Regulation of Exopolysaccharide Production by ProE, a Cyclic-Di-GMP Phosphodiesterase in Pseudomonas aeruginosa PAO1
The ubiquitous second messenger c-di-GMP is involved in regulation of multiple biological functions including the important extracellular matrix exopolysaccharides (EPS). But how c-di-GMP metabolic proteins influence EPS and their enzymatic properties are not fully understood. Here we showed that de...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-06-01
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| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.01226/full |
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Article |
| collection |
DOAJ |
| language |
English |
| format |
Article |
| sources |
DOAJ |
| author |
Qishun Feng Qishun Feng Stephen Dela Ahator Stephen Dela Ahator Tian Zhou Tian Zhou Zhiqing Liu Zhiqing Liu Qiqi Lin Qiqi Lin Yang Liu Yang Liu Jiahui Huang Jiahui Huang Jianuan Zhou Jianuan Zhou Lian-Hui Zhang Lian-Hui Zhang |
| spellingShingle |
Qishun Feng Qishun Feng Stephen Dela Ahator Stephen Dela Ahator Tian Zhou Tian Zhou Zhiqing Liu Zhiqing Liu Qiqi Lin Qiqi Lin Yang Liu Yang Liu Jiahui Huang Jiahui Huang Jianuan Zhou Jianuan Zhou Lian-Hui Zhang Lian-Hui Zhang Regulation of Exopolysaccharide Production by ProE, a Cyclic-Di-GMP Phosphodiesterase in Pseudomonas aeruginosa PAO1 Frontiers in Microbiology Pseudomonas aeruginosa c-di-GMP phosphodiesterase enzymatic properties exopolysaccharide Pel and Psl |
| author_facet |
Qishun Feng Qishun Feng Stephen Dela Ahator Stephen Dela Ahator Tian Zhou Tian Zhou Zhiqing Liu Zhiqing Liu Qiqi Lin Qiqi Lin Yang Liu Yang Liu Jiahui Huang Jiahui Huang Jianuan Zhou Jianuan Zhou Lian-Hui Zhang Lian-Hui Zhang |
| author_sort |
Qishun Feng |
| title |
Regulation of Exopolysaccharide Production by ProE, a Cyclic-Di-GMP Phosphodiesterase in Pseudomonas aeruginosa PAO1 |
| title_short |
Regulation of Exopolysaccharide Production by ProE, a Cyclic-Di-GMP Phosphodiesterase in Pseudomonas aeruginosa PAO1 |
| title_full |
Regulation of Exopolysaccharide Production by ProE, a Cyclic-Di-GMP Phosphodiesterase in Pseudomonas aeruginosa PAO1 |
| title_fullStr |
Regulation of Exopolysaccharide Production by ProE, a Cyclic-Di-GMP Phosphodiesterase in Pseudomonas aeruginosa PAO1 |
| title_full_unstemmed |
Regulation of Exopolysaccharide Production by ProE, a Cyclic-Di-GMP Phosphodiesterase in Pseudomonas aeruginosa PAO1 |
| title_sort |
regulation of exopolysaccharide production by proe, a cyclic-di-gmp phosphodiesterase in pseudomonas aeruginosa pao1 |
| publisher |
Frontiers Media S.A. |
| series |
Frontiers in Microbiology |
| issn |
1664-302X |
| publishDate |
2020-06-01 |
| description |
The ubiquitous second messenger c-di-GMP is involved in regulation of multiple biological functions including the important extracellular matrix exopolysaccharides (EPS). But how c-di-GMP metabolic proteins influence EPS and their enzymatic properties are not fully understood. Here we showed that deletion of proE, which encodes a protein with GGDEF-EAL hybrid domains, significantly increased the transcriptional expression of the genes encoding EPS production in Pseudomonas aeruginosa PAO1 and changed the bacterial colony morphology. Our data showed that ProE is a very active phosphodiesterase (PDE), with a high enzyme activity in degradation of c-di-GMP. Interestingly, the optimal activity of ProE was found in the presence of Co2+, unlike other PDEs that commonly rely on Mg2+ or Mn2+ for best performance. Furthermore, we identified three widely conserved novel residues that are critical for the function of ProE through site-directed mutagenesis. Subsequent study showed that ProE, together with other three key PDEs, i.e., RbdA, BifA, and DipA regulate the EPS production in P. aeruginosa PAO1. Moreover, by using the GFP-fusion approach, we observed that these four EPS associated-PDEs showed a polar localization pattern in general. Taken together, our data unveil the molecular mechanisms of ProE in regulation of EPS production, and provide a new insight on its enzymatic properties in degradation of c-di-GMP. |
| topic |
Pseudomonas aeruginosa c-di-GMP phosphodiesterase enzymatic properties exopolysaccharide Pel and Psl |
| url |
https://www.frontiersin.org/article/10.3389/fmicb.2020.01226/full |
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doaj-b7b2078e86c14d5a969730eb2bb0f4fb2020-11-25T03:41:43ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-06-011110.3389/fmicb.2020.01226542974Regulation of Exopolysaccharide Production by ProE, a Cyclic-Di-GMP Phosphodiesterase in Pseudomonas aeruginosa PAO1Qishun Feng0Qishun Feng1Stephen Dela Ahator2Stephen Dela Ahator3Tian Zhou4Tian Zhou5Zhiqing Liu6Zhiqing Liu7Qiqi Lin8Qiqi Lin9Yang Liu10Yang Liu11Jiahui Huang12Jiahui Huang13Jianuan Zhou14Jianuan Zhou15Lian-Hui Zhang16Lian-Hui Zhang17Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, ChinaThe ubiquitous second messenger c-di-GMP is involved in regulation of multiple biological functions including the important extracellular matrix exopolysaccharides (EPS). But how c-di-GMP metabolic proteins influence EPS and their enzymatic properties are not fully understood. Here we showed that deletion of proE, which encodes a protein with GGDEF-EAL hybrid domains, significantly increased the transcriptional expression of the genes encoding EPS production in Pseudomonas aeruginosa PAO1 and changed the bacterial colony morphology. Our data showed that ProE is a very active phosphodiesterase (PDE), with a high enzyme activity in degradation of c-di-GMP. Interestingly, the optimal activity of ProE was found in the presence of Co2+, unlike other PDEs that commonly rely on Mg2+ or Mn2+ for best performance. Furthermore, we identified three widely conserved novel residues that are critical for the function of ProE through site-directed mutagenesis. Subsequent study showed that ProE, together with other three key PDEs, i.e., RbdA, BifA, and DipA regulate the EPS production in P. aeruginosa PAO1. Moreover, by using the GFP-fusion approach, we observed that these four EPS associated-PDEs showed a polar localization pattern in general. Taken together, our data unveil the molecular mechanisms of ProE in regulation of EPS production, and provide a new insight on its enzymatic properties in degradation of c-di-GMP.https://www.frontiersin.org/article/10.3389/fmicb.2020.01226/fullPseudomonas aeruginosac-di-GMPphosphodiesteraseenzymatic propertiesexopolysaccharidePel and Psl |