Carotenoids from the extreme halophilic archaeon Haloterrigena turkmenica: identification and antioxidant activity

Abstract

Haloterrigena turkmenica was able to synthesize carotenoids when grown in halobacteria medium. These molecules have antioxidant properties and find application in food, cosmetic, and pharmaceutical fields. The carotenoids were extracted with methanol, separated by RP-HPLC, and identified by mass spectrometry and UV/Vis spectra analyses. The C carotenoids were the main pigments, and C, C, and C carotenoids were also detected. Seven geometric isomers were distinguished for bacterioruberin, monoanhydrobacterioruberin, and bisanhydrobacterioruberin. The assignment to a specific isomer was tentatively attempted through the analysis of the corresponding UV/Vis spectrum, the intensity of the cis peak, and its spectral fine structure. Lycopene, phytoene, and lycopersene were among the minor carotenoids further identified. The extract displayed antioxidant power higher than alpha-tocopherol, butylhydroxytoluene, and ascorbic acid used as reference compounds. Our studies identified for the first time seven geometric isomers of bacterioruberin derivatives and 30 carotenoids in a haloarchaeon.

Haloterrigena sp. Strain SGH1, a Bacterioruberin-Rich, Perchlorate-Tolerant Halophilic Archaeon Isolated From Halite Microbial Communities, Atacama Desert, Chile

“…Mass spectrometry provided the corresponding profiles for positively ionized fragments and their m/z for each major subfraction as shown in Figure 6 and Supplementary Figure S4, Supplementary Table S1. From the analysis of these spectroscopic and spectrophotometric data and comparison with previously reported information (Mandelli et al, 2012;Dina et al, 2017;Squillaci et al, 2017), it was inferred that Haloterrigena sp. strain SGH1 cells contain six C-50 molecules related to the BR family: four geometric isomers (5-cis-BR, 9-cis-BR, 13-cis-BR, and all-trans-BR) and two dehydrated derivatives (all-transtetra-anhydrous BR and cis-tetra-anhydrous BR) and, one the metabolic intermediate (all-trans-mono-anhydrous BR).…”

“…strain SGH1 is a reversible, salt-dependent metabolic process and the maximum carotenoid content was obtained in cells grown at 25 • C and 25% NaCl. Comparatively, a lower carotenoid content has been registered for other halophilic archaea; e.g., 45 µg g −1 of dry biomass in Halococcus morrhuae (Mandelli et al, 2012), 75 µg g −1 of dry biomass in H. turkmenica (Squillaci et al, 2017) and 335 µg g −1 of dry biomass Haloarcula japonica (Yatsunami et al, 2014). Recently, Zalazar et al (2019) have reported that the bacterioruberin content (220 mg g −1 dry weight) in a hyperpigmented, genetically modified Haloferax volcanii strain HVLON3 is higher than in other haloarchaea.…”

“…BR-like molecules were the principal carotenoids accumulated by Haloterrigena sp. strain SGH1, based on the UV-Vis spectra (photometric fingerprint) and the three major Raman displacement signals (1502, 1147, and 995 cm −1 ) observed in the methanolic extracts (Imperi et al, 2007;Marshall et al, 2007;Kaczor et al, 2011;Mandelli et al, 2012;Jehlička and Oren, 2013;Jehlička et al, 2014;Dina et al, 2017;Squillaci et al, 2017). According to Jehlièka et al (2019) and under green excitation laser, the strong Raman signals near 1506, 1152, and 1000 cm −1 , are associated to C = C stretching band, to C-C stretching band and methyl groups in the polyene chain bound to C-C bonds, respectively.…”

Deciphering Pathways for Carotenogenesis in Haloarchaea

“…Since the first publication on carotenoids from archaea in the early sixties (last century) [71,72] more than 850 works have been published in indexed journals about this subject (PUBMED: data of access December the 10th, 2019; 856 publications identify using "carotenoids" and "archaea" as keywords). Most of these works addressed the characterization of the pigments synthesized by archaea, mainly haloarchaea, some others look for potential applications (due to their high antioxidant capability) and more recently, several works describe molecular engineering to optimize de production of some pigments in order to upscale their production [73][74][75][76]. However, there is still controversy about the nature of the pathways for carotenogenesis in haloarchaea, and consequently, the production of overpigmented mutants as cell factories for carotenoid production is still a limitation.…”

Fed-batch carotenoid production by Phaffia rhodozyma Y-17268 using agroindustrial substrates

“…The natural pigments most studied are the carotenoids, responsible for the yellow, orange, and red colors of some fruits, vegetables, flowers, fish, crustaceous, bacteria, and fungi [1]. The carotenoids production via biotechnology can be obtained by a diversity of microorganisms, such as bacteria [2], yeasts [3][4][5], microalgal [6], and filamentous fungi [7].…”