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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 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.

SUBMITTER: Contreras-Llano LE

PROVIDER: S-EPMC6426604 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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

Contreras-Llano Luis Eduardo LE Guerrero-Rubio M Alejandra MA Lozada-Ramírez José Daniel JD García-Carmona Francisco F Gandía-Herrero Fernando F

mBio 20190319 2

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, <i>Gluconacetobacter diazotrophicus</i> The enzyme-specific step is the extradiol cleavage of the precursor ...[more]

PMID: 30890610

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Project description:BACKGROUND: Carotenoids and anthocyanins are the predominant non-chlorophyll pigments in plants. However, certain families within the order Caryophyllales produce another class of pigments, the betalains, instead of anthocyanins. The occurrence of betalains and anthocyanins is mutually exclusive. Betalains are divided into two classes, the betaxanthins and betacyanins, which produce yellow to orange or violet colours, respectively. In this article we show betalain production in species that normally produce anthocyanins, through a combination of genetic modification and substrate feeding. RESULTS: The biolistic introduction of DNA constructs for transient overexpression of two different dihydroxyphenylalanine (DOPA) dioxygenases (DODs), and feeding of DOD substrate (L-DOPA), was sufficient to induce betalain production in cell cultures of Solanum tuberosum (potato) and petals of Antirrhinum majus. HPLC analysis showed both betaxanthins and betacyanins were produced. Multi-cell foci with yellow, orange and/or red colours occurred, with either a fungal DOD (from Amanita muscaria) or a plant DOD (from Portulaca grandiflora), and the yellow/orange foci showed green autofluorescence characteristic of betaxanthins. Stably transformed Arabidopsis thaliana (arabidopsis) lines containing 35S: AmDOD produced yellow colouration in flowers and orange-red colouration in seedlings when fed L-DOPA. These tissues also showed green autofluorescence. HPLC analysis of the transgenic seedlings fed L-DOPA confirmed betaxanthin production. CONCLUSIONS: The fact that the introduction of DOD along with a supply of its substrate (L-DOPA) was sufficient to induce betacyanin production reveals the presence of a background enzyme, possibly a tyrosinase, that can convert L-DOPA to cyclo-DOPA (or dopaxanthin to betacyanin) in at least some anthocyanin-producing plants. The plants also demonstrate that betalains can accumulate in anthocyanin-producing species. Thus, introduction of a DOD and an enzyme capable of converting tyrosine to L-DOPA should be sufficient to confer both betaxanthin and betacyanin production to anthocyanin-producing species. The requirement for few novel biosynthetic steps may have assisted in the evolution of the betalain biosynthetic pathway in the Caryophyllales, and facilitated multiple origins of the pathway in this order and in fungi. The stably transformed 35S: AmDOD arabidopsis plants provide material to study, for the first time, the physiological effects of having both betalains and anthocyanins in the same plant tissues.

Project description:Twelve species of Hypomyces/Cladobotryum producing red pigments are reported growing in various tropical areas of the world. Ten of these are described as new, including teleomorphs for two previously known anamorphic species. In two species the teleomorph has been found in nature and in three others it was obtained in culture; only anamorphs are known for the rest. None of the studied tropical collections belongs to the common temperate species H. rosellus and H. odoratus to which the tropical teleomorphic collections had previously been assigned. Instead, taxa encountered in the tropics are genetically and morphologically distinct from the nine species of Hypomyces/Cladobotryum producing red pigments known from temperate regions. Besides observed host preferences, anamorphs of several species can spread fast on soft ephemeral agaricoid basidiomata but the slower developing teleomorphs are mostly found on polyporoid basidiomata or bark. While a majority of previous records from the tropics involve collections from Central America, this paper also reports the diversity of these fungi in the Paleotropics. Africa appears to hold a variety of taxa as five of the new species include material collected in scattered localities of this mostly unexplored continent. In examining distribution patterns, most of the taxa do not appear to be pantropical. Some species are known only from the Western Hemisphere, while others have a geographic range from southeastern Asia to Africa or Australia. The use of various morphological characters of anamorphs and teleomorphs as well as culture characteristics in species delimitation is evaluated. For detecting genetic segregation, partial sequences of the two largest subunits of the ribosomal polymerase perform the best in terms of providing informative sites and the number of well-supported groups recognised in the phylogenies. These are followed by the sequence data of the translation-elongation factor 1-alpha, while the ribosomal DNA ITS regions are of only limited use in distinguishing species and their phylogenetic relationships.

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

Publications

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

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