Autophagy in protists: Examples of secondary loss, lineage-specific innovations, and the conundrum of remodeling a single mitochondrion

Daniel J. Rigden, Paul A. Michels, Michael L. Ginger

Research output: Contribution to journalArticle

34 Citations (Scopus)

Abstract

Autophagy describes the process by which eukaryotes selectively and nonselectively target cytoplasm and entire organelles for lysosomal or (in yeast) vacuolar degradation. More than 30 different proteins contribute to this complex process, and it is widely recognized that the term autophagy does not describe merely a single linear pathway by which intracellular components are routed for lysosomal degradation. Yet, while autophagy has been unequivocally demonstrated in evolutionarily diverse organisms and the importance of autophagy in many aspects of human health and development is becoming ever more apparent, the extent to which autophagy in different taxa draws on a conserved cohort of readily recognizable proteins is not particularly clear. Here, we address this issue by comprehensive mapping of known autophagy components across a taxonomically diverse range of unicellular eukaryotes. Unexpectedly, our analysis points to independent examples of secondary loss of macroautophagy, the best understood of the autophagy pathways, in two parasites and one extremophile. Additionally, while our data point towards autophagy being an ancient innovation, utilizing conserved core machinery, it is also clear that lineage-specific moderation (e.g., probable loss of Atg17 in some unikonts) and elaboration (paralogue expansion) of the core macroautophagy pathway occurs readily. Finally, we also consider the interplay between autophagy and organelle turnover in protists. Here, there are likely to be intriguing issues, as exemplified by mitochondrial turnover. In contrast to the dynamic mitochondrial fusion and fission observed in many eukaryotes (including yeast), cell cycle regulated division of a single mitochondrion occurs in some protists. Yet, in these organisms mitochondrial function can often be rapidly remodeled; we contend that in these species turnover of mitochondrial proteins is the product of intraorganellar protease activity.

LanguageEnglish
Pages784-794
Number of pages11
JournalAutophagy
Volume5
Issue number6
DOIs
Publication statusPublished - 16 Aug 2009
Externally publishedYes

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Autophagy
Mitochondria
Eukaryota
Organelles
Yeasts
Mitochondrial Dynamics
Mitochondrial Turnover
Mitochondrial Proteins
Human Development
Cell Cycle
Cytoplasm
Parasites
Proteins
Peptide Hydrolases

Cite this

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title = "Autophagy in protists: Examples of secondary loss, lineage-specific innovations, and the conundrum of remodeling a single mitochondrion",
abstract = "Autophagy describes the process by which eukaryotes selectively and nonselectively target cytoplasm and entire organelles for lysosomal or (in yeast) vacuolar degradation. More than 30 different proteins contribute to this complex process, and it is widely recognized that the term autophagy does not describe merely a single linear pathway by which intracellular components are routed for lysosomal degradation. Yet, while autophagy has been unequivocally demonstrated in evolutionarily diverse organisms and the importance of autophagy in many aspects of human health and development is becoming ever more apparent, the extent to which autophagy in different taxa draws on a conserved cohort of readily recognizable proteins is not particularly clear. Here, we address this issue by comprehensive mapping of known autophagy components across a taxonomically diverse range of unicellular eukaryotes. Unexpectedly, our analysis points to independent examples of secondary loss of macroautophagy, the best understood of the autophagy pathways, in two parasites and one extremophile. Additionally, while our data point towards autophagy being an ancient innovation, utilizing conserved core machinery, it is also clear that lineage-specific moderation (e.g., probable loss of Atg17 in some unikonts) and elaboration (paralogue expansion) of the core macroautophagy pathway occurs readily. Finally, we also consider the interplay between autophagy and organelle turnover in protists. Here, there are likely to be intriguing issues, as exemplified by mitochondrial turnover. In contrast to the dynamic mitochondrial fusion and fission observed in many eukaryotes (including yeast), cell cycle regulated division of a single mitochondrion occurs in some protists. Yet, in these organisms mitochondrial function can often be rapidly remodeled; we contend that in these species turnover of mitochondrial proteins is the product of intraorganellar protease activity.",
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Autophagy in protists : Examples of secondary loss, lineage-specific innovations, and the conundrum of remodeling a single mitochondrion. / Rigden, Daniel J.; Michels, Paul A.; Ginger, Michael L.

In: Autophagy, Vol. 5, No. 6, 16.08.2009, p. 784-794.

Research output: Contribution to journalArticle

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T2 - Autophagy

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AU - Michels, Paul A.

AU - Ginger, Michael L.

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AB - Autophagy describes the process by which eukaryotes selectively and nonselectively target cytoplasm and entire organelles for lysosomal or (in yeast) vacuolar degradation. More than 30 different proteins contribute to this complex process, and it is widely recognized that the term autophagy does not describe merely a single linear pathway by which intracellular components are routed for lysosomal degradation. Yet, while autophagy has been unequivocally demonstrated in evolutionarily diverse organisms and the importance of autophagy in many aspects of human health and development is becoming ever more apparent, the extent to which autophagy in different taxa draws on a conserved cohort of readily recognizable proteins is not particularly clear. Here, we address this issue by comprehensive mapping of known autophagy components across a taxonomically diverse range of unicellular eukaryotes. Unexpectedly, our analysis points to independent examples of secondary loss of macroautophagy, the best understood of the autophagy pathways, in two parasites and one extremophile. Additionally, while our data point towards autophagy being an ancient innovation, utilizing conserved core machinery, it is also clear that lineage-specific moderation (e.g., probable loss of Atg17 in some unikonts) and elaboration (paralogue expansion) of the core macroautophagy pathway occurs readily. Finally, we also consider the interplay between autophagy and organelle turnover in protists. Here, there are likely to be intriguing issues, as exemplified by mitochondrial turnover. In contrast to the dynamic mitochondrial fusion and fission observed in many eukaryotes (including yeast), cell cycle regulated division of a single mitochondrion occurs in some protists. Yet, in these organisms mitochondrial function can often be rapidly remodeled; we contend that in these species turnover of mitochondrial proteins is the product of intraorganellar protease activity.

KW - Comparative genomics

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