Role of melatonin in regulation of lipid accumulation, autophagy and salinity-induced oxidative stress in microalga Monoraphidium sp. QLY-1
Graphical abstract
Introduction
Biodiesel derived from microalgae is considered a third-generation biofuel due to the fast growth rate, lipid and carbohydrate accumulation, and carbon dioxide fixation of the microalgae [1,2]. However, the high microalgae cultivation cost is one of the feasibility and economically significant challenges for the commercialization of biodiesel production [3]. Recently, improvements in lipid production have revealed the paramount importance of lipids and are currently expected to advance the economic feasibility of microalgal biodiesel on a large scale [4,5].
Lipid accumulation in microalgae under abiotic stress conditions is commonly promoted by nutrient deficiency, high illumination, heavy metals, and salinity stress [6]. Among these inductive stress conditions, salinity stress is one of the most universal tools for inducing lipid synthesis in microalgae because it is readily and inexpensively realized [7]. Other potential approaches, such as two-stage cultivation systems and genetic engineering of microalgae, can also overcome the bottleneck of low lipid production but lack general application because of strain-specific differences and their comparatively high costs [8]. Additionally, it has been demonstrated that phytohormone application can regulate the cell growth and metabolism of microalgae, as well as improve its stress tolerance [[9], [10], [11]]. Specifically, the integration of phytohormones under adverse environmental conditions is considered an efficient strategy for lipid and high-value metabolite production in microalgae [10,12,13].
Melatonin is a significant plant hormone playing multifunctional roles, such as activating the antioxidant system, alleviating abiotic stress, and participating in signal transduction and cell metabolism in plants and microalgae [[13], [14], [15]]. In our previous studies, we found that MT facilitates the attenuation of nitrogen starvation- and high-light-induced stress in microalgal cells and regulates cell growth and lipid and astaxanthin synthesis in microalgae under adverse conditions [16,17]. However, no information indicated the roles of MT in affecting cell growth and lipid accumulation in microalgae under salinity stress.
MT is extensively involved in signal transduction. Exogenous MT application regulated nitric oxide (NO), reactive oxidative species (ROS) and mitogen-activated protein kinase (MAPK) signal transduction and the levels of stress hormones in microalgae in response to inductive stress conditions, resulting in the upregulated expressions of lipogenesis- and carotenogenesis-related genes and the promotion of lipid and astaxanthin accumulation [13,16,18]. Moreover, exogenous MT can also modulate autophagic activity in mammals and plants [19,20]. Autophagy is an important process in eukaryotic cells, inducing the self-degradation of some cellular components, including damaged or excessive proteins and organelles. Thus, vital cell activities and metabolism are sustained in response to abiotic stress, and homeostasis is thus ensured [21]. Although ATG8 was identified as a specific marker for autophagy in microalgae exposed to abiotic stresses [22,23], autophagy in microalgae is poorly understood. Whether lipid accumulation is related to the relationship between MT, autophagy and ROS signalling in microalgae under high salt stress has not been elucidated.
This study focused on promoting lipid production in Monoraphidium sp. QLY-1 exposed to salinity stress. The physiology and biochemistry of the algae were examined, and the transcription levels of lipogenesis-related genes were measured. The variation in ROS levels and expression levels of autophagy-related genes under MT and salinity stress conditions were also quantified. The connections between MT, autophagy, ROS signalling and lipid synthesis in QLY-1 under salinity stress conditions were also analysed. This study indicates that the coupling of MT and salinity stress is a potential process for the production of microalgal lipids. The study also provides novel insights into the regulatory mechanisms underlying the effects of MT and autophagy on the promotion of lipid synthesis and improvements to algal tolerance.
Section snippets
Microalgae and growth conditions
The green microalga Monoraphidium sp. QLY-1 was used in this study. The algal samples were obtained from Qilu Lake in Yunnan Province and saved in our laboratory [24]. A compromising strategy named “heterotrophic cultivation and photo-chemical modulator induction” was applied for lipid production by microalgae [24]. During the first stage, the alga was cultivated in heterotrophic condition to achieve high cell density. However, the lipid content in the first stage was extremely low. Thus, the
Effects of melatonin on the biomass and lipid profiles of Monoraphidium sp. QLY-1 exposed to salinity stress
According to a previous investigation, 20 g L−1 (0.34 M) NaCl is the appropriate dose to induce lipid accumulation in QLY-1 [24]. Thus, 0.34 M NaCl was applied in the present study. The growth and lipid patterns of Monoraphidium sp. QLY-1 after treatment with MT and salinity stress are depicted in Fig. 1. The cell growth was obviously slow during the induction period. The biomass concentration was slightly declined under salinity stress with or without MT treatment compared with the control
Conclusions
The combination of MT and salinity stress exerted an enhancing effect on lipid accumulation by upregulating the transcription levels of lipogenesis-related genes. Moreover, MT treatment alleviated salt-induced oxidative stress and activated cell autophagy in response to high salt exposure. Additional evidence indicated that increased autophagic activity can further increase lipid synthesis by regulating lipogenesis and ROS signalling in QLY-1 under a combination of MT treatment and salinity
CRediT authorship contribution statement
Yongteng Zhao: Methodology, Investigation, Writing-original draft. Xueting Song: Investigation, Formal analysis. Peng Zhao: Conceptualization. Tao Li: Methodology. Jun-Wei Xu: Validation. Xuya Yu: Conceptualization, Writing-review & editing, Supervision, Funding acquisition.
Declaration of competing interest
The authors declare that they have no known competing interest to influence the work presented in this paper.
Acknowledgements
This study was financed by the National Natural Science Foundation of China (No. 21766012) and the Scientific Research Foundation of Yunnan Provincial Department of Education (No. 2020Y0084).
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2023, Algal ResearchCitation Excerpt :Compared to terrestrial crops, microalgae could produce higher lipid productivity for their merits of continuous cultivation mode, fast reproduction rate, smaller footprint, short generational cycle, no seasonal restrictions and higher content in target molecules [6,7]. Additionally, the production of biodiesel from microalgae can also alleviate the greenhouse effect caused by carbon dioxide (CO2), and produce a series of valuable by-products such as astaxanthin and carotenoid with produced in the lipid accumulation process, which has high economic and environmental benefits [8,9]. It is estimated that the number of microalgae species is about 70,000 to one million, but only about 44,000 have been reported [10].
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These authors made equal contribution.