Lipid catabolism in microalgae

Abstract

Lipid degradation processes are important in microalgae because survival and growth of microalgal cells under fluctuating environmental conditions require permanent remodeling or turnover of membrane lipids as well as rapid mobilization of storage lipids. Lipid catabolism comprises two major spatially and temporarily separated steps, namely lipolysis, which releases fatty acids and head groups and is catalyzed by lipases at membranes or lipid droplets, and degradation of fatty acids to acetyl-CoA, which occurs in peroxisomes through the β-oxidation pathway in green microalgae, and can sometimes occur in mitochondria in some other algal species. Here we review the current knowledge on the enzymes and regulatory proteins involved in lipolysis and peroxisomal β-oxidation and highlight gaps in our understanding of lipid degradation pathways in microalgae. Metabolic use of acetyl-CoA products via glyoxylate cycle and gluconeogenesis is also reviewed. We then present the implication of various cellular processes such as vesicle trafficking, cell cycle and autophagy on lipid turnover. Finally, physiological roles and the manipulation of lipid catabolism for biotechnological applications in microalgae are discussed.

Branched-Chain Amino Acid Catabolism Impacts Triacylglycerol Homeostasis in Chlamydomonas reinhardtii

“…In mammalian cells, since fatty acid b-oxidation occurs essentially in mitochondria (Eaton et al, 1996), the metabolic link between storage lipid degradation and mitochondrial activity has been well established (Kujala et al, 2016). Based on our analysis and also based on the literature, BCAA degradation generally occurs in mitochondria, whereas the major steps for b-oxidation of fatty acids occur in peroxisomes of Chlamydomonas (Kong et al, 2017(Kong et al, , 2018a(Kong et al, , 2018b. This raises an interesting question, namely, how a defect in BCAA catabolism can affect lipid degradation.…”

“…Thus, it seems reasonable to postulate that less ATP is produced in the BCKDH-deficient mutants upon N resupply in the dark. The initial steps of b-oxidation of fatty acids require two ATPs, both to fuel the long-chain acyl-CoA synthetase (Fulda et al, 2004;Kong et al, 2018b) as well as to energize fatty acid import into the peroxisomes via an ATP-binding cassette transporter, the plant homolog of which is known to transfer fatty acids from cytosol into peroxisomes (Footitt et al, 2002). We thus propose that when mitochondrial respiration is impaired in the bkdE1a mutant, less ATP is produced, consequently fatty acid activation and import into peroxisomes are reduced, thereby impacting TAG breakdown (Fig.…”

“…Indeed, in plants and algae, TAG is known not to be a good respiratory substrate, and the peroxisomal fatty acid b-oxidation pathway does not directly produce ATP. ATP production from fatty acid breakdown requires cooperation with the glyoxylate cycle and mitochondrial respiration (Kong et al, 2018b). Therefore, ATP production from TAG degradation in Chlamydomonas requires an initial ATP supply, even if TAG degradation will eventually generate a large amount of ATP and become selfsustained.…”

Multiomics analysis reveals a distinct mechanism of oleaginousness in the emerging model alga Chromochloris zofingiensis

“…Several lipases from C. zofingiensis , such as Cz02g29090 and Cz05g31060, were downregulated by ND, inversely related to TAG accumulation (Figure and Table S5); they are possibly involved in TAG degradation and represent candidate lipases worthy of engineering. The fatty acids released from TAG are subject to beta‐oxidation, which is likely to occur in peroxisomes in algae (Kong et al ., ). An insertional mutation of acyl‐CoA oxidase 2 (ACX2) in C. reinhardtii led to 20% increased TAG levels under ND conditions and maintained much higher TAG levels when exposed to N replenishment (Kong et al ., ), pointing to the feasibility of improving algal TAG through suppressing the fatty acid beta‐oxidation pathway.…”

Earlier Degraded Tapetum1 (EDT1) Encodes an ATP-Citrate Lyase Required for Tapetum Programmed Cell Death

“…Acetyl-CoA is a central intermediate that mediates energy flowing and material circulation, and its molecule synthesis is essential for growth and adaptation to stress (Morrish et al, 2010;Cai et al, 2011). In plants, acetyl-CoA is found in at least five different subcellular compartments with differential roles: as a substrate for acetylation in the nucleus, for de novo fatty acid biosynthesis in the plastids, incorporated into the tricarboxylic acid cycle in the mitochondria, for production of fatty acids by b-oxidation and conversion of fatty acids into sugars in the peroxisomes, and for biosynthesis of a large battery of important compounds in the cytosol (Gengenbach et al, 2001;Fatland et al, 2002Fatland et al, , 2005Davidj et al, 2009;Morrish et al, 2010;Kong et al, 2017Kong et al, , 2018Li et al, 2019).…”