How mitochondrial cristae illuminate the important role of oxygen during eukaryogenesis DOI Creative Commons
Dave Speijer

BioEssays, Journal Year: 2024, Volume and Issue: 46(5)

Published: March 6, 2024

Abstract Inner membranes of mitochondria are extensively folded, forming cristae. The observed overall correlation between efficient eukaryotic ATP generation and the area internal mitochondrial inner both in unicellular organisms metazoan tissues seems to explain why they evolved. However, crucial use molecular oxygen (O 2 ) as final acceptor electron transport chain is still not sufficiently appreciated. O was an essential prerequisite for cristae development during early eukaryogenesis could be factor allowing retention upon loss generation. Here I analyze illuminating bacterial examples. also discuss formative influences intracellular consumption on evolution last common ancestor (LECA). These considerations bring about explanation many genes coming from other than archaeon bacterium merging at start eukaryogenesis.

Language: Английский

Mitochondrial genomes revisited: why do different lineages retain different genes? DOI Creative Commons
Anzhelika Butenko, Julius Lukeš, Dave Speijer

et al.

BMC Biology, Journal Year: 2024, Volume and Issue: 22(1)

Published: Jan. 25, 2024

Abstract The mitochondria contain their own genome derived from an alphaproteobacterial endosymbiont. From thousands of protein-coding genes originally encoded by ancestor, only between 1 and about 70 are on extant mitochondrial genomes (mitogenomes). Thanks to a dramatically increasing number sequenced annotated mitogenomes coherent picture why some were lost, or relocated the nucleus, is emerging. In this review, we describe characteristics mitochondria-to-nucleus gene transfer resulting varied content across eukaryotes. We introduce ‘burst-upon-drift’ model best explain nuclear-mitochondrial population genetics with flares due genetic drift.

Language: Английский

Citations

22

Genome evolution in plants and the origins of innovation DOI Creative Commons
James Clark

New Phytologist, Journal Year: 2023, Volume and Issue: 240(6), P. 2204 - 2209

Published: Sept. 2, 2023

Summary Plant evolution has been characterised by a series of major novelties in their vegetative and reproductive traits that have led to greater complexity. Underpinning this diversification the genome. When viewed at scale plant kingdom, genome punctuated conspicuous instances gene whole‐genome duplication, horizontal transfer extensive loss. The periods dynamic often coincide with key traits, demonstrating coevolution genomes phenotypes macroevolutionary scale. Conventionally, complexity diversity considered through lens duplication role loss remains comparatively unexplored. However, light reductive across multiple lineages, association between phenotypic warrants attention.

Language: Английский

Citations

25

Diplonemid protists possess exotic endomembrane machinery, impacting models of membrane trafficking in modern and ancient eukaryotes DOI
Kristína Záhonová, Julius Lukeš, Joel B. Dacks

et al.

Current Biology, Journal Year: 2025, Volume and Issue: unknown

Published: March 1, 2025

Language: Английский

Citations

1

Eukaryotic CD-NTase, STING, and viperin proteins evolved via domain shuffling, horizontal transfer, and ancient inheritance from prokaryotes DOI Creative Commons
Edward M. Culbertson, Tera C. Levin

PLoS Biology, Journal Year: 2023, Volume and Issue: 21(12), P. e3002436 - e3002436

Published: Dec. 8, 2023

Animals use a variety of cell-autonomous innate immune proteins to detect viral infections and prevent replication. Recent studies have discovered that subset mammalian antiviral homology antiphage defense in bacteria, implying there are aspects immunity shared across the Tree Life. While majority these focused on characterizing diversity biochemical functions bacterial proteins, evolutionary relationships between animal less clear. This ambiguity is partly due long distances separating which obscures their relationships. Here, we tackle this problem for 3 families (CD-NTases [including cGAS], STINGs, viperins) by deeply sampling protein eukaryotes. We find viperins OAS family CD-NTases ancient likely inherited since earliest eukaryotes first arose. In contrast, other were acquired via at least 4 independent events horizontal gene transfer (HGT) from bacteria. Two allowed algae acquire new viperins, while 2 more HGT gave rise distinct superfamilies eukaryotic CD-NTases: cGLR superfamily (containing cGAS) has diversified series animal-specific duplications previously undefined eSMODS superfamily, closely resembles CD-NTases. Finally, found cGAS STING substantially different histories, with domains undergoing convergent domain shuffling bacteria Overall, our findings paint picture as highly dynamic, where build upon repertoires through reuse repeatedly rich reservoir genes.

Language: Английский

Citations

20

Euglena’s atypical respiratory chain adapts to the discoidal cristae and flexible metabolism DOI Creative Commons

Zhaoxiang He,

Mengchen Wu,

Hongtao Tian

et al.

Nature Communications, Journal Year: 2024, Volume and Issue: 15(1)

Published: Feb. 22, 2024

Abstract Euglena gracilis , a model organism of the eukaryotic supergroup Discoba harbouring also clinically important parasitic species, possesses diverse metabolic strategies and an atypical electron transport chain. While structures chain complexes supercomplexes most other clades have been reported, no similar structure is currently available for Discoba, limiting understandings its core metabolism leaving gap in evolutionary tree bioenergetics. Here, we report high-resolution cryo-EM ’s respirasome I + III 2 IV supercomplex . A previously unreported fatty acid synthesis domain locates on tip complex I’s peripheral arm, providing clear picture subunit composition identified previously. Individual are re-arranged to adapt non-uniform membrane curvature discoidal cristae. Furthermore, conformationally rigid deactivated by restricting ubiquinone’s access substrate tunnel. Our findings provide structural insights therapeutic developments against euglenozoan parasite infections.

Language: Английский

Citations

8

Shaping up genomes: Prokaryotic roots and eukaryotic diversification of SMC complexes DOI Creative Commons
Jolien J. E. van Hooff, Maximilian W. D. Raas, Eelco C. Tromer

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Jan. 8, 2024

Summary Across the tree of life, SMC complexes organize, segregate and regulate DNA. In contrast to prokaryotes, which often possess one complex, eukaryotes usually have four such complexes. This expanded set is involved in managing considerably larger nuclear genomes eukaryotes, are distributed across multiple chromosomes. Despite their essential functions, exhibit variations model suggesting an even greater variety these that remains unexplored. Here, we aimed uncover diversity evolution deeper, prokaryotic evolutionary origins. For this, conducted in-depth comparative genomic phylogenetic analyses We show last eukaryotic common ancestor (LECA) likely had fully-fledged versions all condensin II complex was later lost at least 30 times eukaryotes. report evidence proteins previously designated as functional analogs various organisms (e.g., Sororin, Securin, Nse5 Nse6) fact genuine orthologs. Finally, traced origins propose a single duplicated early archaeon. Altogether, provide comprehensive overview evolution, both addressing generating questions about functioning ancestral contemporary organisms.

Language: Английский

Citations

7

Reconstructing the last common ancestor of all eukaryotes DOI Creative Commons
Thomas A. Richards, Laura Eme, John M. Archibald

et al.

PLoS Biology, Journal Year: 2024, Volume and Issue: 22(11), P. e3002917 - e3002917

Published: Nov. 25, 2024

Understanding the origin of eukaryotic cells is one most difficult problems in all biology. A key challenge relevant to question eukaryogenesis reconstructing gene repertoire last common ancestor (LECA). As data sets grow, sketching an accurate genomics-informed picture early cellular complexity requires provision analytical resources and a commitment sharing. Here, we summarise progress towards understanding biology LECA outline community approach inferring its wider repertoire. Once assembled, robust set will be useful tool for evaluating alternative hypotheses about eukaryotes evolution traits descendant lineages, with relevance diverse fields such as cell biology, microbial ecology, biotechnology, agriculture, medicine. In this Consensus View, put forth status quo agreed path forward reconstruct LECA's content.

Language: Английский

Citations

6

The core MICOS complex subunit Mic60 has been substituted by two cryptic mitofilin-containing proteins in Euglenozoa DOI Creative Commons
Shaghayegh Sheikh,

Barbora Knotkova,

Corinna Benz

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2025, Volume and Issue: unknown

Published: Jan. 31, 2025

ABSTRACT Cristae enclose respiratory chain protein complexes, making them the bioenergetic subcompartments of mitochondria. The MICOS complex is among inducers sharp membrane curvature needed for crista formation. Resembling organized around a core protein, mitofilin-domain bearing Mic60, that was inherited from alphaproteobacterial progenitor Extant alphaproteobacteria express Mic60 to form their own subcompartments, demonstrating permeance Mic60’s and function during long span prokaryotic eukaryotic evolution. Yet, unlike virtually all aerobic eukaryotes, not encoded in any genome multifarious protists comprise phylum Euglenozoa, including trypanosomes. Here, we show has been replaced euglenozoans by two cryptic mitofilin domain-containing subunits, Mic34 Mic40. Sharply contrasting domains life, these are integral proteins. Reverse genetics revealed they intertwined with oxidative folding pathway required mitochondrial–and crista–biogenesis, veiling potential remodeling role. Nevertheless, binds phospholipid bilayers vitro . Mic40 heterologous expression remodels gammaproteobacterial cytoplasmic membranes, like Mic60. Astoundingly, overexpression elaborates simplified tubular mitochondrion Trypanosoma brucei life cycle stage repressed phosphorylation. structural correspondence Mic34’s domain predicted mutations conserved motifs ablated mitochondria-remodeling activity. Thus, family more diverse than originally supposed, its structurally most divergent members altering euglenozoan MICOS. SIGNIFICANCE STATEMENT mitochondrial give organelle distinctive ruffled appearance. They house multiprotein-complex machinery cellular respiration. These crista-embedded complexes built an immutable bacterial symbiont engendered represents one such protein. Because fundamental role formation, present organisms cristae, even closest known relatives mitochondria, reflecting symbiotic origin. Euglenozoan strange exception, lacking recognizable despite having cristae. Instead, have Mic60-like proteins evaded recognition due radically altered structures. This demonstrates normally cores ancient can change

Language: Английский

Citations

0

Eukaryotic antiviral immune proteins arose via convergence, horizontal transfer, and ancient inheritance DOI Creative Commons
Edward M. Culbertson, Tera C. Levin

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: June 27, 2023

Abstract Animals use a variety of cell-autonomous innate immune proteins to detect viral infections and prevent replication. Recent studies have discovered that subset mammalian antiviral homology anti-phage defense in bacteria, implying there are aspects immunity shared across the Tree Life. While majority these focused on characterizing diversity biochemical functions bacterial proteins, evolutionary relationships between animal less clear. This ambiguity is partly due long distances separating which obscures their relationships. Here, we tackle this problem for three families (CD-NTases [including cGAS], STINGs, Viperins) by deeply sampling protein eukaryotes. We find Viperins OAS family CD-NTases truly ancient likely inherited since last eukaryotic common ancestor possibly longer. In contrast, other arose via at least four independent events horizontal gene transfer (HGT) from bacteria. Two allowed algae acquire new viperins, while two more HGT gave rise distinct superfamilies CD-NTases: Mab21 superfamily (containing cGAS) has diversified series animal-specific duplications, previously undefined eSMODS superfamily, closely resembles CD-NTases. Finally, found cGAS STING substantially different histories, with STINGs arising convergent domain shuffling bacteria Overall, our findings paint picture as highly dynamic, where eukaryotes build upon repertoires through reuse domains repeatedly rich reservoir genes.

Language: Английский

Citations

7

The contours of evolution: In defence of Darwin's tree of life paradigm DOI Creative Commons
Peter T. S. van der Gulik, Wouter D. Hoff, Dave Speijer

et al.

BioEssays, Journal Year: 2024, Volume and Issue: 46(5)

Published: March 4, 2024

Abstract Both the concept of a Darwinian tree life (TOL) and possibility its accurate reconstruction have been much criticized. Criticisms mostly revolve around extensive occurrence lateral gene transfer (LGT), instances uptake complete organisms to become organelles (with associated subsequent nucleus), as well implications more subtle aspects biological species concept. Here we argue that none these criticisms are sufficient abandon valuable TOL realities it captures. Especially important is need conceptually distinguish between organismal trees trees, which necessitates incorporating insights widely occurring LGT into modern evolutionary theory. We demonstrate all criticisms, while based on new findings, do not invalidate TOL. After considering insights, find contours evolution best represented by

Language: Английский

Citations

2