Differential remodelling of peroxisome function underpins the environmental and metabolic adaptability of diplonemids and kinetoplastids

The remodelling of organelle function is increasingly appreciated as a central driver of eukaryotic biodiversity and evolution. Kinetoplastids including Trypanosoma and Leishmania have evolved specialized peroxisomes, called glycosomes. Glycosomes uniquely contain a glycolytic pathway as well as oth...

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Published in:Proceedings of the Royal Society. B, Biological sciences Biological sciences, 2016-05, Vol.283 (1830), p.20160520
Main Authors: Morales, Jorge, Hashimoto, Muneaki, Williams, Tom A., Hirawake-Mogi, Hiroko, Makiuchi, Takashi, Tsubouchi, Akiko, Kaga, Naoko, Taka, Hikari, Fujimura, Tsutomu, Koike, Masato, Mita, Toshihiro, Bringaud, Frédéric, Concepción, Juan L., Hashimoto, Tetsuo, Embley, T. Martin, Nara, Takeshi
Format: Article
Language:English
Subjects:
Amino Acids - metabolism
Biodiversity
Carbon - metabolism
Diplonemids
Enzymes - metabolism
Euglenozoa - cytology
Euglenozoa - genetics
Euglenozoa - metabolism
Gluconeogenesis
Glycolysis
Kinetoplastids
Life Sciences
Metabolic Compartmentalization
Microbiology and Parasitology
Microbodies
Organelle Evolution
Parasitology
Pentose Phosphate Pathway
Peroxisomes
Peroxisomes - metabolism
Phylogeny
Populations and Evolution
Signal Transduction
Systematics, Phylogenetics and taxonomy
Trypanosoma cruzi - cytology
Trypanosoma cruzi - metabolism
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Summary:The remodelling of organelle function is increasingly appreciated as a central driver of eukaryotic biodiversity and evolution. Kinetoplastids including Trypanosoma and Leishmania have evolved specialized peroxisomes, called glycosomes. Glycosomes uniquely contain a glycolytic pathway as well as other enzymes, which underpin the physiological flexibility of these major human pathogens. The sister group of kinetoplastids are the diplonemids, which are among the most abundant eukaryotes in marine plankton. Here we demonstrate the compartmentalization of gluconeogenesis, or glycolysis in reverse, in the peroxisomes of the free-living marine diplonemid, Diplonema papillatum. Our results suggest that peroxisome modification was already under way in the common ancestor of kinetoplastids and diplonemids, and raise the possibility that the central importance of gluconeogenesis to carbon metabolism in the heterotrophic free-living ancestor may have been an important selective driver. Our data indicate that peroxisome modification is not confined to the kinetoplastid lineage, but has also been a factor in the success of their free-living euglenozoan relatives.
ISSN:0962-8452
1471-2954
DOI:10.1098/rspb.2016.0520