A major isoform of mitochondrial trans-2-enoyl-CoA reductase is dispensable for wax ester production in Euglena gracilis under anaerobic conditions

PLoS One. 2019 Jan 16;14(1):e0210755. doi: 10.1371/journal.pone.0210755. eCollection 2019.

Abstract

Under anaerobic conditions, Euglena gracilis produces a large amount of wax ester through mitochondrial fatty acid synthesis from storage polysaccharides termed paramylon, to generate ATP. Trans-2-enoyl-CoA reductases (TERs) in mitochondria have been considered to play a key role in this process, because the enzymes catalyze the reduction of short chain length CoA-substrates (such as crotonyl-CoA). A TER enzyme (EgTER1) has been previously identified and enzymologically characterized; however, its physiological significance remained to be evaluated by genetic analysis. We herein generated EgTER1-knockdown Euglena cells, in which total crotonyl-CoA reductase activity was decreased to 10% of control value. Notably, the knockdown cells showed a severe bleaching phenotype with deficiencies in chlorophylls and glycolipids, but grew normally under heterotrophic conditions (with glucose supplementation). Moreover, the knockdown cells accumulated much greater quantities of wax ester than control cells before and after transfer to anaerobic conditions, which was accompanied by a large metabolomic change. Furthermore, we failed to find any contribution of other potential TER genes in wax ester production. Our findings propose a novel role of EgTER1 in the greening process and demonstrate that this enzyme is dispensable for wax ester production under anaerobic conditions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anaerobiosis
  • Esters / metabolism
  • Euglena gracilis / enzymology*
  • Euglena gracilis / genetics
  • Fatty Acids / metabolism
  • Fermentation
  • Gene Knockdown Techniques
  • Isoenzymes / antagonists & inhibitors
  • Isoenzymes / genetics
  • Isoenzymes / metabolism
  • Metabolome
  • Metabolomics
  • Mitochondria / enzymology
  • Oxidoreductases Acting on CH-CH Group Donors / antagonists & inhibitors
  • Oxidoreductases Acting on CH-CH Group Donors / genetics
  • Oxidoreductases Acting on CH-CH Group Donors / metabolism*
  • Waxes / metabolism

Substances

  • Esters
  • Fatty Acids
  • Isoenzymes
  • Waxes
  • Oxidoreductases Acting on CH-CH Group Donors
  • trans-2-enoyl-CoA reductase (NADPH)

Grants and funding

This study was supported by the Core Research for Evolutional Science and Technology (CREST) Program of the Japan Science and Technology Agency (JST) (YT, TM, TO, TI), http://www.jst.go.jp/presto/bioenergy/english/index.html. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.