Haley F. Oliver Lalit Ponnala Ahmed Gaballa Martin Wiedmann Alternative σ Factors Regulate Overlapping as Well as Distinct Stress Response and Metabolic Functions in <i>Listeria monocytogenes</i> under Stationary Phase Stress Condition Pathogens <i>Listeria monocytogenes</i> stress response alternative sigma factors SigmaB SigmaC SigmaH |
| title | Alternative σ Factors Regulate Overlapping as Well as Distinct Stress Response and Metabolic Functions in <i>Listeria monocytogenes</i> under Stationary Phase Stress Condition |
| title_full | Alternative σ Factors Regulate Overlapping as Well as Distinct Stress Response and Metabolic Functions in <i>Listeria monocytogenes</i> under Stationary Phase Stress Condition |
| title_fullStr | Alternative σ Factors Regulate Overlapping as Well as Distinct Stress Response and Metabolic Functions in <i>Listeria monocytogenes</i> under Stationary Phase Stress Condition |
| title_full_unstemmed | Alternative σ Factors Regulate Overlapping as Well as Distinct Stress Response and Metabolic Functions in <i>Listeria monocytogenes</i> under Stationary Phase Stress Condition |
| title_short | Alternative σ Factors Regulate Overlapping as Well as Distinct Stress Response and Metabolic Functions in <i>Listeria monocytogenes</i> under Stationary Phase Stress Condition |
| title_sort | alternative σ factors regulate overlapping as well as distinct stress response and metabolic functions in i listeria monocytogenes i under stationary phase stress condition |
| topic | <i>Listeria monocytogenes</i> stress response alternative sigma factors SigmaB SigmaC SigmaH |
| url | https://www.mdpi.com/2076-0817/10/4/411 |
| work_keys_str_mv | AT renatohorsi alternativesfactorsregulateoverlappingaswellasdistinctstressresponseandmetabolicfunctionsinilisteriamonocytogenesiunderstationaryphasestresscondition AT sorayachaturongakul alternativesfactorsregulateoverlappingaswellasdistinctstressresponseandmetabolicfunctionsinilisteriamonocytogenesiunderstationaryphasestresscondition AT haleyfoliver alternativesfactorsregulateoverlappingaswellasdistinctstressresponseandmetabolicfunctionsinilisteriamonocytogenesiunderstationaryphasestresscondition AT lalitponnala alternativesfactorsregulateoverlappingaswellasdistinctstressresponseandmetabolicfunctionsinilisteriamonocytogenesiunderstationaryphasestresscondition AT ahmedgaballa alternativesfactorsregulateoverlappingaswellasdistinctstressresponseandmetabolicfunctionsinilisteriamonocytogenesiunderstationaryphasestresscondition AT martinwiedmann alternativesfactorsregulateoverlappingaswellasdistinctstressresponseandmetabolicfunctionsinilisteriamonocytogenesiunderstationaryphasestresscondition |