A plastid two-pore channel essential for inter-organelle communication and growth of Toxoplasma gondii

Zhu-Hong Li, Thayer P. King, Lawrence Ayong, Beejan Asady, Xinjiang Cai, Taufiq Rahman, Stephen A. Vella, Isabelle Coppens, Sandip Patel and Silvia N. J. Moreno ()
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Zhu-Hong Li: University of Georgia
Thayer P. King: University of Georgia
Lawrence Ayong: University of Georgia
Beejan Asady: Johns Hopkins Bloomberg School of Public Heath
Xinjiang Cai: David Geffen School of Medicine at UCLA
Taufiq Rahman: University of Cambridge
Stephen A. Vella: University of Georgia
Isabelle Coppens: Johns Hopkins Bloomberg School of Public Heath
Sandip Patel: University College London
Silvia N. J. Moreno: University of Georgia

Nature Communications, 2021, vol. 12, issue 1, 1-14

Abstract: Abstract Two-pore channels (TPCs) are a ubiquitous family of cation channels that localize to acidic organelles in animals and plants to regulate numerous Ca2+-dependent events. Little is known about TPCs in unicellular organisms despite their ancient origins. Here, we characterize a TPC from Toxoplasma gondii, the causative agent of toxoplasmosis. TgTPC is a member of a novel clad of TPCs in Apicomplexa, distinct from previously identified TPCs and only present in coccidians. We show that TgTPC localizes not to acidic organelles but to the apicoplast, a non-photosynthetic plastid found in most apicomplexan parasites. Conditional silencing of TgTPC resulted in progressive loss of apicoplast integrity, severely affecting growth and the lytic cycle. Isolation of TPC null mutants revealed a selective role for TPCs in replication independent of apicoplast loss that required conserved residues within the pore-lining region. Using a genetically-encoded Ca2+ indicator targeted to the apicoplast, we show that Ca2+ signals deriving from the ER but not from the extracellular space are selectively transmitted to the lumen. Deletion of the TgTPC gene caused reduced apicoplast Ca2+ uptake and membrane contact site formation between the apicoplast and the ER. Fundamental roles for TPCs in maintaining organelle integrity, inter-organelle communication and growth emerge.

Date: 2021
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DOI: 10.1038/s41467-021-25987-5

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