Ferrichrome, a fungal-type siderophore, confers high ammonium tolerance to fission yeast
Abstract Microorganisms and plants produce siderophores, which function to transport environmental iron into cells as well as participate in cellular iron use and deposition. Their biological functions are diverse although their role in primary metabolism is poorly understood. Ferrichrome is a funga...
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Nature Portfolio
2022-10-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-022-22108-0 |
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| author | Po-Chang Chiu Yuri Nakamura Shinichi Nishimura Toshitsugu Tabuchi Yoko Yashiroda Go Hirai Akihisa Matsuyama Minoru Yoshida |
| author_facet | Po-Chang Chiu Yuri Nakamura Shinichi Nishimura Toshitsugu Tabuchi Yoko Yashiroda Go Hirai Akihisa Matsuyama Minoru Yoshida |
| author_sort | Po-Chang Chiu |
| collection | DOAJ |
| description | Abstract Microorganisms and plants produce siderophores, which function to transport environmental iron into cells as well as participate in cellular iron use and deposition. Their biological functions are diverse although their role in primary metabolism is poorly understood. Ferrichrome is a fungal-type siderophore synthesized by nonribosomal peptide synthetase (NRPS). Herein we show that ferrichrome induces adaptive growth of fission yeast on high ammonium media. Ammonium is a preferred nitrogen source as it suppresses uptake and catabolism of less preferred nitrogen sources such as leucine through a mechanism called nitrogen catabolite repression (NCR). Therefore, the growth of fission yeast mutant cells with leucine auxotrophy is suppressed in the presence of high concentrations of ammonium. This growth suppression was canceled by ferrichrome in a manner dependent on the amino acid transporter Cat1. Additionally, growth retardation of wild-type cells by excess ammonium was exacerbated by deleting the NRPS gene sib1, which is responsible for the biosynthesis of ferrichrome, suggesting that intrinsically produced ferrichrome functions in suppressing the metabolic action of ammonium. Furthermore, ferrichrome facilitated the growth of both wild-type and sib1-deficient cells under low glucose conditions. These results suggest that intracellular iron regulates primary metabolism, including NCR, which is mediated by siderophores. |
| format | Article |
| id | doaj-art-f8b31ac44cb9474fb85f3aa1151e56de |
| institution | Kabale University |
| issn | 2045-2322 |
| language | English |
| publishDate | 2022-10-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj-art-f8b31ac44cb9474fb85f3aa1151e56de2025-02-02T12:25:37ZengNature PortfolioScientific Reports2045-23222022-10-0112111010.1038/s41598-022-22108-0Ferrichrome, a fungal-type siderophore, confers high ammonium tolerance to fission yeastPo-Chang Chiu0Yuri Nakamura1Shinichi Nishimura2Toshitsugu Tabuchi3Yoko Yashiroda4Go Hirai5Akihisa Matsuyama6Minoru Yoshida7Department of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of TokyoDepartment of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of TokyoDepartment of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of TokyoDepartment of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of TokyoRIKEN Center for Sustainable Resource ScienceRIKEN Center for Sustainable Resource ScienceDepartment of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of TokyoDepartment of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of TokyoAbstract Microorganisms and plants produce siderophores, which function to transport environmental iron into cells as well as participate in cellular iron use and deposition. Their biological functions are diverse although their role in primary metabolism is poorly understood. Ferrichrome is a fungal-type siderophore synthesized by nonribosomal peptide synthetase (NRPS). Herein we show that ferrichrome induces adaptive growth of fission yeast on high ammonium media. Ammonium is a preferred nitrogen source as it suppresses uptake and catabolism of less preferred nitrogen sources such as leucine through a mechanism called nitrogen catabolite repression (NCR). Therefore, the growth of fission yeast mutant cells with leucine auxotrophy is suppressed in the presence of high concentrations of ammonium. This growth suppression was canceled by ferrichrome in a manner dependent on the amino acid transporter Cat1. Additionally, growth retardation of wild-type cells by excess ammonium was exacerbated by deleting the NRPS gene sib1, which is responsible for the biosynthesis of ferrichrome, suggesting that intrinsically produced ferrichrome functions in suppressing the metabolic action of ammonium. Furthermore, ferrichrome facilitated the growth of both wild-type and sib1-deficient cells under low glucose conditions. These results suggest that intracellular iron regulates primary metabolism, including NCR, which is mediated by siderophores.https://doi.org/10.1038/s41598-022-22108-0 |
| spellingShingle | Po-Chang Chiu Yuri Nakamura Shinichi Nishimura Toshitsugu Tabuchi Yoko Yashiroda Go Hirai Akihisa Matsuyama Minoru Yoshida Ferrichrome, a fungal-type siderophore, confers high ammonium tolerance to fission yeast Scientific Reports |
| title | Ferrichrome, a fungal-type siderophore, confers high ammonium tolerance to fission yeast |
| title_full | Ferrichrome, a fungal-type siderophore, confers high ammonium tolerance to fission yeast |
| title_fullStr | Ferrichrome, a fungal-type siderophore, confers high ammonium tolerance to fission yeast |
| title_full_unstemmed | Ferrichrome, a fungal-type siderophore, confers high ammonium tolerance to fission yeast |
| title_short | Ferrichrome, a fungal-type siderophore, confers high ammonium tolerance to fission yeast |
| title_sort | ferrichrome a fungal type siderophore confers high ammonium tolerance to fission yeast |
| url | https://doi.org/10.1038/s41598-022-22108-0 |
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