Carboxythiazole is a key microbial nutrient currency and critical component of thiamin biosynthesis

Ryan W. Paerl; Erin M. Bertrand; Elden Rowland; Phillippe Schatt; Mohamed Mehiri; Thomas D. Niehaus; Andrew D. Hanson; Lasse Riemann; Francois Yves-Bouget

doi:10.1038/s41598-018-24321-2

Carboxythiazole is a key microbial nutrient currency and critical component of thiamin biosynthesis

Ryan W. Paerl, Erin M. Bertrand, Elden Rowland, Phillippe Schatt, Mohamed Mehiri, Thomas D. Niehaus, Andrew D. Hanson, Lasse Riemann, Francois Yves-Bouget

Medicine

Résultat de recherche: Article › examen par les pairs

22 Citations (Scopus)

Résumé

Almost all cells require thiamin, vitamin B1 (B1), which is synthesized via the coupling of thiazole and pyrimidine precursors. Here we demonstrate that 5-(2-hydroxyethyl)-4-methyl-1,3-thiazole-2-carboxylic acid (cHET) is a useful in vivo B1 precursor for representatives of ubiquitous marine picoeukaryotic phytoplankton and Escherichia coli - drawing attention to cHET as a valuable exogenous micronutrient for microorganisms with ecological, industrial, and biomedical value. Comparative utilization experiments with the terrestrial plant Arabidopsis thaliana revealed that it can also use exogenous cHET, but notably, picoeukaryotic marine phytoplankton and E. coli were adapted to grow on low (picomolar) concentrations of exogenous cHET. Our results call for the modification of the conventional B1 biosynthesis model to incorporate cHET as a key precursor for B1 biosynthesis in two domains of life, and for consideration of cHET as a microbial micronutrient currency modulating marine primary productivity and community interactions in human gut-hosted microbiomes.

Langue d'origine	English
Numéro d'article	5940
Journal	Scientific Reports
Volume	8
Numéro de publication	1
DOI	https://doi.org/10.1038/s41598-018-24321-2
Statut de publication	Published - déc. 1 2018

Note bibliographique

Funding Information:
Thanks are extended to S. Svenningsen for providing E. coli JW5549 ΔthiG761::kan, C. Kachuk for technical assistance, and H. Paerl for comments on the manuscript. This research was supported by the BONUS Blueprint project that has received funding from BONUS, the joint Baltic Sea research and development programme (Art 185), funded jointly from the European Union's Seventh Programme for research, technological development and demonstration, and the Danish Council for Strategic Research (LR). Additional funding was provided by the French Agence Nationale de la recherche (Photo-Phyto, ANR-14-CE02-0018) (FYB), and the projet d'investissement d'Avenir UCAJEDI ANR-15-IDEX-01 (MM), NSERC grant 950-230440 (EMB), and NSF award IOS-1444202 (ADH).

Funding Information:
Thanks are extended to S. Svenningsen for providing E. coli JW5549 ΔthiG761::kan, C. Kachuk for technical assistance, and H. Paerl for comments on the manuscript. This research was supported by the BONUS Blueprint project that has received funding from BONUS, the joint Baltic Sea research and development programme (Art 185), funded jointly from the European Union’s Seventh Programme for research, technological development and demonstration, and the Danish Council for Strategic Research (LR). Additional funding was provided by the French Agence Nationale de la recherche (Photo-Phyto, ANR-14-CE02-0018) (FYB), and the projet d’investissement d’Avenir UCAJEDIANR-15-IDEX-01 (MM), NSERC grant 950-230440 (EMB), and NSF award IOS-1444202 (ADH).

Publisher Copyright:
© 2018 The Author(s).

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Cette action contribue à la réalisation des objectifs de développement durable suivants

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10.1038/s41598-018-24321-2

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abstract = "Almost all cells require thiamin, vitamin B1 (B1), which is synthesized via the coupling of thiazole and pyrimidine precursors. Here we demonstrate that 5-(2-hydroxyethyl)-4-methyl-1,3-thiazole-2-carboxylic acid (cHET) is a useful in vivo B1 precursor for representatives of ubiquitous marine picoeukaryotic phytoplankton and Escherichia coli - drawing attention to cHET as a valuable exogenous micronutrient for microorganisms with ecological, industrial, and biomedical value. Comparative utilization experiments with the terrestrial plant Arabidopsis thaliana revealed that it can also use exogenous cHET, but notably, picoeukaryotic marine phytoplankton and E. coli were adapted to grow on low (picomolar) concentrations of exogenous cHET. Our results call for the modification of the conventional B1 biosynthesis model to incorporate cHET as a key precursor for B1 biosynthesis in two domains of life, and for consideration of cHET as a microbial micronutrient currency modulating marine primary productivity and community interactions in human gut-hosted microbiomes.",

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note = "Funding Information: Thanks are extended to S. Svenningsen for providing E. coli JW5549 ΔthiG761::kan, C. Kachuk for technical assistance, and H. Paerl for comments on the manuscript. This research was supported by the BONUS Blueprint project that has received funding from BONUS, the joint Baltic Sea research and development programme (Art 185), funded jointly from the European Union's Seventh Programme for research, technological development and demonstration, and the Danish Council for Strategic Research (LR). Additional funding was provided by the French Agence Nationale de la recherche (Photo-Phyto, ANR-14-CE02-0018) (FYB), and the projet d'investissement d'Avenir UCAJEDI ANR-15-IDEX-01 (MM), NSERC grant 950-230440 (EMB), and NSF award IOS-1444202 (ADH). Funding Information: Thanks are extended to S. Svenningsen for providing E. coli JW5549 ΔthiG761::kan, C. Kachuk for technical assistance, and H. Paerl for comments on the manuscript. This research was supported by the BONUS Blueprint project that has received funding from BONUS, the joint Baltic Sea research and development programme (Art 185), funded jointly from the European Union{\textquoteright}s Seventh Programme for research, technological development and demonstration, and the Danish Council for Strategic Research (LR). Additional funding was provided by the French Agence Nationale de la recherche (Photo-Phyto, ANR-14-CE02-0018) (FYB), and the projet d{\textquoteright}investissement d{\textquoteright}Avenir UCAJEDIANR-15-IDEX-01 (MM), NSERC grant 950-230440 (EMB), and NSF award IOS-1444202 (ADH). Publisher Copyright: {\textcopyright} 2018 The Author(s).",

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AU - Mehiri, Mohamed

AU - Niehaus, Thomas D.

AU - Hanson, Andrew D.

AU - Riemann, Lasse

AU - Yves-Bouget, Francois

N1 - Funding Information: Thanks are extended to S. Svenningsen for providing E. coli JW5549 ΔthiG761::kan, C. Kachuk for technical assistance, and H. Paerl for comments on the manuscript. This research was supported by the BONUS Blueprint project that has received funding from BONUS, the joint Baltic Sea research and development programme (Art 185), funded jointly from the European Union's Seventh Programme for research, technological development and demonstration, and the Danish Council for Strategic Research (LR). Additional funding was provided by the French Agence Nationale de la recherche (Photo-Phyto, ANR-14-CE02-0018) (FYB), and the projet d'investissement d'Avenir UCAJEDI ANR-15-IDEX-01 (MM), NSERC grant 950-230440 (EMB), and NSF award IOS-1444202 (ADH). Funding Information: Thanks are extended to S. Svenningsen for providing E. coli JW5549 ΔthiG761::kan, C. Kachuk for technical assistance, and H. Paerl for comments on the manuscript. This research was supported by the BONUS Blueprint project that has received funding from BONUS, the joint Baltic Sea research and development programme (Art 185), funded jointly from the European Union’s Seventh Programme for research, technological development and demonstration, and the Danish Council for Strategic Research (LR). Additional funding was provided by the French Agence Nationale de la recherche (Photo-Phyto, ANR-14-CE02-0018) (FYB), and the projet d’investissement d’Avenir UCAJEDIANR-15-IDEX-01 (MM), NSERC grant 950-230440 (EMB), and NSF award IOS-1444202 (ADH). Publisher Copyright: © 2018 The Author(s).

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N2 - Almost all cells require thiamin, vitamin B1 (B1), which is synthesized via the coupling of thiazole and pyrimidine precursors. Here we demonstrate that 5-(2-hydroxyethyl)-4-methyl-1,3-thiazole-2-carboxylic acid (cHET) is a useful in vivo B1 precursor for representatives of ubiquitous marine picoeukaryotic phytoplankton and Escherichia coli - drawing attention to cHET as a valuable exogenous micronutrient for microorganisms with ecological, industrial, and biomedical value. Comparative utilization experiments with the terrestrial plant Arabidopsis thaliana revealed that it can also use exogenous cHET, but notably, picoeukaryotic marine phytoplankton and E. coli were adapted to grow on low (picomolar) concentrations of exogenous cHET. Our results call for the modification of the conventional B1 biosynthesis model to incorporate cHET as a key precursor for B1 biosynthesis in two domains of life, and for consideration of cHET as a microbial micronutrient currency modulating marine primary productivity and community interactions in human gut-hosted microbiomes.

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Carboxythiazole is a key microbial nutrient currency and critical component of thiamin biosynthesis

Résumé

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ASJC Scopus Subject Areas

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