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Background  Docosahexaenoic acid (DHA, C22:6) and odd-chain fatty acids (OCFAs, C15:0 and C17:0) have attracted great interest, since they have been widely used in food and therapeutic industries, as well as chemical industry, such as biodiesel production and improvement. The oil-producing heterotrophic microalgae  Schizochytrium  sp. 31 is one of main DHA-producing strains. Recently, it was found that  Schizochytrium  can also synthesize OCFAs; however, contents and titers of DHA and OCFAs in  Schizochytrium  are still low, which limit its practical application.    Results  In this study, we found that acetyl-CoA carboxylase suffered from a feedback inhibition by C16-CoA in  Schizochytrium , and relief of the inhibition resulted in improved both lipid content and the ratio of OCFAs in total fatty acids. Based on this finding, a novel strategy for elevating both DHA and OCFAs contents was established. First, the total lipid accumulation was increased by overexpressing a malic enzyme from  Crypthecodinium cohnii  to elevate NADPH supply. Second, the inhibition effect on acetyl-CoA carboxylase was relieved by overexpressing a codon-optimized  ELO3  gene from  Mortierella alpina , which encodes an elongase enzyme responsible for converting C16 into C18 fatty acids. After the above two-step engineering, contents of DHA and OCFAs were increased by 1.39- and 3.30-fold, reaching a level of 26.70 and 25.08% of dry cell weight, respectively, which are the highest contents reported so far for  Schizochytrium . The titers of DHA and OCFAs were elevated by 1.08- and 2.57-fold, reaching a level of 3.54 and 3.32 g/L, respectively. Notably, the OCFAs titer achieved was 2.66-fold higher than the highest reported in  Escherichia coli  (1.25 g/L), implying potential value for industry application. To reveal the potential metabolic mechanism for the enhanced biosynthesis of both DHA and OCFAs, LC–MS metabolomic analysis was employed and the results showed that the pentose phosphate pathway and the glycolysis pathway were strengthened and intracellular propionyl-CoA concentration were also significantly increased in the engineered  Schizochytrium , suggesting an increased supply of NADPH, acetyl-CoA, and propionyl-CoA for DHA and OCFAs accumulation.    Conclusions  The discovery provides a new source of OCFAs production, and proposes a new strategy to improve contents and titers of both DHA and OCFAs in  Schizochytrium . These will be valuable for improving commercial potential of  Schizochytrium  and guiding the engineering strategy in other fatty acids producing heterotrophic microalga.    Electronic supplementary material  The online version of this article (10.1186/s13068-019-1484-x) contains supplementary material, which is available to authorized users.

Metabolic engineering to enhance biosynthesis of both docosahexaenoic acid and odd-chain fatty acids in Schizochytrium sp. S31