Acidocalcisomes: Ultrastructure, Biogenesis, and Distribution in Microbial Eukaryotes

Ursula Goodenough, Aaron A. Heiss, Robyn Roth, Jannette Rusch, Jae Hyeok Lee

Research output: Contribution to journalArticlepeer-review

35 Scopus citations

Abstract

Acidocalcisomes are membrane-enclosed organelles with acidic lumens that accumulate polyphosphate, often in granular form, and sequester calcium and metals. They carry a transmembrane polyphosphate polymerase and two classes of proton pumps: H+-pyrophosphatases (H+-PPases) and V-type ATPases. This report describes acidocalcisomes that were snap-frozen in living cells, primarily the green alga Chlamydomonas reinhardtii, and then fractured and etched (QFDEEM). Polyphosphate granules prove to be uncommon in log-phase C. reinhardtii cells and abundant in stressed cells, where they are also found within autophagy-related vacuoles. Their E (ectoplasmic) fracture face adopts a unique rugose morphology with etching, and displays ∼14 nm globular domains in broken cell preparations. Using etched membrane morphology as a guide, acidocalcisomes were identified during assembly in the trans-Golgi and were recognized in QFDEEM replicas of 18 additional algae and protists. Phylogenetic analysis documents that the eukaryotic gene encoding the signature acidocalcisomal H+-PPase pump has homologues in three widespread eukaryotic clades and has been lost in opisthokonts and Amoebozoa. The eukaryotic clades are related to three functionally diverged prokaryotic PPase pumps, one of which transports Na+. Our data indicate that the Last Eukaryotic Common Ancestor (LECA) encoded two bacteria-derived pumps and one Asgard-archaea-derived pump.

Original languageEnglish
Pages (from-to)287-313
Number of pages27
JournalProtist
Volume170
Issue number3
DOIs
StatePublished - Jul 2019
Externally publishedYes

Keywords

  • Acidocalcisomes
  • Asgard archaea.
  • Chlamydomonas reinhardtii
  • freeze-fracture
  • phylogenetic analyses
  • polyphosphate granules

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