First Betalain-Producing Bacteria Break the Exclusive Presence of the Pigments in the Plant Kingdom

ABSTRACT The biosynthesis of antioxidant pigments, namely, betalains, was believed to be restricted to Caryophyllales plants. This paper changes this paradigm, and enzyme mining from bacterial hosts promoted the discovery of bacterial cultures producing betalains. The spectrum of possible sources of...

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Autores principales:	Luis Eduardo Contreras-Llano, M. Alejandra Guerrero-Rubio, José Daniel Lozada-Ramírez, Francisco García-Carmona, Fernando Gandía-Herrero
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	betalains betalamic acid dioxygenase enzyme mining pigments Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/da58f584fd8b437b91e4e984bedb6072
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spelling	oai:doaj.org-article:da58f584fd8b437b91e4e984bedb60722021-11-15T15:55:26ZFirst Betalain-Producing Bacteria Break the Exclusive Presence of the Pigments in the Plant Kingdom10.1128/mBio.00345-192150-7511https://doaj.org/article/da58f584fd8b437b91e4e984bedb60722019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00345-19https://doaj.org/toc/2150-7511ABSTRACT The biosynthesis of antioxidant pigments, namely, betalains, was believed to be restricted to Caryophyllales plants. This paper changes this paradigm, and enzyme mining from bacterial hosts promoted the discovery of bacterial cultures producing betalains. The spectrum of possible sources of betalain pigments in nature is broadened by our description of the first betalain-forming bacterium, Gluconacetobacter diazotrophicus. The enzyme-specific step is the extradiol cleavage of the precursor amino acid l-dihydroxyphenylalanine (l-DOPA) to form the structural unit betalamic acid. Molecular and functional work conducted led to the characterization of a novel dioxygenase, a polypeptide of 17.8 kDa with a Km of 1.36 mM, with higher activity and affinity than those of its plant counterparts. Its superior activity allowed the first experimental characterization of the early steps in the biosynthesis of betalains by fully characterizing the presence and time evolution of 2,3- and 4,5-seco-DOPA intermediates. Furthermore, spontaneous chemical reactions are characterized and incorporated into a comprehensive enzymatic-chemical mechanism that yields the final pigments. IMPORTANCE Several studies have demonstrated the health-promoting effects of betalains due to their high antioxidant capacity and their positive effect on the dose-dependent inhibition of cancer cells and their proliferation. To date, betalains were restricted to plants of the order Caryophyllales and some species of fungi, but the present study reveals the first betalain-producing bacterium, as well as the first steps in the formation of pigments. This finding demonstrates that betalain biosynthesis can be expanded to prokaryotes.Luis Eduardo Contreras-LlanoM. Alejandra Guerrero-RubioJosé Daniel Lozada-RamírezFrancisco García-CarmonaFernando Gandía-HerreroAmerican Society for Microbiologyarticlebetalainsbetalamic aciddioxygenaseenzyme miningpigmentsMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	betalains betalamic acid dioxygenase enzyme mining pigments Microbiology QR1-502
spellingShingle	betalains betalamic acid dioxygenase enzyme mining pigments Microbiology QR1-502 Luis Eduardo Contreras-Llano M. Alejandra Guerrero-Rubio José Daniel Lozada-Ramírez Francisco García-Carmona Fernando Gandía-Herrero First Betalain-Producing Bacteria Break the Exclusive Presence of the Pigments in the Plant Kingdom
description	ABSTRACT The biosynthesis of antioxidant pigments, namely, betalains, was believed to be restricted to Caryophyllales plants. This paper changes this paradigm, and enzyme mining from bacterial hosts promoted the discovery of bacterial cultures producing betalains. The spectrum of possible sources of betalain pigments in nature is broadened by our description of the first betalain-forming bacterium, Gluconacetobacter diazotrophicus. The enzyme-specific step is the extradiol cleavage of the precursor amino acid l-dihydroxyphenylalanine (l-DOPA) to form the structural unit betalamic acid. Molecular and functional work conducted led to the characterization of a novel dioxygenase, a polypeptide of 17.8 kDa with a Km of 1.36 mM, with higher activity and affinity than those of its plant counterparts. Its superior activity allowed the first experimental characterization of the early steps in the biosynthesis of betalains by fully characterizing the presence and time evolution of 2,3- and 4,5-seco-DOPA intermediates. Furthermore, spontaneous chemical reactions are characterized and incorporated into a comprehensive enzymatic-chemical mechanism that yields the final pigments. IMPORTANCE Several studies have demonstrated the health-promoting effects of betalains due to their high antioxidant capacity and their positive effect on the dose-dependent inhibition of cancer cells and their proliferation. To date, betalains were restricted to plants of the order Caryophyllales and some species of fungi, but the present study reveals the first betalain-producing bacterium, as well as the first steps in the formation of pigments. This finding demonstrates that betalain biosynthesis can be expanded to prokaryotes.
format	article
author	Luis Eduardo Contreras-Llano M. Alejandra Guerrero-Rubio José Daniel Lozada-Ramírez Francisco García-Carmona Fernando Gandía-Herrero
author_facet	Luis Eduardo Contreras-Llano M. Alejandra Guerrero-Rubio José Daniel Lozada-Ramírez Francisco García-Carmona Fernando Gandía-Herrero
author_sort	Luis Eduardo Contreras-Llano
title	First Betalain-Producing Bacteria Break the Exclusive Presence of the Pigments in the Plant Kingdom
title_short	First Betalain-Producing Bacteria Break the Exclusive Presence of the Pigments in the Plant Kingdom
title_full	First Betalain-Producing Bacteria Break the Exclusive Presence of the Pigments in the Plant Kingdom
title_fullStr	First Betalain-Producing Bacteria Break the Exclusive Presence of the Pigments in the Plant Kingdom
title_full_unstemmed	First Betalain-Producing Bacteria Break the Exclusive Presence of the Pigments in the Plant Kingdom
title_sort	first betalain-producing bacteria break the exclusive presence of the pigments in the plant kingdom
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/da58f584fd8b437b91e4e984bedb6072
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First Betalain-Producing Bacteria Break the Exclusive Presence of the Pigments in the Plant Kingdom

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