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Ronan K. Carroll
Ohio University

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Journal article
Published: 28 April 2021 in mSphere
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Enteric bacterial pathogens, like Escherichia coli , are known to experience large temperature differences as they are transmitted through the fecal oral route. This change in temperature has been demonstrated to influence bacterial gene expression and facilitate infection. Staphylococcus aureus is a human-associated pathogen that can live as a commensal on the skin and nares or cause invasive infections of the deeper tissues and blood.

ACS Style

Raeven A. Bastock; Emily C. Marino; Richard E. Wiemels; Donald L. Holzschu; Rebecca A. Keogh; Rachel L. Zapf; Erin R. Murphy; Ronan K. Carroll. Staphylococcus aureus Responds to Physiologically Relevant Temperature Changes by Altering Its Global Transcript and Protein Profile. mSphere 2021, 6, 1 .

AMA Style

Raeven A. Bastock, Emily C. Marino, Richard E. Wiemels, Donald L. Holzschu, Rebecca A. Keogh, Rachel L. Zapf, Erin R. Murphy, Ronan K. Carroll. Staphylococcus aureus Responds to Physiologically Relevant Temperature Changes by Altering Its Global Transcript and Protein Profile. mSphere. 2021; 6 (2):1.

Chicago/Turabian Style

Raeven A. Bastock; Emily C. Marino; Richard E. Wiemels; Donald L. Holzschu; Rebecca A. Keogh; Rachel L. Zapf; Erin R. Murphy; Ronan K. Carroll. 2021. "Staphylococcus aureus Responds to Physiologically Relevant Temperature Changes by Altering Its Global Transcript and Protein Profile." mSphere 6, no. 2: 1.

Journal article
Published: 19 January 2021 in Journal of Bacteriology
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Peptidyl-prolyl cis/trans isomerases (PPIases) are enzymes that assist in protein folding around proline-peptide bonds, and they often possess chaperone activity. Staphylococcus aureus encodes three PPIases, i.e., PrsA, PpiB, and trigger factor (TF). Previous work by our group demonstrated a role for both PrsA and PpiB in S. aureus; however, TF remains largely unstudied. Here, we identify a role for TF in S. aureus biofilm formation and demonstrate cooperation between TF and the cytoplasmic PPIase PpiB. Mutation of the tig gene (encoding TF) led to reduced biofilm development in vitro but no significant attenuation of virulence in a mouse model of infection. To investigate whether TF possesses chaperone activity, we analyzed the ability of a tig mutant to survive acid and base stress. While there was no significant decrease for a tig mutant, a ppiB tig double mutant exhibited significant decreases in cell viability after acid and base challenges. We then demonstrated that a ppiB tig double mutant had exacerbated phenotypes in vitro and in vivo, compared to either single mutant. Finally, in vivo immunoprecipitation of epitope-tagged PpiB revealed that PpiB interacted with 4 times the number of proteins when TF was absent from the cell, suggesting that it may be compensating for the loss of TF. Interestingly, the only proteins found to interact with TF were TF itself, fibronectin-binding protein B (FnBPB), and the chaperone protein ClpB. Collectively, these results support the first phenotype for S. aureus TF and demonstrate a greater network of cooperation between chaperone proteins in Staphylococcus aureus. IMPORTANCE S. aureus encodes a large number of virulence factors that aid the bacterium in survival and pathogenesis. These virulence factors have a wide variety of functions; however, they must all be properly secreted in order to be functional. Bacterial chaperone proteins often assist in secretion by trafficking proteins to secretion machinery or assisting in proper protein folding. Here, we report that the S. aureus chaperone TF contributes to biofilm formation and cooperates with the chaperone PpiB to regulate S. aureus virulence processes. These data highlight the first known role for TF in S. aureus and suggest that S. aureus chaperone proteins may be involved in a greater regulatory network in the cell.

ACS Style

Rebecca A. Keogh; Rachel L. Zapf; Andrew Frey; Emily C. Marino; Gillian G. Null; Richard E. Wiemels; Donald L. Holzschu; Lindsey N. Shaw; Ronan K. Carroll. Staphylococcus aureus Trigger Factor Is Involved in Biofilm Formation and Cooperates with the Chaperone PpiB. Journal of Bacteriology 2021, 203, 1 .

AMA Style

Rebecca A. Keogh, Rachel L. Zapf, Andrew Frey, Emily C. Marino, Gillian G. Null, Richard E. Wiemels, Donald L. Holzschu, Lindsey N. Shaw, Ronan K. Carroll. Staphylococcus aureus Trigger Factor Is Involved in Biofilm Formation and Cooperates with the Chaperone PpiB. Journal of Bacteriology. 2021; 203 (7):1.

Chicago/Turabian Style

Rebecca A. Keogh; Rachel L. Zapf; Andrew Frey; Emily C. Marino; Gillian G. Null; Richard E. Wiemels; Donald L. Holzschu; Lindsey N. Shaw; Ronan K. Carroll. 2021. "Staphylococcus aureus Trigger Factor Is Involved in Biofilm Formation and Cooperates with the Chaperone PpiB." Journal of Bacteriology 203, no. 7: 1.

Journal article
Published: 09 January 2021 in Chemical Engineering Journal
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A standalone electrochemical method for detecting the bacterium Escherichia coli in water was developed using a nickel electrode and no biorecognition element. Electric current responses from different E. coli concentrations were recorded based on their interaction with a locally formed electrocatalyst. A rotating disk electrode was used to minimize the mass transport limitations at the interface. Results from experiments with the rotating disk electrode also paved the way for hypothesizing the detection mechanism. The operating conditions were established for sensing the electric current responses in the presence of E. coli. The least-squares linear regression model was fit to the data obtained from currents of some known E. coli concentrations. This probe had a detection limit in the order of 104 CFU/ml. The response time to detect the presence/absence of E. coli was less than half a second, while the total assay time, including quantification of its concentration, was 10 min. The electric current response from a solution mixed with E. coli and S. aureus showed current similar to E. coli only solution indicating the specificity of the sensor to respond to signals from E. coli. This electrochemical microbial sensor's uniqueness lies in its ability to rapidly detect E. coli by forming the catalyst locally on demand without the attachment of biorecognition elements.

ACS Style

Ashwin Ramanujam; Bertrand Neyhouse; Rebecca A. Keogh; Madhivanan Muthuvel; Ronan K. Carroll; Gerardine G. Botte. Rapid electrochemical detection of Escherichia coli using nickel oxidation reaction on a rotating disk electrode. Chemical Engineering Journal 2021, 411, 128453 .

AMA Style

Ashwin Ramanujam, Bertrand Neyhouse, Rebecca A. Keogh, Madhivanan Muthuvel, Ronan K. Carroll, Gerardine G. Botte. Rapid electrochemical detection of Escherichia coli using nickel oxidation reaction on a rotating disk electrode. Chemical Engineering Journal. 2021; 411 ():128453.

Chicago/Turabian Style

Ashwin Ramanujam; Bertrand Neyhouse; Rebecca A. Keogh; Madhivanan Muthuvel; Ronan K. Carroll; Gerardine G. Botte. 2021. "Rapid electrochemical detection of Escherichia coli using nickel oxidation reaction on a rotating disk electrode." Chemical Engineering Journal 411, no. : 128453.

Article
Published: 18 December 2020 in Journal of Bacteriology
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Dental caries form when acid produced by oral bacteria erodes tooth enamel. This process is driven by the fermentative metabolism of cariogenic bacteria, most notably Streptococcus mutans . Nutrient acquisition is key in the competitive oral cavity, and many organisms have evolved various strategies to procure carbon sources or necessary biomolecules. B vitamins, such as riboflavin, which many oral streptococci must scavenge from the oral environment, are necessary for survival within the competitive oral cavity. However, the primary mechanism and proteins involved in this process remain uncharacterized. This study is important because it identifies a key step in S. mutans riboflavin acquisition and cofactor generation, which may enable the development of novel anticaries treatment strategies via selective targeting of metabolite transporters.

ACS Style

Matthew E. Turner; Khanh Huynh; Ronan K. Carroll; Sang-Joon Ahn; Kelly C. Rice. Characterization of the Streptococcus mutans SMU.1703c-SMU.1702c Operon Reveals Its Role in Riboflavin Import and Response to Acid Stress. Journal of Bacteriology 2020, 203, 1 .

AMA Style

Matthew E. Turner, Khanh Huynh, Ronan K. Carroll, Sang-Joon Ahn, Kelly C. Rice. Characterization of the Streptococcus mutans SMU.1703c-SMU.1702c Operon Reveals Its Role in Riboflavin Import and Response to Acid Stress. Journal of Bacteriology. 2020; 203 (2):1.

Chicago/Turabian Style

Matthew E. Turner; Khanh Huynh; Ronan K. Carroll; Sang-Joon Ahn; Kelly C. Rice. 2020. "Characterization of the Streptococcus mutans SMU.1703c-SMU.1702c Operon Reveals Its Role in Riboflavin Import and Response to Acid Stress." Journal of Bacteriology 203, no. 2: 1.

Journal article
Published: 16 November 2020 in Infection and Immunity
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Extracellular vesicles (EVs) are membrane-derived lipid bilayers secreted by bacteria and eukaryotic cells. Bacterial membrane vesicles were discovered over 60 years ago and have been extensively studied in Gram-negative bacteria. During their production, EVs are loaded with proteins, nucleic acids, and various compounds that are subsequently released into the environment. Depending on the packaged cargo, EVs have a broad spectrum of action and are involved in pathogenesis, antibiotic resistance, nutrient uptake, and nucleic acid transfer.

ACS Style

Paul Briaud; Ronan K. Carroll. Extracellular Vesicle Biogenesis and Functions in Gram-Positive Bacteria. Infection and Immunity 2020, 88, 1 .

AMA Style

Paul Briaud, Ronan K. Carroll. Extracellular Vesicle Biogenesis and Functions in Gram-Positive Bacteria. Infection and Immunity. 2020; 88 (12):1.

Chicago/Turabian Style

Paul Briaud; Ronan K. Carroll. 2020. "Extracellular Vesicle Biogenesis and Functions in Gram-Positive Bacteria." Infection and Immunity 88, no. 12: 1.

Journal article
Published: 26 August 2020 in mSphere
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Regulatory small RNAs (sRNAs) are a class of RNA molecules that are produced in bacterial cells but that typically do not encode proteins. Instead, they perform a variety of critical functions within the cell as RNA. Most bacterial genomes do not include annotations for sRNA genes, and any type of analysis that is performed using a bacterial genome as a reference will therefore overlook data for sRNAs. In this study, we reexamined hundreds of previously generated S. aureus RNA-Seq data sets and reanalyzed them to generate data for sRNAs. To do so, we utilized an updated S. aureus genome annotation file, previously generated by our group, which contains annotations for 303 sRNAs. The data generated (which were previously discarded) shed new light on sRNAs in S. aureus , most of which are unstudied, and highlight certain sRNAs that are likely to play important roles in the cell.

ACS Style

Hailee M. Sorensen; Rebecca A. Keogh; Marcus A. Wittekind; Andrew R. Caillet; Richard E. Wiemels; Elizabeth A. Laner; Ronan K. Carroll. Reading between the Lines: Utilizing RNA-Seq Data for Global Analysis of sRNAs in Staphylococcus aureus. mSphere 2020, 5, 1 .

AMA Style

Hailee M. Sorensen, Rebecca A. Keogh, Marcus A. Wittekind, Andrew R. Caillet, Richard E. Wiemels, Elizabeth A. Laner, Ronan K. Carroll. Reading between the Lines: Utilizing RNA-Seq Data for Global Analysis of sRNAs in Staphylococcus aureus. mSphere. 2020; 5 (4):1.

Chicago/Turabian Style

Hailee M. Sorensen; Rebecca A. Keogh; Marcus A. Wittekind; Andrew R. Caillet; Richard E. Wiemels; Elizabeth A. Laner; Ronan K. Carroll. 2020. "Reading between the Lines: Utilizing RNA-Seq Data for Global Analysis of sRNAs in Staphylococcus aureus." mSphere 5, no. 4: 1.

Scholarlyarticle
Published: 26 February 2020 in Endocrinology
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The gut microbiome has been implicated in host metabolism, endocrinology, and pathophysiology. Furthermore, several studies have shown that gut bacteria impact host growth, partially mediated through the growth hormone (GH)/insulin-like growth factor 1 (IGF-1) axis. Yet, no study to date has examined the specific role of GH on the gut microbiome. Our study thus characterized the adult gut microbial profile and intestinal phenotype in GH gene-disrupted (GH-/-) mice (a model of GH deficiency) and bovine GH transgenic (bGH) mice (a model of chronic, excess GH action) at 6 months of age. Both the GH-/- and bGH mice had altered microbial signatures, in opposing directions at the phylum and genus levels. For example, GH-/- mice had significantly reduced abundance in the Proteobacteria, Campylobacterota, and Actinobacteria phyla, whereas bGH mice exhibited a trending increase in those phyla compared with respective controls. Analysis of maturity of the microbial community demonstrated that lack of GH results in a significantly more immature microbiome while excess GH increases microbial maturity. Several common bacterial genera were shared, although in opposing directions, between the 2 mouse lines (e.g., decreased in GH-/- mice and increased in bGH mice), suggesting an association with GH. Similarly, metabolic pathways like acetate, butyrate, heme B, and folate biosynthesis were predicted to be impacted by GH. This study is the first to characterize the gut microbiome in mouse lines with altered GH action and indicates that GH may play a role in the growth of certain microbiota thus impacting microbial maturation and metabolic function.

ACS Style

Elizabeth A Jensen; Jonathan A Young; Zachary Jackson; Joshua Busken; Edward O List; Ronan K Carroll; John J Kopchick; Erin R Murphy; Darlene E Berryman. Growth Hormone Deficiency and Excess Alter the Gut Microbiome in Adult Male Mice. Endocrinology 2020, 161, 1 .

AMA Style

Elizabeth A Jensen, Jonathan A Young, Zachary Jackson, Joshua Busken, Edward O List, Ronan K Carroll, John J Kopchick, Erin R Murphy, Darlene E Berryman. Growth Hormone Deficiency and Excess Alter the Gut Microbiome in Adult Male Mice. Endocrinology. 2020; 161 (4):1.

Chicago/Turabian Style

Elizabeth A Jensen; Jonathan A Young; Zachary Jackson; Joshua Busken; Edward O List; Ronan K Carroll; John J Kopchick; Erin R Murphy; Darlene E Berryman. 2020. "Growth Hormone Deficiency and Excess Alter the Gut Microbiome in Adult Male Mice." Endocrinology 161, no. 4: 1.

Journal article
Published: 16 June 2019 in Toxins
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Peptidyl-prolyl cis/trans isomerases (PPIases) are enzymes that catalyze the cis-to-trans isomerization around proline bonds, allowing proteins to fold into their correct confirmation. Previously, we identified two PPIase enzymes in Staphylococcus aureus (PpiB and PrsA) that are involved in the regulation of virulence determinants and have shown that PpiB contributes to S. aureus virulence in a murine abscess model of infection. Here, we further examine the role of these PPIases in S. aureus virulence and, in particular, their regulation of hemolytic toxins. Using murine abscess and systemic models of infection, we show that a ppiB mutant in a USA300 background is attenuated for virulence but that a prsA mutant is not. Deletion of the ppiB gene leads to decreased bacterial survival in macrophages and nasal epithelial cells, while there is no significant difference when prsA is deleted. Analysis of culture supernatants reveals that a ppiB mutant strain has reduced levels of the phenol-soluble modulins and that both ppiB and prsA mutants have reduced alpha-toxin activity. Finally, we perform immunoprecipitation to identify cellular targets of PpiB and PrsA. Results suggest a novel role for PpiB in S. aureus protein secretion. Collectively, our results demonstrate that PpiB and PrsA influence S. aureus toxins via distinct mechanisms, and that PpiB but not PrsA contributes to disease.

ACS Style

Rebecca A. Keogh; Rachel L. Zapf; Emily Trzeciak; Gillian G. Null; Richard E. Wiemels; Ronan K. Carroll. Novel Regulation of Alpha-Toxin and the Phenol-Soluble Modulins by Peptidyl-Prolyl cis/trans Isomerase Enzymes in Staphylococcus aureus. Toxins 2019, 11, 343 .

AMA Style

Rebecca A. Keogh, Rachel L. Zapf, Emily Trzeciak, Gillian G. Null, Richard E. Wiemels, Ronan K. Carroll. Novel Regulation of Alpha-Toxin and the Phenol-Soluble Modulins by Peptidyl-Prolyl cis/trans Isomerase Enzymes in Staphylococcus aureus. Toxins. 2019; 11 (6):343.

Chicago/Turabian Style

Rebecca A. Keogh; Rachel L. Zapf; Emily Trzeciak; Gillian G. Null; Richard E. Wiemels; Ronan K. Carroll. 2019. "Novel Regulation of Alpha-Toxin and the Phenol-Soluble Modulins by Peptidyl-Prolyl cis/trans Isomerase Enzymes in Staphylococcus aureus." Toxins 11, no. 6: 343.

Journal article
Published: 01 May 2019 in Infection and Immunity
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Numerous factors have, to date, been identified as playing a role in the regulation of Agr activity in Staphylococcus aureus , including transcription factors, antisense RNAs, and host elements. Herein we investigated the product of SAUSA300_1984 (termed MroQ), a transmembrane Abi-domain/M79 protease-family protein, as a novel effector of this system.

ACS Style

Stephanie Marroquin; Brittney Gimza; Brooke Tomlinson; Michelle Stein; Andrew Frey; Rebecca A. Keogh; Rachel Zapf; Daniel A. Todd; Nadja B. Cech; Ronan K. Carroll; Lindsey N. Shaw. MroQ Is a Novel Abi-Domain Protein That Influences Virulence Gene Expression in Staphylococcus aureus via Modulation of Agr Activity. Infection and Immunity 2019, 87, e00002-19 .

AMA Style

Stephanie Marroquin, Brittney Gimza, Brooke Tomlinson, Michelle Stein, Andrew Frey, Rebecca A. Keogh, Rachel Zapf, Daniel A. Todd, Nadja B. Cech, Ronan K. Carroll, Lindsey N. Shaw. MroQ Is a Novel Abi-Domain Protein That Influences Virulence Gene Expression in Staphylococcus aureus via Modulation of Agr Activity. Infection and Immunity. 2019; 87 (5):e00002-19.

Chicago/Turabian Style

Stephanie Marroquin; Brittney Gimza; Brooke Tomlinson; Michelle Stein; Andrew Frey; Rebecca A. Keogh; Rachel Zapf; Daniel A. Todd; Nadja B. Cech; Ronan K. Carroll; Lindsey N. Shaw. 2019. "MroQ Is a Novel Abi-Domain Protein That Influences Virulence Gene Expression in Staphylococcus aureus via Modulation of Agr Activity." Infection and Immunity 87, no. 5: e00002-19.

Journal article
Published: 26 February 2019 in mBio
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The alpha phenol-soluble modulins (αPSMs) are among the most potent toxins produced by Staphylococcus aureus . Their biological role during infection has been studied in detail; however, the way they are produced by the bacterial cell is not well understood. In this work, we identify a small RNA molecule called Teg41 that plays an important role in αPSM production by S. aureus . Teg41 positively influences αPSM production. The importance of Teg41 is highlighted by the fact that a strain containing a deletion in the 3′ end of Teg41 produces significantly less αPSMs and is attenuated for virulence in a mouse abscess model of infection. As the search for new therapeutic strategies to combat S. aureus infection proceeds, Teg41 may represent a novel target.

ACS Style

Rachel Zapf; Richard E. Wiemels; Rebecca A. Keogh; Donald L. Holzschu; Kayla M. Howell; Emily Trzeciak; Andrew R. Caillet; Kellie A. King; Samantha A. Selhorst; Michael J. Naldrett; Jeffrey L. Bose; Ronan K. Carroll. The Small RNA Teg41 Regulates Expression of the Alpha Phenol-Soluble Modulins and Is Required for Virulence in Staphylococcus aureus. mBio 2019, 10, e02484-18 .

AMA Style

Rachel Zapf, Richard E. Wiemels, Rebecca A. Keogh, Donald L. Holzschu, Kayla M. Howell, Emily Trzeciak, Andrew R. Caillet, Kellie A. King, Samantha A. Selhorst, Michael J. Naldrett, Jeffrey L. Bose, Ronan K. Carroll. The Small RNA Teg41 Regulates Expression of the Alpha Phenol-Soluble Modulins and Is Required for Virulence in Staphylococcus aureus. mBio. 2019; 10 (1):e02484-18.

Chicago/Turabian Style

Rachel Zapf; Richard E. Wiemels; Rebecca A. Keogh; Donald L. Holzschu; Kayla M. Howell; Emily Trzeciak; Andrew R. Caillet; Kellie A. King; Samantha A. Selhorst; Michael J. Naldrett; Jeffrey L. Bose; Ronan K. Carroll. 2019. "The Small RNA Teg41 Regulates Expression of the Alpha Phenol-Soluble Modulins and Is Required for Virulence in Staphylococcus aureus." mBio 10, no. 1: e02484-18.

Preprint content
Published: 10 January 2019
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Numerous factors have to date been identified as playing a role in the regulation of Agr activity in S. aureus, including transcription factors, antisense RNAs, and host elements. Herein we investigate the product of SAUSA300_1984 (termed MroQ), a transmembrane Abi-domain/M79 protease-family protein, as a novel effector of this system. Using a USA300 mroQ mutant we observed a drastic reduction in proteolysis, hemolysis and pigmentation that was fully complementable. This appears to result from diminished agr activity, as transcriptional analysis revealed significant decreases in expression of both RNAII and RNAIII in the mroQ mutant. Such effects appear to be direct, rather than indirect, as known agr effectors demonstrated limited alterations in their activity upon mroQ disruption. A comparison of RNA-sequencing datasets for both mroQ and agr mutants reveal a profound overlap in their regulomes, with the majority of factors affected being known virulence determinants. Importantly, the preponderance of alterations in expression were more striking in the agr mutant, indicating that MroQ is necessary, but not sufficient, for Agr function. Mechanism profiling revealed that putative residues for metalloprotease activity within MroQ are required for its Agr controlling effect, however this is not wielded at the level of AgrD processing. Virulence assessment demonstrated that mroQ and agr mutants both exhibited increased formation of renal abscesses, but decreased skin abscess formation, alongside diminished dermonecrosis. Collectively, we present the characterization of a novel agr effector in S. aureus, which would appear to be a direct regulator, potentially functioning via interaction with the AgrC histidine kinase.

ACS Style

Stephanie Marroquin; Brittney D. Gimza; Brooke Tomlinson; Michelle Stein; Andrew Frey; Rebecca A. Keogh; Rachel L Zapf; Daniel A. Todd; Nadja B. Cech; Ronan K. Carroll; Lindsey N. Shaw. MroQ is a Novel Abi-domain Protein That Influences Virulence Gene Expression in Staphylococcus aureus via Modulation of Agr Activity. 2019, 516914 .

AMA Style

Stephanie Marroquin, Brittney D. Gimza, Brooke Tomlinson, Michelle Stein, Andrew Frey, Rebecca A. Keogh, Rachel L Zapf, Daniel A. Todd, Nadja B. Cech, Ronan K. Carroll, Lindsey N. Shaw. MroQ is a Novel Abi-domain Protein That Influences Virulence Gene Expression in Staphylococcus aureus via Modulation of Agr Activity. . 2019; ():516914.

Chicago/Turabian Style

Stephanie Marroquin; Brittney D. Gimza; Brooke Tomlinson; Michelle Stein; Andrew Frey; Rebecca A. Keogh; Rachel L Zapf; Daniel A. Todd; Nadja B. Cech; Ronan K. Carroll; Lindsey N. Shaw. 2019. "MroQ is a Novel Abi-domain Protein That Influences Virulence Gene Expression in Staphylococcus aureus via Modulation of Agr Activity." , no. : 516914.

Journal article
Published: 01 November 2018 in Infection and Immunity
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The Staphylococcus aureus cyclophilin PpiB is an intracellular peptidyl prolyl cis/trans isomerase (PPIase) that has previously been shown to contribute to secreted nuclease and hemolytic activity. In this study, we investigated the contribution of PpiB to S. aureus virulence.

ACS Style

Rebecca A. Keogh; Rachel Zapf; Richard E. Wiemels; Marcus A. Wittekind; Ronan K. Carroll. The Intracellular Cyclophilin PpiB Contributes to the Virulence of Staphylococcus aureus Independently of Its Peptidyl-Prolyl cis/trans Isomerase Activity. Infection and Immunity 2018, 86, e00379-18 .

AMA Style

Rebecca A. Keogh, Rachel Zapf, Richard E. Wiemels, Marcus A. Wittekind, Ronan K. Carroll. The Intracellular Cyclophilin PpiB Contributes to the Virulence of Staphylococcus aureus Independently of Its Peptidyl-Prolyl cis/trans Isomerase Activity. Infection and Immunity. 2018; 86 (11):e00379-18.

Chicago/Turabian Style

Rebecca A. Keogh; Rachel Zapf; Richard E. Wiemels; Marcus A. Wittekind; Ronan K. Carroll. 2018. "The Intracellular Cyclophilin PpiB Contributes to the Virulence of Staphylococcus aureus Independently of Its Peptidyl-Prolyl cis/trans Isomerase Activity." Infection and Immunity 86, no. 11: e00379-18.

Journal article
Published: 24 April 2018 in FEMS Microbiology Letters
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ACS Style

Halie K Miller; Whittney N Burda; Ronan K Carroll; Lindsey N Shaw. Identification of a unique transcriptional architecture for the sigS operon in Staphylococcus aureus. FEMS Microbiology Letters 2018, 365, 1 .

AMA Style

Halie K Miller, Whittney N Burda, Ronan K Carroll, Lindsey N Shaw. Identification of a unique transcriptional architecture for the sigS operon in Staphylococcus aureus. FEMS Microbiology Letters. 2018; 365 (12):1.

Chicago/Turabian Style

Halie K Miller; Whittney N Burda; Ronan K Carroll; Lindsey N Shaw. 2018. "Identification of a unique transcriptional architecture for the sigS operon in Staphylococcus aureus." FEMS Microbiology Letters 365, no. 12: 1.

Journal article
Published: 26 January 2017 in Genes
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Small regulatory RNAs (sRNAs) of Shigella dysenteriae and other pathogens are vital for the regulation of virulence-associated genes and processes. Here, we characterize RyfA1, one member of a sibling pair of sRNAs produced by S. dysenteriae. Unlike its nearly identical sibling molecule, RyfA2, predicted to be encoded almost exclusively by non-pathogenic species, the presence of a gene encoding RyfA1, or a RyfA1-like molecule, is strongly correlated with virulence in a variety of enteropathogens. In S. dysenteriae, the overproduction of RyfA1 negatively impacts the virulence-associated process of cell-to-cell spread as well as the expression of ompC, a gene encoding a major outer membrane protein important for the pathogenesis of Shigella. Interestingly, the production of RyfA1 is controlled by a second sRNA, here termed RyfB1, the first incidence of one regulatory small RNA controlling another in S. dysenteriae or any Shigella species.

ACS Style

Megan E. Fris; William H. Broach; Sarah E. Klim; Peter W. Coschigano; Ronan K. Carroll; Clayton C. Caswell; Erin R. Murphy. Sibling sRNA RyfA1 Influences Shigella dysenteriae Pathogenesis. Genes 2017, 8, 50 .

AMA Style

Megan E. Fris, William H. Broach, Sarah E. Klim, Peter W. Coschigano, Ronan K. Carroll, Clayton C. Caswell, Erin R. Murphy. Sibling sRNA RyfA1 Influences Shigella dysenteriae Pathogenesis. Genes. 2017; 8 (2):50.

Chicago/Turabian Style

Megan E. Fris; William H. Broach; Sarah E. Klim; Peter W. Coschigano; Ronan K. Carroll; Clayton C. Caswell; Erin R. Murphy. 2017. "Sibling sRNA RyfA1 Influences Shigella dysenteriae Pathogenesis." Genes 8, no. 2: 50.

Journal article
Published: 01 January 2017 in Journal of Bacteriology
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Staphylococcus aureus is an important human pathogen that relies on a large repertoire of secreted and cell wall-associated proteins for pathogenesis. Consequently, the ability of the organism to cause disease is absolutely dependent on its ability to synthesize and successfully secrete these proteins. In this study, we investigate the role of peptidyl-prolyl cis/trans isomerases (PPIases) on the activity of the S. aureus secreted virulence factor nuclease (Nuc). We identify a staphylococcal cyclophilin-type PPIase (PpiB) that is required for optimal activity of Nuc. Disruption of ppiB results in decreased nuclease activity in culture supernatants; however, the levels of Nuc protein are not altered, suggesting that the decrease in activity results from misfolding of Nuc in the absence of PpiB. We go on to demonstrate that PpiB exhibits PPIase activity in vitro , is localized to the bacterial cytosol, and directly interacts with Nuc in vitro to accelerate the rate of Nuc refolding. Finally, we demonstrate an additional role for PpiB in S. aureus hemolysis and demonstrate that the S. aureus parvulin-type PPIase PrsA also plays a role in the activity of secreted virulence factors. The deletion of prsA leads to a decrease in secreted protease and phospholipase activity, similar to that observed in other Gram-positive pathogens. Together, these results demonstrate, for the first time to our knowledge, that PPIases play an important role in the secretion of virulence factors in S. aureus . IMPORTANCE Staphylococcus aureus is a highly dangerous bacterial pathogen capable of causing a variety of infections throughout the human body. The ability of S. aureus to cause disease is largely due to an extensive repertoire of secreted and cell wall-associated proteins, including adhesins, toxins, exoenzymes, and superantigens. These virulence factors, once produced, are typically transported across the cell membrane by the secretory (Sec) system in a denatured state. Consequently, once outside the cell, they must refold into their active form. This step often requires the assistance of bacterial folding proteins, such as PPIases. In this work, we investigate the role of PPIases in S. aureus and uncover a cyclophilin-type enzyme that assists in the folding/refolding of staphylococcal nuclease.

ACS Style

Richard E. Wiemels; Stephanie M. Cech; Nikki M. Meyer; Caleb A. Burke; Andy Weiss; Anastacia R. Parks; Lindsey N. Shaw; Ronan K. Carroll. An Intracellular Peptidyl-Prolyl cis / trans Isomerase Is Required for Folding and Activity of the Staphylococcus aureus Secreted Virulence Factor Nuclease. Journal of Bacteriology 2017, 199, 1 .

AMA Style

Richard E. Wiemels, Stephanie M. Cech, Nikki M. Meyer, Caleb A. Burke, Andy Weiss, Anastacia R. Parks, Lindsey N. Shaw, Ronan K. Carroll. An Intracellular Peptidyl-Prolyl cis / trans Isomerase Is Required for Folding and Activity of the Staphylococcus aureus Secreted Virulence Factor Nuclease. Journal of Bacteriology. 2017; 199 (1):1.

Chicago/Turabian Style

Richard E. Wiemels; Stephanie M. Cech; Nikki M. Meyer; Caleb A. Burke; Andy Weiss; Anastacia R. Parks; Lindsey N. Shaw; Ronan K. Carroll. 2017. "An Intracellular Peptidyl-Prolyl cis / trans Isomerase Is Required for Folding and Activity of the Staphylococcus aureus Secreted Virulence Factor Nuclease." Journal of Bacteriology 199, no. 1: 1.

Journal article
Published: 02 March 2016 in mBio
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In Staphylococcus aureus , hundreds of small regulatory or small RNAs (sRNAs) have been identified, yet this class of molecule remains poorly understood and severely understudied. sRNA genes are typically absent from genome annotation files, and as a consequence, their existence is often overlooked, particularly in global transcriptomic studies. To facilitate improved detection and analysis of sRNAs in S. aureus , we generated updated GenBank files for three commonly used S. aureus strains (MRSA252, NCTC 8325, and USA300), in which we added annotations for >260 previously identified sRNAs. These files, the first to include genome-wide annotation of sRNAs in S. aureus , were then used as a foundation to identify novel sRNAs in the community-associated methicillin-resistant strain USA300. This analysis led to the discovery of 39 previously unidentified sRNAs. Investigating the genomic loci of the newly identified sRNAs revealed a surprising degree of inconsistency in genome annotation in S. aureus , which may be hindering the analysis and functional exploration of these elements. Finally, using our newly created annotation files as a reference, we perform a global analysis of sRNA gene expression in S. aureus and demonstrate that the newly identified tsr25 is the most highly upregulated sRNA in human serum. This study provides an invaluable resource to the S. aureus research community in the form of our newly generated annotation files, while at the same time presenting the first examination of differential sRNA expression in pathophysiologically relevant conditions. IMPORTANCE Despite a large number of studies identifying regulatory or small RNA (sRNA) genes in Staphylococcus aureus , their annotation is notably lacking in available genome files. In addition to this, there has been a considerable lack of cross-referencing in the wealth of studies identifying these elements, often leading to the same sRNA being identified multiple times and bearing multiple names. In this work, we have consolidated and curated known sRNA genes from the literature and mapped them to their position on the S. aureus genome, creating new genome annotation files. These files can now be used by the scientific community at large in experiments to search for previously undiscovered sRNA genes and to monitor sRNA gene expression by transcriptome sequencing (RNA-seq). We demonstrate this application, identifying 39 new sRNAs and studying their expression during S. aureus growth in human serum.

ACS Style

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

AMA Style

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

Chicago/Turabian Style

Ronan K. Carroll; Andy Weiss; William H. Broach; Richard E. Wiemels; Austin B. Mogen; Kelly C. Rice; Lindsey N. Shaw. 2016. "Genome-wide Annotation, Identification, and Global Transcriptomic Analysis of Regulatory or Small RNA Gene Expression in Staphylococcus aureus." mBio 7, no. 1: e01990-15-15.

Journal article
Published: 01 February 2016 in Journal of Bacteriology
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Global regulator of virulence A (GrvA) is a ToxR-family transcriptional regulator that activates locus of enterocyte effacement (LEE)-dependent adherence in enterohemorrhagic Escherichia coli (EHEC). LEE activation by GrvA requires the Rcs phosphorelay response regulator RcsB and is sensitive to physiologically relevant concentrations of bicarbonate, a known stimulant of virulence systems in intestinal pathogens. This study determines the genomic scale of GrvA-dependent regulation and uncovers details of the molecular mechanism underlying GrvA-dependent regulation of pathogenic mechanisms in EHEC. In a grvA -null background of EHEC strain TW14359, RNA sequencing analysis revealed the altered expression of over 700 genes, including the downregulation of LEE- and non-LEE-encoded effectors and the upregulation of genes for glutamate-dependent acid resistance (GDAR). Upregulation of GDAR genes corresponded with a marked increase in acid resistance. GrvA-dependent regulation of GDAR and the LEE required gadE , the central activator of GDAR genes and a direct repressor of the LEE. Control of gadE by GrvA was further determined to occur through downregulation of the gadE activator GadW. This interaction of GrvA with GadW-GadE represses the acid resistance phenotype, while it concomitantly activates the LEE-dependent adherence and secretion of immune subversion effectors. The results of this study significantly broaden the scope of GrvA-dependent regulation and its role in EHEC pathogenesis. IMPORTANCE Enterohemorrhagic Escherichia coli (EHEC) is an intestinal human pathogen causing acute hemorrhagic colitis and life-threatening hemolytic-uremic syndrome. For successful transmission and gut colonization, EHEC relies on the glutamate-dependent acid resistance (GDAR) system and a type III secretion apparatus, encoded on the LEE pathogenicity island. This study investigates the mechanism whereby the DNA-binding regulator GrvA coordinates activation of the LEE with repression of GDAR. Investigating how these systems are regulated leads to an understanding of pathogenic behavior and novel strategies aimed at disease prevention and control.

ACS Style

Jason K. Morgan; Ronan K. Carroll; Carly M. Harro; Khoury W. Vendura; Lindsey Shaw; James T. Riordan. Global Regulator of Virulence A (GrvA) Coordinates Expression of Discrete Pathogenic Mechanisms in Enterohemorrhagic Escherichia coli through Interactions with GadW-GadE. Journal of Bacteriology 2016, 198, 394 -409.

AMA Style

Jason K. Morgan, Ronan K. Carroll, Carly M. Harro, Khoury W. Vendura, Lindsey Shaw, James T. Riordan. Global Regulator of Virulence A (GrvA) Coordinates Expression of Discrete Pathogenic Mechanisms in Enterohemorrhagic Escherichia coli through Interactions with GadW-GadE. Journal of Bacteriology. 2016; 198 (3):394-409.

Chicago/Turabian Style

Jason K. Morgan; Ronan K. Carroll; Carly M. Harro; Khoury W. Vendura; Lindsey Shaw; James T. Riordan. 2016. "Global Regulator of Virulence A (GrvA) Coordinates Expression of Discrete Pathogenic Mechanisms in Enterohemorrhagic Escherichia coli through Interactions with GadW-GadE." Journal of Bacteriology 198, no. 3: 394-409.