Potential for the Production of Carotenoids of Interest in the Polar Diatom Fragilariopsis cylindrus

Abstract

Carotenoid xanthophyll pigments are receiving growing interest in various industrial fields due to their broad and diverse bioactive and health beneficial properties. Fucoxanthin (Fx) and the inter-convertible couple diadinoxanthin-diatoxanthin (Ddx+Dtx) are acknowledged as some of the most promising xanthophylls; they are mainly synthesized by diatoms (Bacillariophyta). While temperate strains of diatoms have been widely investigated, recent years showed a growing interest in using polar strains, which are better adapted to the natural growth conditions of Nordic countries. The aim of the present study was to explore the potential of the polar diatom Fragilariopsis cylindrus in producing Fx and Ddx+Dtx by means of the manipulation of the growth light climate (daylength, light intensity and spectrum) and temperature. We further compared its best capacity to the strongest xanthophyll production levels reported for temperate counterparts grown under comparable conditions. In our hands, the best growing conditions for F. cylindrus were a semi-continuous growth at 7 °C and under a 12 h light:12 h dark photoperiod of monochromatic blue light (445 nm) at a PUR of 11.7 μmol photons m^-2 s^-1. This allowed the highest Fx productivity of 43.80 µg L^-1 day^-1 and the highest Fx yield of 7.53 µg Wh^-1, more than two times higher than under 'white' light. For Ddx+Dtx, the highest productivity (4.55 µg L^-1 day^-1) was reached under the same conditions of 'white light' and at 0 °C. Our results show that F. cylindrus, and potentially other polar diatom strains, are very well suited for Fx and Ddx+Dtx production under conditions of low temperature and light intensity, reaching similar productivity levels as model temperate counterparts such as Phaeodactylum tricornutum. The present work supports the possibility of using polar diatoms as an efficient cold and low light-adapted bioresource for xanthophyll pigments, especially usable in Nordic countries.

Keywords: blue light; diadinoxanthin; diatoxanthin; fucoxanthin; photosynthesis; polar diatoms.

Figure 1

Two-dimensional structure of fucoxanthin, diadinoxanthin and diatoxanthin. Two-dimensional structural images of CID 5281239 (fucoxanthin), 6449888 (diadinoxanthin), 6440986 (Diatoxathin) were obtained from PubChem (https://pubchem.ncbi.nlm.nih.gov, accessed on 27 June 2022).

Figure 2

Photosynthetic potential, fucoxanthin (Fx), diadinoxanthin and diatoxanthin (Ddx+Dtx) synthesis in Fragilariopsis cylindrus grown under different photoperiods (0 h light:24 h darkness; 6 h L:18 h D; 12 h L:12 h D; 18 h L:6 h D; 24 h L:0 h D) under a ‘white’ spectrum (see Figure S1) with the same photosynthetically usable radiation (PUR) (11.7 µmol photons m⁻² s⁻¹): (a) growth rate (bars), dark-acclimated photochemical efficiency (F_v/F_M, black dots), effective non-photochemical quenching (NPQ_gE, green dots); (b) Fx content (bars), Fx productivity (dots); (c) Ddx+Dtx content (bars), Ddx+Dtx productivity (dots). Data are the mean values n = 3 ± SD. Letters represent clusters of non-significantly different means for the corresponding parameter, with the letter ‘a’ representing the highest mean values and the other letters following in alphabetic order.

Figure 3

Growth, photosynthetic potential and fucoxanthin (Fx) synthesis in Fragilariopsis cylindrus grown under different light spectra (‘white’(yellow), blue (445 nm, blue) and red (660 nm, red)) with the same photosynthetically usable radiation (PUR) (11.7 µmol photons m⁻² s⁻¹) and photoperiod of 12 h L:12 h D: (a) growth rate (bars), maximum photochemical efficiency (F_v/F_M, black dots), non-photochemical quenching at growing PUR intensity (NPQ_gE, green dots), (b) Fx content (bars), Fx productivity (green dots) and Fx yield (black dots). Data are the mean values n = 3 ± SD; see Table S1 for all values and see Table 2 for parameter definitions. Letters represent clusters of non-significantly different means for the corresponding parameter, with the letter ‘a’ representing the highest mean values and the other letters following in alphabetic order.

Figure 4

Growth, photosynthetic potential and fucoxanthin (Fx) synthesis in Fragilariopsis cylindrus grown under two light spectra (‘white’ (yellow bars), blue (445 nm, blue bars)) and two photosynthetically usable radiation (PUR) levels (5.8 and 11.7 µmol photons m⁻² s⁻¹) with the same photoperiod of 12 h L:12 h D: (a) growth rate (bars), maximum photochemical efficiency (F_v/F_M, black dots), non-photochemical quenching at growing PUR intensity (NPQ_gE, green dots), (b) Fx content (bars), Fx productivity (green dots) and Fx yield (black dots). Data are the mean values n = 3 ± SD; see Table S1 for all values and see Table 2 for parameter definitions. Letters represent clusters of non-significantly different means for the corresponding parameter, with the letter ‘a’ representing the highest mean values and the other letters following in alphabetic order. NS represent non statically different means for the parameter across the treatments.

Figure 5

Growth, photosynthetic potential and fucoxanthin (Fx) synthesis in Fragilariopsis cylindrus grown under different photosynthetically usable radiation (PUR) levels (5.8, 11.7 and 23.4 µmol photons m⁻² s⁻¹) and photoperiods (12 h L:12 h D and continuous light, 24 h L:0 h D) with the same light spectra (445 nm, blue): (a) growth rate (bars), maximum photochemical efficiency (F_v/F_M, black dots), non-photochemical quenching at growing PUR intensity (NPQ_gE, green dots), (b) Fx content (bars), Fx productivity (green dots) and Fx yield (black dots). Data are the mean values n = 3 ± SD; see Table S1 for all values and see Table 2 for parameter definitions. Letters represent clusters of non-significantly different means for the corresponding parameter, with the letter ‘a’ representing the highest mean values and the other letters following in alphabetic order.

Figure 6

Growth, photosynthetic potential and fucoxanthin (Fx) synthesis in Fragilariopsis cylindrus grown under two light spectra (‘white’ (yellow bars), blue (445 nm, blue bars)) and two temperatures (0 °C (plain bars), and 7 °C (striped bars)) with the same photosynthetically usable radiation (PUR) levels (11.7 µmol photons m⁻² s⁻¹) and photoperiod of 12 h L:12 h D: (a) growth rate (bars), maximum photochemical efficiency (F_v/F_M, black dots), non-photochemical quenching at growing PUR intensity (NPQ_gE, green dots), (b) Fx content (bars), Fx productivity (green dots) and Fx yield (black dots). Data are the mean values n = 3 ± SD; see Table S1 for all values and see Table 2 for parameter definitions. Letters represent clusters of non-significantly different means for the corresponding parameter, the letter ‘a’ being the highest mean values and the other letters following in alphabetic order.

Figure 7

Diadinoxanthin and diatoxanthin (Ddx+Dtx) synthesis in Fragilariopsis cylindrus grown under different light spectra (‘white’ (yellow bars), blue (445 nm, blue bars) and red (660 nm, red bars), photosynthetically usable radiation (PUR) levels (5.8, 11.7, 23.4 µmol photons m⁻² s⁻¹), photoperiods (12 h L:12 h D and continuous light, 24 h L:0 h D), and temperatures (0 °C (plain bars), and 7 °C (striped bars)). Data are the mean values n = 3 ± SD; see Table S1 for all values and see Table 2 for parameter definitions. Letters represent clusters of non-significantly different means for the corresponding parameter, with the letter ‘a’ representing the highest mean values and the other letters following in alphabetic order.

Figure 8

Growth, fucoxanthin (Fx), diadinoxanthin and diatoxanthin (Ddx+Dtx) synthesis in Fragilariopsis cylindrus grown in batch culturing mode at 0 °C (plain bars) and 7 °C (striped bars), in f/2 (light grey) and f medium (medium and dark grey), and under the same photosynthetically usable radiation (PUR) (11.7 µmol photons m⁻² s⁻¹) and photoperiod of 12 h light:12 h darkness: (a) biomass dry weight increase over days, (b) growth rate, (c) Fx content (bars), Fx productivity (dots), (d) Ddx+Dtx content (bars), Ddx+Dtx productivity (dots). f/2 and f refer to the culturing medium enriched at half and full concentration. Data are the mean values n = 3 ± SD; see Table 2 for parameter definitions. Letters represent clusters of non-significantly different means for the corresponding parameter, with letter ‘a’ representing the highest mean values and the other letters following in alphabetic order. NS represents non statistically different means for the parameter across the treatments.

Figure 9

Fragilariopsis cylindrus (CCMP 3323) scanning electron microscope picture. Taken by Adèle Luthi-Marie and Suzie Côté at the microanalysis laboratory of University Laval.