Host-symbiont interactions in Angomonas deanei include the evolution of a host-derived dynamin ring around the endosymbiont division site

Morales, Jorge; Ehret, Georg; Poschmann, Gereon; Reinicke, Tobias; Maurya, Anay K; Kröninger, Lena; Zanini, D.; Wolters, Rebecca; Kalyanaraman, Dhevi; Krakovka, M.; Bäumers, Miriam; Nowack, Eva C. M.

doi:10.1016/j.cub.2022.11.020

Cited by 12 publications

(5 citation statements)

References 95 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Angomonas deanei is the only trypanosomatid that expresses OCD, whose encoding gene was transferred to the protozoa from its obligatory endosymbiotic Betaproteobacteria (41, 42). Our searches in the Tritryp genome database did not retrieve any candidate gene for OCD in Leishmania spp.…”

Section: Resultsmentioning

confidence: 99%

Genetic and functional dissection of the glutamate-proline pathway reveals a shortcut for glutamate catabolism inLeishmania

Campagnaro,

Cruz

2024

Preprint

View full text Add to dashboard Cite

Trypanosomatids are early-divergent eukaryotes that have adapted to parasitism. During their life cycles, these parasites switch between a mammalian and an invertebrate host, and the ability to adapt their metabolism to different nutritional sources is detrimental for their success. In the invertebrate host, these protists have access to high amounts of amino acids and efficiently utilise it for energy production. Proline is a particularly efficient energy source for trypanosomes. Glutamate is also efficiently used byTrypanosoma cruzi, but it needs to be converted into proline prior to its catabolism. By employing a series of genetic modifications and functional analysis, we show here thatLeishmaniaparasites, the causative agents of leishmaniases, can utilise proline, glutamate and glutamine as energy sources, and although these parasites possess all the genes necessary for the biosynthesis of proline from glutamate, this pathway has, at best, limited function, with at least one of its components (pyrroline-5-carboxylate reductase) assuming divergent functions in different life cycle stages of the parasite. In fact, we show that the catabolism of glutamate is independent of proline biosynthesis and the former is most likely directly imported into the mitochondrion and catabolised to recover the cellular redox metabolism and increase mitochondrial membrane potential. Moreover, our data suggest a relevant role for glutamate dehydrogenase in nutritional stress response inLeishmania. These findings highlight relevant differences in amino acid metabolism betweenTrypanosomaandLeishmaniaand suggest a diversification in amino acid metabolic pathways within Trypanosomatidae.

show abstract

Section: Resultsmentioning

confidence: 99%

Genetic and functional dissection of the glutamate-proline pathway reveals a shortcut for glutamate catabolism inLeishmania

Campagnaro,

Cruz

2024

Preprint

View full text Add to dashboard Cite

show abstract

“…5 C ). These cytoplasmic protrusions sometimes even included multiple peroxisome-related organelles called glycosomes ( Moyersoen et al 2004 ). The average diameter of a glycosome is between 270 and 300 nm ( Tetley and Vickerman 1991 ), which is a testament to how voluminous the MidX-induced cytoplasmic protrusions can become.…”

Section: Resultsmentioning

confidence: 99%

A Novel Group of Dynamin-Related Proteins Shared by Eukaryotes and Giant Viruses Is Able to Remodel Mitochondria From Within the Matrix

Sheikh

Pánek

Gahura

et al. 2023

Molecular Biology and Evolution

View full text Add to dashboard Cite

The diverse GTPases of the dynamin superfamily play various roles in the cell, as exemplified by the dynamin-related proteins (DRPs) Mgm1 and Opa1, which remodel the mitochondrial inner membrane in fungi and metazoans, respectively. Via an exhaustive search of genomic and metagenomic databases we found previously unknown DRP types occurring in diverse eukaryotes and giant viruses (phylum Nucleocytoviricota). One novel DRP clade, termed MidX, combined hitherto uncharacterized proteins from giant viruses and six distantly related eukaryote taxa (Stramenopiles, Telonemia, Picozoa, Amoebozoa, Apusomonadida, and Choanoflagellata). MidX stood out because it was not only predicted to be mitochondria-targeted, but also to assume a tertiary structure not observed in other DRPs before. To understand how MidX affects mitochondria, we exogenously expressed MidX from Hyperionvirus in the kinetoplastid Trypanosoma brucei, which lacks Mgm1 or Opa1 orthologs. MidX massively affected mitochondrial morphology from inside the matrix, where it closely associates with the inner membrane. This unprecedented mode of action is contrasts to those of Mgm1 and Opa1, which mediate inner membrane remodeling in the intermembrane space. We speculate that MidX was acquired in Nucleocytoviricota evolution by horizontal gene transfer from eukaryotes and is used by giant viruses to remodel host mitochondria during infection. MidX’s unique structure may be an adaptation for reshaping mitochondria from the inside. Finally, Mgm1 forms a sister to MidX and not Opa1 in our phylogenetic analysis, throwing into question the long-presumed homology of these DRPs with similar roles in sister lineages.

show abstract

“…The evolution of such a protein targeting and import system seems like a huge leap, and it has often been described as a major milestone in the evolution of a bona fide organelle [ 57 , 58 ]. Landmark experiments surveying the protein content of small-genome (but pre-“tipping point”) endosymbionts in unicellular eukaryotes have shown that host protein import does indeed occur on a large scale [ 59 , 60 ]. There is also some evidence suggesting that sap-feeding insects, including the hosts of tipping-point endosymbionts, have the ability to import proteins and other large molecules into their endosymbionts.…”

Section: How Do You Transport Molecules Across the Cell Envelope With...mentioning

confidence: 99%

How do bacterial endosymbionts work with so few genes?

McCutcheon,

Garber,

Spencer

et al. 2024

PLoS Biol

View full text Add to dashboard Cite

The move from a free-living environment to a long-term residence inside a host eukaryotic cell has profound effects on bacterial function. While endosymbioses are found in many eukaryotes, from protists to plants to animals, the bacteria that form these host-beneficial relationships are even more diverse. Endosymbiont genomes can become radically smaller than their free-living relatives, and their few remaining genes show extreme compositional biases. The details of how these reduced and divergent gene sets work, and how they interact with their host cell, remain mysterious. This Unsolved Mystery reviews how genome reduction alters endosymbiont biology and highlights a “tipping point” where the loss of the ability to build a cell envelope coincides with a marked erosion of translation-related genes.

show abstract

Host-symbiont interactions in Angomonas deanei include the evolution of a host-derived dynamin ring around the endosymbiont division site

Cited by 12 publications

References 95 publications

Genetic and functional dissection of the glutamate-proline pathway reveals a shortcut for glutamate catabolism inLeishmania

Genetic and functional dissection of the glutamate-proline pathway reveals a shortcut for glutamate catabolism inLeishmania

A Novel Group of Dynamin-Related Proteins Shared by Eukaryotes and Giant Viruses Is Able to Remodel Mitochondria From Within the Matrix

How do bacterial endosymbionts work with so few genes?

Contact Info

Product

Resources

About