Control of pili synthesis and putrescine homeostasis in Escherichia coli
Polyamines are biologically ubiquitous cations that bind to nucleic acids, ribosomes, and phospholipids and, thereby, modulate numerous processes, including surface motility in Escherichia coli. We characterized the metabolic pathways that contribute to polyamine-dependent control of surface motilit...
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eLife Sciences Publications Ltd
2025-04-01
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| Online Access: | https://elifesciences.org/articles/102439 |
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| author | Iti Mehta Jacob B Hogins Sydney R Hall Gabrielle Vragel Sankalya Ambagaspitiye Philippe E Zimmern Larry Reitzer |
| author_facet | Iti Mehta Jacob B Hogins Sydney R Hall Gabrielle Vragel Sankalya Ambagaspitiye Philippe E Zimmern Larry Reitzer |
| author_sort | Iti Mehta |
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| description | Polyamines are biologically ubiquitous cations that bind to nucleic acids, ribosomes, and phospholipids and, thereby, modulate numerous processes, including surface motility in Escherichia coli. We characterized the metabolic pathways that contribute to polyamine-dependent control of surface motility in the commonly used strain W3110 and the transcriptome of a mutant lacking a putrescine synthetic pathway that was required for surface motility. Genetic analysis showed that surface motility required type 1 pili, the simultaneous presence of two independent putrescine anabolic pathways, and modulation by putrescine transport and catabolism. An immunological assay for FimA—the major pili subunit, reverse transcription quantitative PCR of fimA, and transmission electron microscopy confirmed that pili synthesis required putrescine. Comparative RNAseq analysis of a wild type and ΔspeB mutant which exhibits impaired pili synthesis showed that the latter had fewer transcripts for pili structural genes and for fimB which codes for the phase variation recombinase that orients the fim operon promoter in the ON phase, although loss of speB did not affect the promoter orientation. Results from the RNAseq analysis also suggested (a) changes in transcripts for several transcription factor genes that affect fim operon expression, (b) compensatory mechanisms for low putrescine which implies a putrescine homeostatic network, and (c) decreased transcripts of genes for oxidative energy metabolism and iron transport which a previous genetic analysis suggests may be sufficient to account for the pili defect in putrescine synthesis mutants. We conclude that pili synthesis requires putrescine and putrescine concentration is controlled by a complex homeostatic network that includes the genes of oxidative energy metabolism. |
| format | Article |
| id | doaj-art-eaf4b6e2e29c4257b88b995e4151dc73 |
| institution | DOAJ |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-04-01 |
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| spelling | doaj-art-eaf4b6e2e29c4257b88b995e4151dc732025-08-20T03:16:50ZengeLife Sciences Publications LtdeLife2050-084X2025-04-011310.7554/eLife.102439Control of pili synthesis and putrescine homeostasis in Escherichia coliIti Mehta0Jacob B Hogins1https://orcid.org/0000-0001-6041-7332Sydney R Hall2Gabrielle Vragel3Sankalya Ambagaspitiye4Philippe E Zimmern5Larry Reitzer6https://orcid.org/0000-0002-4406-6090Department of Biological Sciences, The University of Texas at Dallas, Richardson, United StatesDepartment of Biological Sciences, The University of Texas at Dallas, Richardson, United StatesDepartment of Biological Sciences, The University of Texas at Dallas, Richardson, United StatesDepartment of Biological Sciences, The University of Texas at Dallas, Richardson, United StatesDepartment of Biological Sciences, The University of Texas at Dallas, Richardson, United StatesDepartment of Urology, University of Texas Southwestern Medical Center, Dallas, United StatesDepartment of Biological Sciences, The University of Texas at Dallas, Richardson, United StatesPolyamines are biologically ubiquitous cations that bind to nucleic acids, ribosomes, and phospholipids and, thereby, modulate numerous processes, including surface motility in Escherichia coli. We characterized the metabolic pathways that contribute to polyamine-dependent control of surface motility in the commonly used strain W3110 and the transcriptome of a mutant lacking a putrescine synthetic pathway that was required for surface motility. Genetic analysis showed that surface motility required type 1 pili, the simultaneous presence of two independent putrescine anabolic pathways, and modulation by putrescine transport and catabolism. An immunological assay for FimA—the major pili subunit, reverse transcription quantitative PCR of fimA, and transmission electron microscopy confirmed that pili synthesis required putrescine. Comparative RNAseq analysis of a wild type and ΔspeB mutant which exhibits impaired pili synthesis showed that the latter had fewer transcripts for pili structural genes and for fimB which codes for the phase variation recombinase that orients the fim operon promoter in the ON phase, although loss of speB did not affect the promoter orientation. Results from the RNAseq analysis also suggested (a) changes in transcripts for several transcription factor genes that affect fim operon expression, (b) compensatory mechanisms for low putrescine which implies a putrescine homeostatic network, and (c) decreased transcripts of genes for oxidative energy metabolism and iron transport which a previous genetic analysis suggests may be sufficient to account for the pili defect in putrescine synthesis mutants. We conclude that pili synthesis requires putrescine and putrescine concentration is controlled by a complex homeostatic network that includes the genes of oxidative energy metabolism.https://elifesciences.org/articles/102439polyaminespilitranscriptomicsgene regulationputrescine homeostasissurface motility |
| spellingShingle | Iti Mehta Jacob B Hogins Sydney R Hall Gabrielle Vragel Sankalya Ambagaspitiye Philippe E Zimmern Larry Reitzer Control of pili synthesis and putrescine homeostasis in Escherichia coli eLife polyamines pili transcriptomics gene regulation putrescine homeostasis surface motility |
| title | Control of pili synthesis and putrescine homeostasis in Escherichia coli |
| title_full | Control of pili synthesis and putrescine homeostasis in Escherichia coli |
| title_fullStr | Control of pili synthesis and putrescine homeostasis in Escherichia coli |
| title_full_unstemmed | Control of pili synthesis and putrescine homeostasis in Escherichia coli |
| title_short | Control of pili synthesis and putrescine homeostasis in Escherichia coli |
| title_sort | control of pili synthesis and putrescine homeostasis in escherichia coli |
| topic | polyamines pili transcriptomics gene regulation putrescine homeostasis surface motility |
| url | https://elifesciences.org/articles/102439 |
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