The Toxoplasma monocarboxylate transporters are involved in the metabolism within the apicoplast and are linked to parasite survival

Elife. 2024 Mar 19:12:RP88866. doi: 10.7554/eLife.88866.

Abstract

The apicoplast is a four-membrane plastid found in the apicomplexans, which harbors biosynthesis and organelle housekeeping activities in the matrix. However, the mechanism driving the flux of metabolites, in and out, remains unknown. Here, we used TurboID and genome engineering to identify apicoplast transporters in Toxoplasma gondii. Among the many novel transporters, we show that one pair of apicomplexan monocarboxylate transporters (AMTs) appears to have evolved from a putative host cell that engulfed a red alga. Protein depletion showed that AMT1 and AMT2 are critical for parasite growth. Metabolite analyses supported the notion that AMT1 and AMT2 are associated with biosynthesis of isoprenoids and fatty acids. However, stronger phenotypic defects were observed for AMT2, including in the inability to establish T. gondii parasite virulence in mice. This study clarifies, significantly, the mystery of apicoplast transporter composition and reveals the importance of the pair of AMTs in maintaining the apicoplast activity in apicomplexans.

Keywords: Toxoplasma gondii; apicomplexans; apicoplast; infectious disease; microbiology; monocarboxylate transporters; parasite physiology; transporters.

MeSH terms

  • Animals
  • Apicoplasts* / metabolism
  • Fatty Acids / metabolism
  • Mice
  • Monocarboxylic Acid Transporters* / genetics
  • Monocarboxylic Acid Transporters* / metabolism
  • Organic Chemicals / metabolism
  • Parasites* / metabolism
  • Protozoan Proteins / genetics
  • Protozoan Proteins / metabolism
  • Toxoplasma* / genetics
  • Toxoplasma* / metabolism

Substances

  • Fatty Acids
  • Organic Chemicals
  • Protozoan Proteins
  • Monocarboxylic Acid Transporters