Biology subjects

van Hooff, J. J. E.

Publications and source records attributed to van Hooff, J. J. E..

6 recordsLinked to original sources

bioRxiv2024

Structure-based inference of eukaryotic complexity in Asgard archaea

Asgard archaea played a key role in the origin of the eukaryotic cell. While previous studies found that Asgard genomes encode diverse eukaryotic signature proteins (ESPs), representing homologs of proteins that play important roles in the complex organization of eukaryotic cells, the cellular characteristics and complexity of the Asgard archaeal ancestor of eukaryotes remain unclear. Here, we used de novo protein structure modeling and sensitive sequence similarity detection algorithms within an expanded Asgard archaeal genomic dataset to build a structural catalogue of the Asgard archaeal pangenome and identify 908 new isomorphic ESPs (iESPs), representing clusters of protein structures most similar to eukaryotic proteins and that likely underwent extensive sequence divergence. While most previously identified ESPs were involved in cellular processes and signaling, iESPs are enriched in information storage and processing functions, with several being potentially implicated in facilitating cellular complexity. By expanding the complement of eukaryotic proteins in Asgard archaea, this study indicates that the archaeal ancestor of eukaryotes was more complex than previously assumed.

evolutionary biology↗

bioRxiv2024

Shaping up genomes: Prokaryotic roots and eukaryotic diversification of SMC complexes

Chromosome organization ensures accurate DNA replication, segregation, gene regulation and DNA damage repair. Across the tree of life, protein assemblages termed Structural Maintenance of Chromosomes (SMC) complexes determine chromosome organization. Eukaryotes usually have four SMC complex types (condensin I, condensin II, cohesin, and SMC5/6), whereas prokaryotes mostly have one. The expanded set is probably needed to accommodate the considerably larger eukaryotic genomes. Despite their essential functions, SMC complexes exhibit notable variation among model organisms, suggesting underexplored diversity across eukaryotes. Here, we provide a thorough reconstruction of the evolution of SMC complex subunits and accessory proteins across eukaryotes. We show that the last eukaryotic common ancestor (LECA) had all four complete SMC complexes, supporting the notion that LECA was already a sophisticated cell. At later timepoints, condensin II was lost at least thirty times, rendering it one of the most frequently lost eukaryotic cellular machineries. We identify multiple components (e.g., Sororin, Securin, Nse5, and Nse6) as much more ancient and widespread than previously appreciated. Finally, we traced the prokaryotic origins of these complexes and propose an ancient SMC complex was already duplicated in the ancestor of TACK and Asgard archaea, suggesting a sophisticated chromosome organization in the archaeal ancestor of eukaryotes. The eukaryotic SMC complex inventory was further expanded through gene duplications, highlighting the importance of these events in the emergence of eukaryotic complexity. Altogether, our results address questions and raise new ones about how SMC complex evolution affected the genome organizations of ancestral and contemporary organisms.

cell biology↗

bioRxiv2024

Kinetoplastid kinetochore proteins KKT14-KKT15 are divergent Bub1/BubR1-Bub3 proteins

Faithful transmission of genetic material is crucial for the survival of all organisms. In many eukaryotes, a feedback control mechanism called the spindle checkpoint ensures chromosome segregation fidelity by delaying cell cycle progression until all chromosomes achieve proper attachment to the mitotic spindle. Kinetochores are the macromolecular complexes that act as the interface between chromosomes and spindle microtubules. While most eukaryotes have canonical kinetochore proteins that are widely conserved, kinetoplastids such as Trypanosoma brucei have a seemingly unique set of kinetochore proteins including KKT1-25. Available evidence suggests that T. brucei lacks components of the spindle checkpoint and is unable to delay cell cycle progression in response to spindle defects. It therefore remains poorly understood how kinetoplastids regulate cell cycle progression or ensure chromosome segregation fidelity. Here, we report a crystal structure of the C-terminal domain of KKT14 from Apiculatamorpha spiralis and uncover that it is a pseudokinase. Its structure is most similar to the kinase domain of Bub1, a key component of the spindle checkpoint in other eukaryotes. In addition, KKT14 in T. brucei and other trypanosomatids has a putative ABBA motif that is present in Bub1 and its paralog BubR1. We also find that the N-terminal part of KKT14 interacts with KKT15, whose WD40 repeat beta-propeller is phylogenetically closely related to a direct interactor of Bub1/BubR1 called Bub3. Our findings indicate that KKT14-KKT15 are divergent orthologs of Bub1/BubR1-Bub3, which promote accurate chromosome segregation in trypanosomes.

cell biology↗

bioRxiv2023

Lateral gene transfer leaves lasting traces in Rhizaria

Lateral gene transfer (LGT) has contributed to the genetic makeup of various eukaryotic lineages, yet its prevalence and long-term significance remain poorly understood, particularly for transfers between eukaryotes. Here, we investigate LGT across 29 species of Rhizaria, an ancient and ecologically diverse clade of predominantly free-living, single-celled phagotrophs. Using phylogenetic analyses of over 40,000 gene families complemented by machine learning-based prediction, we estimate that 8-20% of protein-coding genes in contemporary rhizarian genomes were acquired through LGT at various points during their billion-year history, with ~2,000 transfer events shared between at least two species across the rhizarian tree of life. Gene duplications outnumber LGTs across most lineages, yet LGT-derived genes themselves duplicate more frequently than vertically inherited ones, amplifying the genomic impact of each transfer event. Notably, transfers from other eukaryotes outnumber those from prokaryotes and show distinct signatures: prokaryote-derived LGTs are enriched among extracellular proteins, whereas eukaryote-derived LGTs are overrepresented in nuclear and informational processes. Prokaryote-derived LGT genes progressively acquire introns over evolutionary time, confirming their genomic integration and long-term retention. Our findings establish LGT as a pervasive force in rhizarian genome evolution and highlight eukaryote-to-eukaryote transfer as a substantial but often overlooked component of eukaryotic genetic innovation.

evolutionary biology↗

bioRxiv2022

Increased sampling and intra-complex homologies favor vertical over horizontal inheritance of the Dam1 complex

Kinetochores connect chromosomes to spindle microtubules to ensure their correct segregation during cell division. Kinetochores of human and yeast are largely homologous, their ability to track depolymerizing microtubules however is carried out by the non-homologous complexes Ska1-C and Dam1-C, respectively. We previously reported the unique anti-correlating phylogenetic profiles of Dam1-C and Ska-C found amongst a wide variety of eukaryotes. Based on these profiles and the limited presence of Dam1-C, we speculated that horizontal gene transfer (HGT) could have played a role in the evolutionary history of Dam1-C. Here, we present expanded analyses of Dam1-c evolution, using additional genome as well as transcriptome sequences and recently acquired 3D structure data. This analysis revealed a wider and more complete presence of Dam1-C in Cryptista, Rhizaria, Ichthyosporea, CRuMs, and Colponemidia. The fungal Dam1-C cryo-EM structure supports earlier hypothesized intra-complex homologies, which enables the reconstruction of rooted and unrooted phylogenies. The rooted tree of concatenated Dam1-C subunits is statistically consistent with the species tree of eukaryotes, suggesting that Dam1-C is ancient, and that the present-day phylogenetic distribution is best explained by multiple, independent losses and no HGT was involved. Furthermore, we investigated the ancient origin of Dam1-C via profile-profile searches. Homology among eight out of the ten Dam1-C subunits suggested that the complex largely evolved from a single multimerizing subunit that diversified into an octameric core via stepwise duplication and sub-functionalization of the subunits before the origin of the Last Common Ancestor. SignificanceThe Dam1 complex has a crucial role in cell division yet its distribution across species is very patchy. To resolve the evolutionary origin of this peculiar distribution, we used the recently acquired 3D structure to obtain a rooted phylogeny. This study makes an important step in discovering the evolutionary history of the Dam1 complex, by determining that Dam1-C was part of the Last eukaryotic Common Ancestor and arose via stepwise duplications during the transition from prokaryotes to eukaryotes.

evolutionary biology↗

bioRxiv2019

Timing the origin of eukaryotic cellular complexity with ancient duplications

Eukaryogenesis is one of the most enigmatic evolutionary transitions, during which simple prokaryotic cells gave rise to complex eukaryotic cells. While evolutionary intermediates are lacking, gene duplications allow us to elucidate the order of events by which eukaryotes originated. Here we use a phylogenomics approach to reconstruct successive steps during eukaryogenesis. We found that gene duplications roughly doubled the proto-eukaryotic genome, with families inherited from the Asgard archaea-related host being duplicated most. By relatively timing events using phylogenetic distances we inferred that duplications in cytoskeletal and membrane trafficking families were among the earliest events, whereas most other families expanded primarily after mitochondrial endosymbiosis. Altogether, we demonstrate that the host that engulfed the proto-mitochondrion had some eukaryote-like complexity, which further increased drastically upon mitochondrial acquisition. This scenario bridges the signs of complexity observed in Asgard archaeal genomes to the proposed role of mitochondria in triggering eukaryogenesis.

evolutionary biology↗