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Natural combinatorial genetics and prolific polyamine production enable siderophore diversification in Serratia plymuthica

BACKGROUND: Iron is essential for bacterial survival. Bacterial siderophores are small molecules with unmatched capacity to scavenge iron from proteins and the extracellular milieu, where it mostly occurs as insoluble Fe(3+). Siderophores chelate Fe(3+) for uptake into the cell, where it is reduced...

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Autores principales: Cleto, Sara, Haslinger, Kristina, Prather, Kristala L. J., Lu, Timothy K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7962358/
https://www.ncbi.nlm.nih.gov/pubmed/33722216
http://dx.doi.org/10.1186/s12915-021-00971-z
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author Cleto, Sara
Haslinger, Kristina
Prather, Kristala L. J.
Lu, Timothy K.
author_facet Cleto, Sara
Haslinger, Kristina
Prather, Kristala L. J.
Lu, Timothy K.
author_sort Cleto, Sara
collection PubMed
description BACKGROUND: Iron is essential for bacterial survival. Bacterial siderophores are small molecules with unmatched capacity to scavenge iron from proteins and the extracellular milieu, where it mostly occurs as insoluble Fe(3+). Siderophores chelate Fe(3+) for uptake into the cell, where it is reduced to soluble Fe(2+). Siderophores are key molecules in low soluble iron conditions. The ability of bacteria to synthesize proprietary siderophores may have increased bacterial evolutionary fitness; one way that bacteria diversify siderophore structure is by incorporating different polyamine backbones while maintaining the catechol moieties. RESULTS: We report that Serratia plymuthica V4 produces a variety of siderophores, which we term the siderome, and which are assembled by the concerted action of enzymes encoded in two independent gene clusters. Besides assembling serratiochelin A and B with diaminopropane, S. plymuthica utilizes putrescine and the same set of enzymes to assemble photobactin, a siderophore found in the bacterium Photorhabdus luminescens. The enzymes encoded by one of the gene clusters can independently assemble enterobactin. A third, independent operon is responsible for biosynthesis of the hydroxamate siderophore aerobactin, initially described in Enterobacter aerogenes. Mutant strains not synthesizing polyamine-siderophores significantly increased enterobactin production levels, though lack of enterobactin did not impact the production of serratiochelins. Knocking out SchF0, an enzyme involved in the assembly of enterobactin alone, significantly reduced bacterial fitness. CONCLUSIONS: This study shows the natural occurrence of serratiochelins, photobactin, enterobactin, and aerobactin in a single bacterial species and illuminates the interplay between siderophore biosynthetic pathways and polyamine production, indicating routes of molecular diversification. Given its natural yields of diaminopropane (97.75 μmol/g DW) and putrescine (30.83 μmol/g DW), S. plymuthica can be exploited for the industrial production of these compounds. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-00971-z.
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spelling pubmed-79623582021-03-16 Natural combinatorial genetics and prolific polyamine production enable siderophore diversification in Serratia plymuthica Cleto, Sara Haslinger, Kristina Prather, Kristala L. J. Lu, Timothy K. BMC Biol Research Article BACKGROUND: Iron is essential for bacterial survival. Bacterial siderophores are small molecules with unmatched capacity to scavenge iron from proteins and the extracellular milieu, where it mostly occurs as insoluble Fe(3+). Siderophores chelate Fe(3+) for uptake into the cell, where it is reduced to soluble Fe(2+). Siderophores are key molecules in low soluble iron conditions. The ability of bacteria to synthesize proprietary siderophores may have increased bacterial evolutionary fitness; one way that bacteria diversify siderophore structure is by incorporating different polyamine backbones while maintaining the catechol moieties. RESULTS: We report that Serratia plymuthica V4 produces a variety of siderophores, which we term the siderome, and which are assembled by the concerted action of enzymes encoded in two independent gene clusters. Besides assembling serratiochelin A and B with diaminopropane, S. plymuthica utilizes putrescine and the same set of enzymes to assemble photobactin, a siderophore found in the bacterium Photorhabdus luminescens. The enzymes encoded by one of the gene clusters can independently assemble enterobactin. A third, independent operon is responsible for biosynthesis of the hydroxamate siderophore aerobactin, initially described in Enterobacter aerogenes. Mutant strains not synthesizing polyamine-siderophores significantly increased enterobactin production levels, though lack of enterobactin did not impact the production of serratiochelins. Knocking out SchF0, an enzyme involved in the assembly of enterobactin alone, significantly reduced bacterial fitness. CONCLUSIONS: This study shows the natural occurrence of serratiochelins, photobactin, enterobactin, and aerobactin in a single bacterial species and illuminates the interplay between siderophore biosynthetic pathways and polyamine production, indicating routes of molecular diversification. Given its natural yields of diaminopropane (97.75 μmol/g DW) and putrescine (30.83 μmol/g DW), S. plymuthica can be exploited for the industrial production of these compounds. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-00971-z. BioMed Central 2021-03-15 /pmc/articles/PMC7962358/ /pubmed/33722216 http://dx.doi.org/10.1186/s12915-021-00971-z Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Cleto, Sara
Haslinger, Kristina
Prather, Kristala L. J.
Lu, Timothy K.
Natural combinatorial genetics and prolific polyamine production enable siderophore diversification in Serratia plymuthica
title Natural combinatorial genetics and prolific polyamine production enable siderophore diversification in Serratia plymuthica
title_full Natural combinatorial genetics and prolific polyamine production enable siderophore diversification in Serratia plymuthica
title_fullStr Natural combinatorial genetics and prolific polyamine production enable siderophore diversification in Serratia plymuthica
title_full_unstemmed Natural combinatorial genetics and prolific polyamine production enable siderophore diversification in Serratia plymuthica
title_short Natural combinatorial genetics and prolific polyamine production enable siderophore diversification in Serratia plymuthica
title_sort natural combinatorial genetics and prolific polyamine production enable siderophore diversification in serratia plymuthica
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7962358/
https://www.ncbi.nlm.nih.gov/pubmed/33722216
http://dx.doi.org/10.1186/s12915-021-00971-z
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