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

Abstract

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.

A Revised Taxonomy of Diplonemids Including the Eupelagonemidae n. fam. and a Type Species, Eupelagonema oceanica n. gen. & sp.

“…), as well as some curious metabolic and molecular traits (Morales et al. ; Qian and Keeling ). But overall, the group has not been extensively described, with multiple undetermined phylotypes present in environmental molecular surveys (Tashyreva et al.…”

“…The newly described genera are also marine, though their habitats are yet to be clarified (Tashyreva et al 2018a). Some of these diplonemids have been studied mostly due to their relationship to the more famous kinetoplastids, and because of their baroque mitochondrial genome architecture and posttranscriptional editing characteristics (Kiethega et al 2013;Marande et al 2005;Valach et al 2016;Yabuki et al 2016), as well as some curious metabolic and molecular traits (Morales et al 2016;Qian and Keeling 2001). But overall, the group has not been extensively described, with multiple undetermined phylotypes present in environmental molecular surveys (Tashyreva et al 2018a,b).…”

Comparative molecular cell biology of phototrophic euglenids and parasitic trypanosomatids sheds light on the ancestor of Euglenozoa

“…While kinetoplastid nuclear genomes are relatively small (∼ 10 7 bp) (Gull, Alsford & Ersfeld, ; Berriman et al, ; Ivens et al, ; Jackson et al, ), euglenid nuclear genomes are much larger with estimated sizes in different species of approximately 3–24 Gb (reviewed in Ebenezer et al, ) which is equal to or greater than the size of the human genome (3 Gb). The size of the draft genome of the diplonemid D. papillatum has been estimated to be 176.5 Mb (Morales et al, ). The newest estimations of the E. gracilis nuclear genome size based on DNA sequencing (but not DNA content) range from less than 0.5 Gb to more than 2 Gb (Ebenezer et al, , ).…”

“…Figure 1 shows the diplonemids and kinetoplastids as sister groups, since this is supported by most phylogenetic analyses. Their close relationship is also supported by the presence of glycosomes, highly modified peroxisomes containing glycolytic enzymes, which are not present in euglenids (Cavalier‐Smith, ; Morales et al, ).…”

Transformation of Diplonema papillatum, the type species of the highly diverse and abundant marine microeukaryotes Diplonemida (Euglenozoa)

“…The mitochondrial genome and transcriptome have been analyzed in detail, revealing novel modes of posttranscriptional gene expression (Marande and Burger, 2007;Kiethega et al, 2013;Moreira et al, 2016;Valach et al, 2016;Faktorov a et al, 2018). Further, D. papillatum has been investigated regarding its compartmentalization of gluconeogenesis (Makiuchi et al, 2011;Morales et al, 2016). Finally, the nuclear genome has recently been sequenced and assembled, and functional annotation is under way (unpubl.…”