Abstract
By screening a collection of Salmonella mutants deleted for genes encoding small proteins of 60 amino acids, we identified three paralogous small genes (ymdF, STM14_1829, and yciG) required for wild-type flagellum-dependent swimming and swarming motility. The ymdF, STM14_1829, and yciG genes encode small proteins of 55, 60, and 60 amino acid residues, respectively. A bioinformatics analysis predicted that these small proteins are intrinsically disordered proteins, and circular dichroism analysis of purified recombinant proteins confirmed that all three proteins are unstructured in solution. A mutant deleted for STM14_1829 showed the most severe motility defect, indicating that among the three paralogs, STM14_1829 is a key protein required for wild-type motility. We determined that relative to the wild type, the expression of the flagellin protein FliC is lower in the ΔSTM14_1829 mutant due to the downregulation of the flhDC operon encoding the FlhDC master regulator. By comparing the gene expression profiles between the wild-type and ΔSTM14_1829 strains via RNA sequencing, we found that the gene encoding the response regulator PhoP is upregulated in the ΔSTM14_1829 mutant, suggesting the indirect repression of the flhDC operon by the activated PhoP. Homologs of STM14_1829 are conserved in a wide range of bacteria, including Escherichia coli and Pseudomonas aeruginosa. We showed that the inactivation of STM14_1829 homologs in E. coli and P. aeruginosa also alters motility, suggesting that this family of small intrinsically disordered proteins may play a role in the cellular pathway(s) that affects motility. IMPORTANCE This study reports the identification of a novel family of small intrinsically disordered proteins that are conserved in a wide range of flagellated and nonflagellated bacteria. Although this study identifies the role of these small proteins in the scope of flagellum-dependent motility in Salmonella, they likely play larger roles in a more conserved cellular pathway(s) that indirectly affects flagellum expression in the case of motile bacteria. Small intrinsically disordered proteins have not been well characterized in prokaryotes, and the results of our study provide a basis for their detailed functional characterization.
Original language | English (US) |
---|---|
Article number | e00415-18 |
Journal | Journal of Bacteriology |
Volume | 201 |
Issue number | 2 |
DOIs | |
State | Published - Jan 1 2019 |
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Keywords
- Flagella
- Intrinsically disordered proteins
- Motility
- PhoP
- Salmonella
- Small proteins
ASJC Scopus subject areas
- Microbiology
- Molecular Biology
Cite this
A family of small intrinsically disordered proteins involved in flagellum-dependent motility in salmonella enterica. / Oguri, Tamiko; Kwon, Youjeong; Woo, Jerry K.K.; Prehna, Gerd; Lee, Hyun; Ning, Miaoran; Won, Kyoung Jae; Lee, Jiyoung; Mei, Sally; Shi, Yixin; Jeong, Hyunyoung; Lee, Hyunwoo.
In: Journal of Bacteriology, Vol. 201, No. 2, e00415-18, 01.01.2019.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - A family of small intrinsically disordered proteins involved in flagellum-dependent motility in salmonella enterica
AU - Oguri, Tamiko
AU - Kwon, Youjeong
AU - Woo, Jerry K.K.
AU - Prehna, Gerd
AU - Lee, Hyun
AU - Ning, Miaoran
AU - Won, Kyoung Jae
AU - Lee, Jiyoung
AU - Mei, Sally
AU - Shi, Yixin
AU - Jeong, Hyunyoung
AU - Lee, Hyunwoo
PY - 2019/1/1
Y1 - 2019/1/1
N2 - By screening a collection of Salmonella mutants deleted for genes encoding small proteins of 60 amino acids, we identified three paralogous small genes (ymdF, STM14_1829, and yciG) required for wild-type flagellum-dependent swimming and swarming motility. The ymdF, STM14_1829, and yciG genes encode small proteins of 55, 60, and 60 amino acid residues, respectively. A bioinformatics analysis predicted that these small proteins are intrinsically disordered proteins, and circular dichroism analysis of purified recombinant proteins confirmed that all three proteins are unstructured in solution. A mutant deleted for STM14_1829 showed the most severe motility defect, indicating that among the three paralogs, STM14_1829 is a key protein required for wild-type motility. We determined that relative to the wild type, the expression of the flagellin protein FliC is lower in the ΔSTM14_1829 mutant due to the downregulation of the flhDC operon encoding the FlhDC master regulator. By comparing the gene expression profiles between the wild-type and ΔSTM14_1829 strains via RNA sequencing, we found that the gene encoding the response regulator PhoP is upregulated in the ΔSTM14_1829 mutant, suggesting the indirect repression of the flhDC operon by the activated PhoP. Homologs of STM14_1829 are conserved in a wide range of bacteria, including Escherichia coli and Pseudomonas aeruginosa. We showed that the inactivation of STM14_1829 homologs in E. coli and P. aeruginosa also alters motility, suggesting that this family of small intrinsically disordered proteins may play a role in the cellular pathway(s) that affects motility. IMPORTANCE This study reports the identification of a novel family of small intrinsically disordered proteins that are conserved in a wide range of flagellated and nonflagellated bacteria. Although this study identifies the role of these small proteins in the scope of flagellum-dependent motility in Salmonella, they likely play larger roles in a more conserved cellular pathway(s) that indirectly affects flagellum expression in the case of motile bacteria. Small intrinsically disordered proteins have not been well characterized in prokaryotes, and the results of our study provide a basis for their detailed functional characterization.
AB - By screening a collection of Salmonella mutants deleted for genes encoding small proteins of 60 amino acids, we identified three paralogous small genes (ymdF, STM14_1829, and yciG) required for wild-type flagellum-dependent swimming and swarming motility. The ymdF, STM14_1829, and yciG genes encode small proteins of 55, 60, and 60 amino acid residues, respectively. A bioinformatics analysis predicted that these small proteins are intrinsically disordered proteins, and circular dichroism analysis of purified recombinant proteins confirmed that all three proteins are unstructured in solution. A mutant deleted for STM14_1829 showed the most severe motility defect, indicating that among the three paralogs, STM14_1829 is a key protein required for wild-type motility. We determined that relative to the wild type, the expression of the flagellin protein FliC is lower in the ΔSTM14_1829 mutant due to the downregulation of the flhDC operon encoding the FlhDC master regulator. By comparing the gene expression profiles between the wild-type and ΔSTM14_1829 strains via RNA sequencing, we found that the gene encoding the response regulator PhoP is upregulated in the ΔSTM14_1829 mutant, suggesting the indirect repression of the flhDC operon by the activated PhoP. Homologs of STM14_1829 are conserved in a wide range of bacteria, including Escherichia coli and Pseudomonas aeruginosa. We showed that the inactivation of STM14_1829 homologs in E. coli and P. aeruginosa also alters motility, suggesting that this family of small intrinsically disordered proteins may play a role in the cellular pathway(s) that affects motility. IMPORTANCE This study reports the identification of a novel family of small intrinsically disordered proteins that are conserved in a wide range of flagellated and nonflagellated bacteria. Although this study identifies the role of these small proteins in the scope of flagellum-dependent motility in Salmonella, they likely play larger roles in a more conserved cellular pathway(s) that indirectly affects flagellum expression in the case of motile bacteria. Small intrinsically disordered proteins have not been well characterized in prokaryotes, and the results of our study provide a basis for their detailed functional characterization.
KW - Flagella
KW - Intrinsically disordered proteins
KW - Motility
KW - PhoP
KW - Salmonella
KW - Small proteins
UR - http://www.scopus.com/inward/record.url?scp=85060178875&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85060178875&partnerID=8YFLogxK
U2 - 10.1128/JB.00415-18
DO - 10.1128/JB.00415-18
M3 - Article
C2 - 30373755
AN - SCOPUS:85060178875
VL - 201
JO - Journal of Bacteriology
JF - Journal of Bacteriology
SN - 0021-9193
IS - 2
M1 - e00415-18
ER -