Division and Adaptation to Host Environment of Apicomplexan Parasites Depend on Apicoplast Lipid Metabolic Plasticity and Host Organelle Remodeling

Apicomplexan parasites are unicellular eukaryotic pathogens that must obtain and combine lipids from both host cell scavenging and de novo synthesis to maintain parasite propagation and survival within their human host. Major questions on the role and regulation of each lipid source upon fluctuating...

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Published inCell reports (Cambridge) Vol. 30; no. 11; pp. 3778 - 3792.e9
Main Authors Amiar, Souad, Katris, Nicholas J., Berry, Laurence, Dass, Sheena, Duley, Samuel, Arnold, Christophe-Sebastien, Shears, Melanie J., Brunet, Camille, Touquet, Bastien, McFadden, Geoffrey I., Yamaryo-Botté, Yoshiki, Botté, Cyrille Y.
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Published United States Elsevier Inc 17.03.2020
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Abstract Apicomplexan parasites are unicellular eukaryotic pathogens that must obtain and combine lipids from both host cell scavenging and de novo synthesis to maintain parasite propagation and survival within their human host. Major questions on the role and regulation of each lipid source upon fluctuating host nutritional conditions remain unanswered. Characterization of an apicoplast acyltransferase, TgATS2, shows that the apicoplast provides (lyso)phosphatidic acid, required for the recruitment of a critical dynamin (TgDrpC) during parasite cytokinesis. Disruption of TgATS2 also leads parasites to shift metabolic lipid acquisition from de novo synthesis toward host scavenging. We show that both lipid scavenging and de novo synthesis pathways in wild-type parasites exhibit major metabolic and cellular plasticity upon sensing host lipid-deprived environments through concomitant (1) upregulation of de novo fatty acid synthesis capacities in the apicoplast and (2) parasite-driven host remodeling to generate multi-membrane-bound structures from host organelles that are imported toward the parasite. [Display omitted] •Knockout of apicoplast TgATS2 disrupts LPA/PA for DrpC recruitment during cytokinesis•T. gondii can sense host environment and adapt to low host nutritional content•Under lipid starvation, parasite FASII and other lipid metabolic genes become essential•Upon nutrient deprivation, T. gondii induces host organelle remodeling and vesiculation Apicoplast de novo lipid synthesis and lipid host scavenging are both critical for apicomplexan intracellular development. Amiar et al. show that the parasite adapts to the fluctuations of host nutritional content to regulate the metabolic activity of both apicoplast and scavenging pathways and maintain parasite development and division.
AbstractList Apicomplexan parasites are unicellular eukaryotic pathogens that must obtain and combine lipids from both host cell scavenging and de novo synthesis to maintain parasite propagation and survival within their human host. Major questions on the role and regulation of each lipid source upon fluctuating host nutritional conditions remain unanswered. Characterization of an apicoplast acyltransferase, TgATS2, shows that the apicoplast provides (lyso)phosphatidic acid, required for the recruitment of a critical dynamin (TgDrpC) during parasite cytokinesis. Disruption of TgATS2 also leads parasites to shift metabolic lipid acquisition from de novo synthesis toward host scavenging. We show that both lipid scavenging and de novo synthesis pathways in wild-type parasites exhibit major metabolic and cellular plasticity upon sensing host lipid-deprived environments through concomitant (1) upregulation of de novo fatty acid synthesis capacities in the apicoplast and (2) parasite-driven host remodeling to generate multi-membrane-bound structures from host organelles that are imported toward the parasite.
Apicomplexan parasites are unicellular eukaryotic pathogens that must obtain and combine lipids from both host cell scavenging and de novo synthesis to maintain parasite propagation and survival within their human host. Major questions on the role and regulation of each lipid source upon fluctuating host nutritional conditions remain unanswered. Characterization of an apicoplast acyltransferase, TgATS2, shows that the apicoplast provides (lyso)phosphatidic acid, required for the recruitment of a critical dynamin (TgDrpC) during parasite cytokinesis. Disruption of TgATS2 also leads parasites to shift metabolic lipid acquisition from de novo synthesis toward host scavenging. We show that both lipid scavenging and de novo synthesis pathways in wild-type parasites exhibit major metabolic and cellular plasticity upon sensing host lipid-deprived environments through concomitant (1) upregulation of de novo fatty acid synthesis capacities in the apicoplast and (2) parasite-driven host remodeling to generate multi-membrane-bound structures from host organelles that are imported toward the parasite. : Apicoplast de novo lipid synthesis and lipid host scavenging are both critical for apicomplexan intracellular development. Amiar et al. show that the parasite adapts to the fluctuations of host nutritional content to regulate the metabolic activity of both apicoplast and scavenging pathways and maintain parasite development and division. Keywords: Apicomplexa, toxoplasmosis, malaria, apicoplast, lipid synthesis, phosphatidic acid, host-parasite interaction, lipidomics, host nutritional environment, cytokinesis
Apicomplexan parasites are unicellular eukaryotic pathogens that must obtain and combine lipids from both host cell scavenging and de novo synthesis to maintain parasite propagation and survival within their human host. Major questions on the role and regulation of each lipid source upon fluctuating host nutritional conditions remain unanswered. Characterization of an apicoplast acyltransferase, TgATS2, shows that the apicoplast provides (lyso)phosphatidic acid, required for the recruitment of a critical dynamin (TgDrpC) during parasite cytokinesis. Disruption of TgATS2 also leads parasites to shift metabolic lipid acquisition from de novo synthesis toward host scavenging. We show that both lipid scavenging and de novo synthesis pathways in wild-type parasites exhibit major metabolic and cellular plasticity upon sensing host lipid-deprived environments through concomitant (1) upregulation of de novo fatty acid synthesis capacities in the apicoplast and (2) parasite-driven host remodeling to generate multi-membrane-bound structures from host organelles that are imported toward the parasite. [Display omitted] •Knockout of apicoplast TgATS2 disrupts LPA/PA for DrpC recruitment during cytokinesis•T. gondii can sense host environment and adapt to low host nutritional content•Under lipid starvation, parasite FASII and other lipid metabolic genes become essential•Upon nutrient deprivation, T. gondii induces host organelle remodeling and vesiculation Apicoplast de novo lipid synthesis and lipid host scavenging are both critical for apicomplexan intracellular development. Amiar et al. show that the parasite adapts to the fluctuations of host nutritional content to regulate the metabolic activity of both apicoplast and scavenging pathways and maintain parasite development and division.
Author Dass, Sheena
Brunet, Camille
Katris, Nicholas J.
Duley, Samuel
McFadden, Geoffrey I.
Shears, Melanie J.
Berry, Laurence
Yamaryo-Botté, Yoshiki
Amiar, Souad
Touquet, Bastien
Botté, Cyrille Y.
Arnold, Christophe-Sebastien
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  givenname: Nicholas J.
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  organization: ApicoLipid Team, Institute for Advanced Biosciences, CNRS UMR5309, Université Grenoble Alpes, INSERM U1209, Grenoble, France
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  givenname: Camille
  surname: Brunet
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  organization: ApicoLipid Team, Institute for Advanced Biosciences, CNRS UMR5309, Université Grenoble Alpes, INSERM U1209, Grenoble, France
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  surname: Touquet
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  givenname: Geoffrey I.
  surname: McFadden
  fullname: McFadden, Geoffrey I.
  organization: McFadden Laboratory, School of Biosciences, University of Melbourne, Melbourne, VIC 3010, Australia
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  email: cyrille.botte@univ-grenoble-alpes.fr
  organization: ApicoLipid Team, Institute for Advanced Biosciences, CNRS UMR5309, Université Grenoble Alpes, INSERM U1209, Grenoble, France
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Issue 11
Keywords Apicomplexa
lipid synthesis
host nutritional environment
toxoplasmosis
cytokinesis
host-parasite interaction
phosphatidic acid
malaria
lipidomics
apicoplast
Language English
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SSID ssj0000601194
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Snippet Apicomplexan parasites are unicellular eukaryotic pathogens that must obtain and combine lipids from both host cell scavenging and de novo synthesis to...
SourceID doaj
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crossref
pubmed
elsevier
SourceType Open Website
Open Access Repository
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Index Database
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StartPage 3778
SubjectTerms Acyltransferases - metabolism
Adaptation, Physiological
Animals
Apicomplexa
apicoplast
Apicoplasts - metabolism
Biochemistry, Molecular Biology
Cancer
Cell Division
Cell Membrane - metabolism
Cellular Biology
Cytokinesis
Fatty Acid Synthases - metabolism
Fatty Acids - biosynthesis
Gene Deletion
host nutritional environment
host-parasite interaction
Host-Parasite Interactions
Human health and pathology
Humans
Infectious diseases
Intracellular Space - parasitology
Life Cycle Stages
Life Sciences
Lipid Metabolism
lipid synthesis
Lipidomics
malaria
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Microbiology and Parasitology
Models, Biological
Multivesicular Bodies - metabolism
Multivesicular Bodies - ultrastructure
Mutation - genetics
Nutrients
Parasites - growth & development
Parasites - metabolism
Parasites - physiology
Parasites - ultrastructure
Parasitology
phosphatidic acid
Protozoan Proteins - metabolism
Quantitative Methods
Toxoplasma - growth & development
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toxoplasmosis
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Title Division and Adaptation to Host Environment of Apicomplexan Parasites Depend on Apicoplast Lipid Metabolic Plasticity and Host Organelle Remodeling
URI https://dx.doi.org/10.1016/j.celrep.2020.02.072
https://www.ncbi.nlm.nih.gov/pubmed/32187549
https://hal.science/hal-03103818
https://doaj.org/article/d93b566505b649d49275779305492146
Volume 30
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