Methylglyoxal synthase regulates cell elongation via alterations of cellular methylglyoxal and spermidine content in Bacillus subtilis
•Methylglyoxal (MG) stimulates the expression of the gene encoding methylglyoxal synthase (mgsA) in Bacillus subtilis.•MgsA-overexpressing cells show remarkable elongation compared with mgsA-deficient cells.•SpeB and speE, which encode agmatinase and spermidine synthase, respectively, induce MG bios...
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| Veröffentlicht in: | The international journal of biochemistry & cell biology 2017-10, Vol.91 (Pt A), p.14-28 |
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| creator | Shin, Sang-Min Song, Sung-Hyun Lee, Jin-Woo Kwak, Min-Kyu Kang, Sa-Ouk |
| description | •Methylglyoxal (MG) stimulates the expression of the gene encoding methylglyoxal synthase (mgsA) in Bacillus subtilis.•MgsA-overexpressing cells show remarkable elongation compared with mgsA-deficient cells.•SpeB and speE, which encode agmatinase and spermidine synthase, respectively, induce MG biosynthesis.•SpeB- and speE-overexpressing cells have an elongated, rod-shaped morphology.•Expression of mgsA and polyamine genes is regulated by clpP-linked spx.
Methylglyoxal regulates cell division and differentiation through its interaction with polyamines. Loss of their biosynthesizing enzyme causes physiological impairment and cell elongation in eukaryotes. However, the reciprocal effects of methylglyoxal and polyamine production and its regulatory metabolic switches on morphological changes in prokaryotes have not been addressed. Here, Bacillus subtilis methylglyoxal synthase (mgsA) and polyamine biosynthesizing genes encoding arginine decarboxylase (SpeA), agmatinase (SpeB), and spermidine synthase (SpeE), were disrupted or overexpressed. Treatment of 0.2mM methylglyoxal and 1mM spermidine led to the elongation and shortening of B. subtilis wild-type cells to 12.38±3.21μm (P |
| doi_str_mv | 10.1016/j.biocel.2017.08.005 |
| format | Article |
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Methylglyoxal regulates cell division and differentiation through its interaction with polyamines. Loss of their biosynthesizing enzyme causes physiological impairment and cell elongation in eukaryotes. However, the reciprocal effects of methylglyoxal and polyamine production and its regulatory metabolic switches on morphological changes in prokaryotes have not been addressed. Here, Bacillus subtilis methylglyoxal synthase (mgsA) and polyamine biosynthesizing genes encoding arginine decarboxylase (SpeA), agmatinase (SpeB), and spermidine synthase (SpeE), were disrupted or overexpressed. Treatment of 0.2mM methylglyoxal and 1mM spermidine led to the elongation and shortening of B. subtilis wild-type cells to 12.38±3.21μm (P<0.05) and 3.24±0.73μm (P<0.01), respectively, compared to untreated cells (5.72±0.68μm). mgsA-deficient (mgsA−) and -overexpressing (mgsAOE) mutants also demonstrated cell shortening and elongation, similar to speB- and speE-deficient (speB− and speE−) and -overexpressing (speBOE and speEOE) mutants. Importantly, both mgsA-depleted speBOE and speEOE mutants (speBOE/mgsA− and speEOE/mgsA−) were drastically shortened to 24.5% and 23.8% of parental speBOE and speEOE mutants, respectively. These phenotypes were associated with reciprocal alterations of mgsA and polyamine transcripts governed by the contents of methylglyoxal and spermidine, which are involved in enzymatic or genetic metabolite-control mechanisms. Additionally, biophysically detected methylglyoxal-spermidine Schiff bases did not affect morphogenesis. Taken together, the findings indicate that methylglyoxal triggers cell elongation. Furthermore, cells with methylglyoxal accumulation commonly exhibit an elongated rod-shaped morphology through upregulation of mgsA, polyamine genes, and the global regulator spx, as well as repression of the cell division and shape regulator, FtsZ.</description><identifier>ISSN: 1357-2725</identifier><identifier>EISSN: 1878-5875</identifier><identifier>DOI: 10.1016/j.biocel.2017.08.005</identifier><identifier>PMID: 28807600</identifier><language>eng</language><publisher>Netherlands: Elsevier Ltd</publisher><subject>Bacillus subtilis ; Bacillus subtilis - cytology ; Bacillus subtilis - drug effects ; Bacillus subtilis - enzymology ; Bacillus subtilis - metabolism ; Carbon-Oxygen Lyases - genetics ; Carbon-Oxygen Lyases - metabolism ; Cell elongation ; Cytoskeleton protein ; Methylglyoxal ; Methylglyoxal synthase ; Pyruvaldehyde - metabolism ; Pyruvaldehyde - pharmacology ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Spermidine ; Spermidine - metabolism ; Spermidine - pharmacology</subject><ispartof>The international journal of biochemistry & cell biology, 2017-10, Vol.91 (Pt A), p.14-28</ispartof><rights>2017 Elsevier Ltd</rights><rights>Copyright © 2017 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c277t-fd9665a88170507fa78bf5ef3177a4bbcf479de4b020643262d600eee4949d803</citedby><cites>FETCH-LOGICAL-c277t-fd9665a88170507fa78bf5ef3177a4bbcf479de4b020643262d600eee4949d803</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.biocel.2017.08.005$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,778,782,3539,27907,27908,45978</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28807600$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shin, Sang-Min</creatorcontrib><creatorcontrib>Song, Sung-Hyun</creatorcontrib><creatorcontrib>Lee, Jin-Woo</creatorcontrib><creatorcontrib>Kwak, Min-Kyu</creatorcontrib><creatorcontrib>Kang, Sa-Ouk</creatorcontrib><title>Methylglyoxal synthase regulates cell elongation via alterations of cellular methylglyoxal and spermidine content in Bacillus subtilis</title><title>The international journal of biochemistry & cell biology</title><addtitle>Int J Biochem Cell Biol</addtitle><description>•Methylglyoxal (MG) stimulates the expression of the gene encoding methylglyoxal synthase (mgsA) in Bacillus subtilis.•MgsA-overexpressing cells show remarkable elongation compared with mgsA-deficient cells.•SpeB and speE, which encode agmatinase and spermidine synthase, respectively, induce MG biosynthesis.•SpeB- and speE-overexpressing cells have an elongated, rod-shaped morphology.•Expression of mgsA and polyamine genes is regulated by clpP-linked spx.
Methylglyoxal regulates cell division and differentiation through its interaction with polyamines. Loss of their biosynthesizing enzyme causes physiological impairment and cell elongation in eukaryotes. However, the reciprocal effects of methylglyoxal and polyamine production and its regulatory metabolic switches on morphological changes in prokaryotes have not been addressed. Here, Bacillus subtilis methylglyoxal synthase (mgsA) and polyamine biosynthesizing genes encoding arginine decarboxylase (SpeA), agmatinase (SpeB), and spermidine synthase (SpeE), were disrupted or overexpressed. Treatment of 0.2mM methylglyoxal and 1mM spermidine led to the elongation and shortening of B. subtilis wild-type cells to 12.38±3.21μm (P<0.05) and 3.24±0.73μm (P<0.01), respectively, compared to untreated cells (5.72±0.68μm). mgsA-deficient (mgsA−) and -overexpressing (mgsAOE) mutants also demonstrated cell shortening and elongation, similar to speB- and speE-deficient (speB− and speE−) and -overexpressing (speBOE and speEOE) mutants. Importantly, both mgsA-depleted speBOE and speEOE mutants (speBOE/mgsA− and speEOE/mgsA−) were drastically shortened to 24.5% and 23.8% of parental speBOE and speEOE mutants, respectively. These phenotypes were associated with reciprocal alterations of mgsA and polyamine transcripts governed by the contents of methylglyoxal and spermidine, which are involved in enzymatic or genetic metabolite-control mechanisms. Additionally, biophysically detected methylglyoxal-spermidine Schiff bases did not affect morphogenesis. Taken together, the findings indicate that methylglyoxal triggers cell elongation. Furthermore, cells with methylglyoxal accumulation commonly exhibit an elongated rod-shaped morphology through upregulation of mgsA, polyamine genes, and the global regulator spx, as well as repression of the cell division and shape regulator, FtsZ.</description><subject>Bacillus subtilis</subject><subject>Bacillus subtilis - cytology</subject><subject>Bacillus subtilis - drug effects</subject><subject>Bacillus subtilis - enzymology</subject><subject>Bacillus subtilis - metabolism</subject><subject>Carbon-Oxygen Lyases - genetics</subject><subject>Carbon-Oxygen Lyases - metabolism</subject><subject>Cell elongation</subject><subject>Cytoskeleton protein</subject><subject>Methylglyoxal</subject><subject>Methylglyoxal synthase</subject><subject>Pyruvaldehyde - metabolism</subject><subject>Pyruvaldehyde - pharmacology</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Spermidine</subject><subject>Spermidine - metabolism</subject><subject>Spermidine - pharmacology</subject><issn>1357-2725</issn><issn>1878-5875</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kctuFDEQRVuIiDzgDxDykk03ZffD7g0SRECQgrJJ1pbbrp545LYH2x1lfoDvxpMJSGxYuSydW7eqblW9pdBQoMOHbTPZoNE1DChvQDQA_YvqjAou6l7w_mWp257XjLP-tDpPaQsAtGftq-qUCQF8ADirfv3AfL93G7cPj8qRtPf5XiUkETerUxkTKRaOoAt-o7INnjxYRZTLGJ--iYT5CSl0JMs_zZQ3JO0wLtZYj0QHn9FnYj35rLQtkkTSOmXrbHpdnczKJXzz_F5Ud1-_3F5e1dc3375ffrquNeM817MZh6FXQlAOPfBZcTHNPc4t5Vx106Tnjo8GuwkYDF3LBmbKlojYjd1oBLQX1ftj310MP1dMWS42HcZXHsOaJB3ZSKEr8oJ2R1THkFLEWe6iXVTcSwrykIDcymMC8pCABCFLAkX27tlhnRY0f0V_Tl6Aj0cAy54PFqNM2qLXaGxEnaUJ9v8OvwEg_pzE</recordid><startdate>201710</startdate><enddate>201710</enddate><creator>Shin, Sang-Min</creator><creator>Song, Sung-Hyun</creator><creator>Lee, Jin-Woo</creator><creator>Kwak, Min-Kyu</creator><creator>Kang, Sa-Ouk</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>201710</creationdate><title>Methylglyoxal synthase regulates cell elongation via alterations of cellular methylglyoxal and spermidine content in Bacillus subtilis</title><author>Shin, Sang-Min ; Song, Sung-Hyun ; Lee, Jin-Woo ; Kwak, Min-Kyu ; Kang, Sa-Ouk</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c277t-fd9665a88170507fa78bf5ef3177a4bbcf479de4b020643262d600eee4949d803</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Bacillus subtilis</topic><topic>Bacillus subtilis - cytology</topic><topic>Bacillus subtilis - drug effects</topic><topic>Bacillus subtilis - enzymology</topic><topic>Bacillus subtilis - metabolism</topic><topic>Carbon-Oxygen Lyases - genetics</topic><topic>Carbon-Oxygen Lyases - metabolism</topic><topic>Cell elongation</topic><topic>Cytoskeleton protein</topic><topic>Methylglyoxal</topic><topic>Methylglyoxal synthase</topic><topic>Pyruvaldehyde - metabolism</topic><topic>Pyruvaldehyde - pharmacology</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Spermidine</topic><topic>Spermidine - metabolism</topic><topic>Spermidine - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shin, Sang-Min</creatorcontrib><creatorcontrib>Song, Sung-Hyun</creatorcontrib><creatorcontrib>Lee, Jin-Woo</creatorcontrib><creatorcontrib>Kwak, Min-Kyu</creatorcontrib><creatorcontrib>Kang, Sa-Ouk</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>The international journal of biochemistry & cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shin, Sang-Min</au><au>Song, Sung-Hyun</au><au>Lee, Jin-Woo</au><au>Kwak, Min-Kyu</au><au>Kang, Sa-Ouk</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Methylglyoxal synthase regulates cell elongation via alterations of cellular methylglyoxal and spermidine content in Bacillus subtilis</atitle><jtitle>The international journal of biochemistry & cell biology</jtitle><addtitle>Int J Biochem Cell Biol</addtitle><date>2017-10</date><risdate>2017</risdate><volume>91</volume><issue>Pt A</issue><spage>14</spage><epage>28</epage><pages>14-28</pages><issn>1357-2725</issn><eissn>1878-5875</eissn><abstract>•Methylglyoxal (MG) stimulates the expression of the gene encoding methylglyoxal synthase (mgsA) in Bacillus subtilis.•MgsA-overexpressing cells show remarkable elongation compared with mgsA-deficient cells.•SpeB and speE, which encode agmatinase and spermidine synthase, respectively, induce MG biosynthesis.•SpeB- and speE-overexpressing cells have an elongated, rod-shaped morphology.•Expression of mgsA and polyamine genes is regulated by clpP-linked spx.
Methylglyoxal regulates cell division and differentiation through its interaction with polyamines. Loss of their biosynthesizing enzyme causes physiological impairment and cell elongation in eukaryotes. However, the reciprocal effects of methylglyoxal and polyamine production and its regulatory metabolic switches on morphological changes in prokaryotes have not been addressed. Here, Bacillus subtilis methylglyoxal synthase (mgsA) and polyamine biosynthesizing genes encoding arginine decarboxylase (SpeA), agmatinase (SpeB), and spermidine synthase (SpeE), were disrupted or overexpressed. Treatment of 0.2mM methylglyoxal and 1mM spermidine led to the elongation and shortening of B. subtilis wild-type cells to 12.38±3.21μm (P<0.05) and 3.24±0.73μm (P<0.01), respectively, compared to untreated cells (5.72±0.68μm). mgsA-deficient (mgsA−) and -overexpressing (mgsAOE) mutants also demonstrated cell shortening and elongation, similar to speB- and speE-deficient (speB− and speE−) and -overexpressing (speBOE and speEOE) mutants. Importantly, both mgsA-depleted speBOE and speEOE mutants (speBOE/mgsA− and speEOE/mgsA−) were drastically shortened to 24.5% and 23.8% of parental speBOE and speEOE mutants, respectively. These phenotypes were associated with reciprocal alterations of mgsA and polyamine transcripts governed by the contents of methylglyoxal and spermidine, which are involved in enzymatic or genetic metabolite-control mechanisms. Additionally, biophysically detected methylglyoxal-spermidine Schiff bases did not affect morphogenesis. Taken together, the findings indicate that methylglyoxal triggers cell elongation. Furthermore, cells with methylglyoxal accumulation commonly exhibit an elongated rod-shaped morphology through upregulation of mgsA, polyamine genes, and the global regulator spx, as well as repression of the cell division and shape regulator, FtsZ.</abstract><cop>Netherlands</cop><pub>Elsevier Ltd</pub><pmid>28807600</pmid><doi>10.1016/j.biocel.2017.08.005</doi><tpages>15</tpages></addata></record> |
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| subjects | Bacillus subtilis Bacillus subtilis - cytology Bacillus subtilis - drug effects Bacillus subtilis - enzymology Bacillus subtilis - metabolism Carbon-Oxygen Lyases - genetics Carbon-Oxygen Lyases - metabolism Cell elongation Cytoskeleton protein Methylglyoxal Methylglyoxal synthase Pyruvaldehyde - metabolism Pyruvaldehyde - pharmacology RNA, Messenger - genetics RNA, Messenger - metabolism Spermidine Spermidine - metabolism Spermidine - pharmacology |
| title | Methylglyoxal synthase regulates cell elongation via alterations of cellular methylglyoxal and spermidine content in Bacillus subtilis |
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