Modulation of the metabolite content of the unicellular rhodophyte Porphyridium purpureum using a 2-stage cultivation approach and chemical stressors

Microalgae have gained traction as suitable sources of bioactive ingredients in the context of increasing demands for health-promoting compounds of natural origins (Borowitzka, 2013, Luo et al., 2015). A variety of both freshwater and marine microalgal species have been the subject of extensive experimentation for enhancing their production of high-value compounds such as antioxidants, omega-3 fatty acids, carotenoid pigments or novel antimicrobial metabolites (Borowitzka, 2013, Cao et al., 2016, Cho and Rhee, 2019, Piña and Contreras-Porcia, 2021). Microalgae are to a large extent photosynthetic microorganisms, the cultivation of which is generally regarded as sustainable (Fabris et al., 2020). They are currently exploited in several sectors, including the cosmetic field (e.g., fucosterol, retinol or mycosporine-2-glycine), the nutraceutical industry (e.g., zeaxanthin or ω-3 fatty acid supplements) or the bioenergy sector (e.g., lipid conversion into biodiesel) (Luo et al., 2015, Del Mondo et al., 2020, Llewellyn and Airs, 2010).

The securing of sustainable food and safeguarding of human health constitute major policy drives in modern societies. Several microalgae species are increasingly considered as suitable sources of nutraceutical compounds and functional foods (Contor, 2001, Yarkent et al., 2020, Koyande et al., 2019, Jha et al., 2017, Moshood et al., 2021, Krishnan et al., 2021). Microalgal cells can adjust their biochemical composition and metabolite production depending on the physico-chemical environment that they are exposed to (González-González and De-Bashan, 2021). Hence, different stressors including nutrient depletion, light intensity variation, light quality shift or the use of metabolic inhibitors or enhancers have been considered for various microalgal species to modulate their content in sought-after compounds (Shi et al., 2020, Chen et al., 2017, Li et al., 2020). For example, nitrogen depletion has been shown to enhance carotenoid content and lipid production in the chlorophytes Chlorella zofingiensis, Dunaliella salina, Neochloris oleoabundans, Muriellopsis sp. and Porphyridium purpureum (Nuutila et al., 1997, Shi et al., 2020, Del Campo et al., 2000, Mulders et al., 2014, Urreta et al., 2014, Zhang et al., 2017). Some plant hormones such as methyl jasmonate have also been shown to contribute to the enhancement of bioactive metabolite yields (e.g., fucoxanthin and lipids) in diatoms, chlorophytes and haptophytes (Mc Gee et al., 2020, McGee et al., 2021, Lu et al., 2010, Ayothi et al., 2021).

Batch cultivation regimes have been the most utilised strategies to produce microalgal biomass and for the experimental assessment of the metabolic consequences of culture condition modulations (Dębowski et al., 2020, Roleda et al., 2013, Ho et al., 2014, Sun et al., 2018). A caveat has been that there is often a trade-off between the successful enhancement of the microalgal content in key metabolites and the overall productivity of cultures (Kumar et al., 2020, Sun et al., 2018). Two-stage approaches have emerged as suitable compromises whereby stressors are introduced at a later stage of the culture growth, with or without nutrient replenishing (Narala et al., 2016, Liyanaarachchi et al., 2021, Ali et al., 2021).

A variety of macro- and micro-algal rhodophytes are currently exploited for nutrition and biotechnology purposes, with a focus on high-value compounds such as EPA, arachidonic acid, polysaccharides or phycoerythrin (Cuellar-Bermudez et al., 2015, Lapidot et al., 2010). The unicellular Porphyridium purpureum has attracted interests owing to its promising potential for the production of floridian starch, phycobiliproteins (PBPs), PUFAs or sulfated exopolysaccharides (EPS) (Kathiresan et al., 2007, Medina-Cabrera et al., 2020). In this study, the growth of Porphyridium purpureum CCAP 1380/1 A was attempted via a two-stage approach using hydrogen peroxide, the phytohormone methyl jasmonate and several plant extracts utilised as stressors introduced during the stationary phase of growth. The response of the microalgae was analysed with respect to its content in terms of neutral lipids, phycobiliproteins, carbohydrates, antioxidants and carotenoid pigments.

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