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Keywords = Eukaryogenesis

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14 pages, 2398 KB  
Review
From Ancient Philosophy to Endosymbiotic Theory: The Bacterial Origin and Key Role of Mitochondria in Immune Responses
by Alexandra Mpakosi, Christiana Kaliouli-Antonopoulou, Vasileios Cholevas, Stamatios Cholevas, Ioannis Tzouvelekis, Maria Mironidou-Tzouveleki, Emmanuel A. Tsantes, Deny Tsakri, Marianna Vlachaki, Stella Baliou, Petros Ioannou, Rozeta Sokou, Stefanos Bonovas and Andreas G. Tsantes
Microorganisms 2025, 13(9), 2149; https://doi.org/10.3390/microorganisms13092149 - 15 Sep 2025
Cited by 1 | Viewed by 5369
Abstract
The endosymbiotic theory, which is the crucial starting point of eukaryogenesis, was first mentioned in the philosophy of the pre-Socratic Greek philosopher Empedocles. According to him, everything merges into units with differential survival. Similarly, during eukaryogenesis, the fusion of two distinct units resulted [...] Read more.
The endosymbiotic theory, which is the crucial starting point of eukaryogenesis, was first mentioned in the philosophy of the pre-Socratic Greek philosopher Empedocles. According to him, everything merges into units with differential survival. Similarly, during eukaryogenesis, the fusion of two distinct units resulted in the creation of a new cell type that possessed a newly formed organelle, the mitochondrion. Since then, the mitochondrion has been a key regulator of health and immunity. Furthermore, many of its characteristics and functions are due to its endosymbiotic bacterial origin. For example, it possesses damage-associated molecular patterns that can activate inflammatory signaling pathways, has circular DNA with CpG-rich motifs, as well as a double phospholipid membrane, and divides by fission. Mitochondrial function plays a critical role in maintaining cellular homeostasis, as they meet the cell’s energy needs and regulate many of its functions. However, after cellular damage due to infection, radiation, or toxins, mitochondrial stress and dysfunction can occur and mitochondrial DNA can be released into the cytosol. Cytosolic mitochondrial DNA can then activate proinflammatory signaling pathways, mediated by TLR9 and cGAS, as well as inflammasomes, triggering inflammation and autoimmunity. Full article
(This article belongs to the Section Molecular Microbiology and Immunology)
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16 pages, 3957 KB  
Article
Expanded Archaeal Genomes Shed New Light on the Evolution of Isoprenoid Biosynthesis
by Pengfei Zhu, Jialin Hou, Yixuan Xiong, Ruize Xie, Yinzhao Wang and Fengping Wang
Microorganisms 2024, 12(4), 707; https://doi.org/10.3390/microorganisms12040707 - 30 Mar 2024
Cited by 3 | Viewed by 3708
Abstract
Isoprenoids and their derivatives, essential for all cellular life on Earth, are particularly crucial in archaeal membrane lipids, suggesting that their biosynthesis pathways have ancient origins and play pivotal roles in the evolution of early life. Despite all eukaryotes, archaea, and a few [...] Read more.
Isoprenoids and their derivatives, essential for all cellular life on Earth, are particularly crucial in archaeal membrane lipids, suggesting that their biosynthesis pathways have ancient origins and play pivotal roles in the evolution of early life. Despite all eukaryotes, archaea, and a few bacterial lineages being known to exclusively use the mevalonate (MVA) pathway to synthesize isoprenoids, the origin and evolutionary trajectory of the MVA pathway remain controversial. Here, we conducted a thorough comparison and phylogenetic analysis of key enzymes across the four types of MVA pathway, with the particular inclusion of metagenome assembled genomes (MAGs) from uncultivated archaea. Our findings support an archaeal origin of the MVA pathway, likely postdating the divergence of Bacteria and Archaea from the Last Universal Common Ancestor (LUCA), thus implying the LUCA’s enzymatic inability for isoprenoid biosynthesis. Notably, the Asgard archaea are implicated in playing central roles in the evolution of the MVA pathway, serving not only as putative ancestors of the eukaryote- and Thermoplasma-type routes, but also as crucial mediators in the gene transfer to eukaryotes, possibly during eukaryogenesis. Overall, this study advances our understanding of the origin and evolutionary history of the MVA pathway, providing unique insights into the lipid divide and the evolution of early life. Full article
(This article belongs to the Section Microbiomes)
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11 pages, 680 KB  
Review
From Mimivirus to Mirusvirus: The Quest for Hidden Giants
by Morgan Gaïa and Patrick Forterre
Viruses 2023, 15(8), 1758; https://doi.org/10.3390/v15081758 - 17 Aug 2023
Cited by 10 | Viewed by 4434
Abstract
Our perception of viruses has been drastically evolving since the inception of the field of virology over a century ago. In particular, the discovery of giant viruses from the Nucleocytoviricota phylum marked a pivotal moment. Their previously concealed diversity and abundance unearthed an [...] Read more.
Our perception of viruses has been drastically evolving since the inception of the field of virology over a century ago. In particular, the discovery of giant viruses from the Nucleocytoviricota phylum marked a pivotal moment. Their previously concealed diversity and abundance unearthed an unprecedented complexity in the virus world, a complexity that called for new definitions and concepts. These giant viruses underscore the intricate interactions that unfold over time between viruses and their hosts, and are themselves suspected to have played a significant role as a driving force in the evolution of eukaryotes since the dawn of this cellular domain. Whether they possess exceptional relationships with their hosts or whether they unveil the actual depths of evolutionary connections between viruses and cells otherwise hidden in smaller viruses, the attraction giant viruses exert on the scientific community and beyond continues to grow. Yet, they still hold surprises. Indeed, the recent identification of mirusviruses connects giant viruses to herpesviruses, each belonging to distinct viral realms. This discovery substantially broadens the evolutionary landscape of Nucleocytoviricota. Undoubtedly, the years to come will reveal their share of surprises. Full article
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17 pages, 1927 KB  
Article
Origin and Early Diversification of the Papain Family of Cysteine Peptidases
by Dušan Kordiš and Vito Turk
Int. J. Mol. Sci. 2023, 24(14), 11761; https://doi.org/10.3390/ijms241411761 - 21 Jul 2023
Cited by 7 | Viewed by 3138
Abstract
Peptidases of the papain family play a key role in protein degradation, regulated proteolysis, and the host–pathogen arms race. Although the papain family has been the subject of many studies, knowledge about its diversity, origin, and evolution in Eukaryota, Bacteria, and Archaea is [...] Read more.
Peptidases of the papain family play a key role in protein degradation, regulated proteolysis, and the host–pathogen arms race. Although the papain family has been the subject of many studies, knowledge about its diversity, origin, and evolution in Eukaryota, Bacteria, and Archaea is limited; thus, we aimed to address these long-standing knowledge gaps. We traced the origin and expansion of the papain family with a phylogenomic analysis, using sequence data from numerous prokaryotic and eukaryotic proteomes, transcriptomes, and genomes. We identified the full complement of the papain family in all prokaryotic and eukaryotic lineages. Analysis of the papain family provided strong evidence for its early diversification in the ancestor of eukaryotes. We found that the papain family has undergone complex and dynamic evolution through numerous gene duplications, which produced eight eukaryotic ancestral paralogous C1A lineages during eukaryogenesis. Different evolutionary forces operated on C1A peptidases, including gene duplication, horizontal gene transfer, and gene loss. This study challenges the current understanding of the origin and evolution of the papain family and provides valuable insights into their early diversification. The findings of this comprehensive study provide guidelines for future structural and functional studies of the papain family. Full article
(This article belongs to the Special Issue Lysosomal Proteases and Their Inhibitors)
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17 pages, 3076 KB  
Article
The Evolution of tRNA Copy Number and Repertoire in Cellular Life
by Fenícia Brito Santos and Luiz-Eduardo Del-Bem
Genes 2023, 14(1), 27; https://doi.org/10.3390/genes14010027 - 22 Dec 2022
Cited by 19 | Viewed by 6893
Abstract
tRNAs are universal decoders that bridge the gap between transcriptome and proteome. They can also be processed into small RNA fragments with regulatory functions. In this work, we show that tRNA copy number is largely controlled by genome size in all cellular organisms, [...] Read more.
tRNAs are universal decoders that bridge the gap between transcriptome and proteome. They can also be processed into small RNA fragments with regulatory functions. In this work, we show that tRNA copy number is largely controlled by genome size in all cellular organisms, in contrast to what is observed for protein-coding genes that stop expanding between ~20,000 and ~35,000 loci per haploid genome in eukaryotes, regardless of genome size. Our analyses indicate that after the bacteria/archaea split, the tRNA gene pool experienced the evolution of increased anticodon diversity in the archaeal lineage, along with a tRNA gene size increase and mature tRNA size decrease. The evolution and diversification of eukaryotes from archaeal ancestors involved further expansion of the tRNA anticodon repertoire, additional increase in tRNA gene size and decrease in mature tRNA length, along with an explosion of the tRNA gene copy number that emerged coupled with accelerated genome size expansion. Our findings support the notion that macroscopic eukaryotes with a high diversity of cell types, such as land plants and vertebrates, independently evolved a high diversity of tRNA anticodons along with high gene redundancy caused by the expansion of the tRNA copy number. The results presented here suggest that the evolution of tRNA genes played important roles in the early split between bacteria and archaea, and in eukaryogenesis and the later emergence of complex eukaryotes, with potential implications in protein translation and gene regulation through tRNA-derived RNA fragments. Full article
(This article belongs to the Special Issue Genome-Wide Identifications: Recent Trends in Genomic Studies)
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20 pages, 1694 KB  
Review
Evolution of the Early Spliceosomal Complex—From Constitutive to Regulated Splicing
by Sonia Borao, José Ayté and Stefan Hümmer
Int. J. Mol. Sci. 2021, 22(22), 12444; https://doi.org/10.3390/ijms222212444 - 18 Nov 2021
Cited by 7 | Viewed by 6479
Abstract
Pre-mRNA splicing is a major process in the regulated expression of genes in eukaryotes, and alternative splicing is used to generate different proteins from the same coding gene. Splicing is a catalytic process that removes introns and ligates exons to create the RNA [...] Read more.
Pre-mRNA splicing is a major process in the regulated expression of genes in eukaryotes, and alternative splicing is used to generate different proteins from the same coding gene. Splicing is a catalytic process that removes introns and ligates exons to create the RNA sequence that codifies the final protein. While this is achieved in an autocatalytic process in ancestral group II introns in prokaryotes, the spliceosome has evolved during eukaryogenesis to assist in this process and to finally provide the opportunity for intron-specific splicing. In the early stage of splicing, the RNA 5′ and 3′ splice sites must be brought within proximity to correctly assemble the active spliceosome and perform the excision and ligation reactions. The assembly of this first complex, termed E-complex, is currently the least understood process. We focused in this review on the formation of the E-complex and compared its composition and function in three different organisms. We highlight the common ancestral mechanisms in S. cerevisiae, S. pombe, and mammals and conclude with a unifying model for intron definition in constitutive and regulated co-transcriptional splicing. Full article
(This article belongs to the Special Issue Splicing Modulators Which Affect Gene Expression)
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24 pages, 5233 KB  
Article
Evidence Supporting an Antimicrobial Origin of Targeting Peptides to Endosymbiotic Organelles
by Clotilde Garrido, Oliver D. Caspari, Yves Choquet, Francis-André Wollman and Ingrid Lafontaine
Cells 2020, 9(8), 1795; https://doi.org/10.3390/cells9081795 - 28 Jul 2020
Cited by 23 | Viewed by 5889
Abstract
Mitochondria and chloroplasts emerged from primary endosymbiosis. Most proteins of the endosymbiont were subsequently expressed in the nucleo-cytosol of the host and organelle-targeted via the acquisition of N-terminal presequences, whose evolutionary origin remains enigmatic. Using a quantitative assessment of their physico-chemical properties, [...] Read more.
Mitochondria and chloroplasts emerged from primary endosymbiosis. Most proteins of the endosymbiont were subsequently expressed in the nucleo-cytosol of the host and organelle-targeted via the acquisition of N-terminal presequences, whose evolutionary origin remains enigmatic. Using a quantitative assessment of their physico-chemical properties, we show that organelle targeting peptides, which are distinct from signal peptides targeting other subcellular compartments, group with a subset of antimicrobial peptides. We demonstrate that extant antimicrobial peptides target a fluorescent reporter to either the mitochondria or the chloroplast in the green alga Chlamydomonas reinhardtii and, conversely, that extant targeting peptides still display antimicrobial activity. Thus, we provide strong computational and functional evidence for an evolutionary link between organelle-targeting and antimicrobial peptides. Our results support the view that resistance of bacterial progenitors of organelles to the attack of host antimicrobial peptides has been instrumental in eukaryogenesis and in the emergence of photosynthetic eukaryotes. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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17 pages, 5034 KB  
Article
Gram-Positive Bacteria-Like DNA Binding Machineries Involved in Replication Initiation and Termination Mechanisms of Mimivirus
by Motohiro Akashi and Masaharu Takemura
Viruses 2019, 11(3), 267; https://doi.org/10.3390/v11030267 - 17 Mar 2019
Cited by 4 | Viewed by 5267
Abstract
The detailed mechanisms of replication initiation, termination and segregation events were not yet known in Acanthamoeba polyphaga mimivirus (APMV). Here, we show detailed bioinformatics-based analyses of chromosomal replication in APMV from initiation to termination mediated by proteins bound to specific DNA sequences. Using [...] Read more.
The detailed mechanisms of replication initiation, termination and segregation events were not yet known in Acanthamoeba polyphaga mimivirus (APMV). Here, we show detailed bioinformatics-based analyses of chromosomal replication in APMV from initiation to termination mediated by proteins bound to specific DNA sequences. Using GC/AT skew and coding sequence skew analysis, we estimated that the replication origin is located at 382 kb in the APMV genome. We performed homology-modeling analysis of the gamma domain of APMV-FtsK (DNA translocase coordinating chromosome segregation) related to FtsK-orienting polar sequences (KOPS) binding, suggesting that there was an insertion in the gamma domain which maintains the structure of the DNA binding motif. Furthermore, UvrD/Rep-like helicase in APMV was homologous to Bacillus subtilis AddA, while the chi-like quartet sequence 5′-CCGC-3′ was frequently found in the estimated ori region, suggesting that chromosomal replication of APMV is initiated via chi-like sequence recognition by UvrD/Rep-like helicase. Therefore, the replication initiation, termination and segregation of APMV are presumably mediated by DNA repair machineries derived from gram-positive bacteria. Moreover, the other frequently observed quartet sequence 5′-CGGC-3′ in the ori region was homologous to the mitochondrial signal sequence of replication initiation, while the comparison of quartet sequence composition in APMV/Rickettsia-genome showed significantly similar values, suggesting that APMV also conserves the mitochondrial replication system acquired from an ancestral genome of mitochondria during eukaryogenesis. Full article
(This article belongs to the Special Issue Virus Bioinformatics)
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18 pages, 540 KB  
Review
A Multi-Functional Tubulovesicular Network as the Ancestral Eukaryotic Endomembrane System
by Juan Carlos González-Sánchez, Ricardo Costa and Damien P. Devos
Biology 2015, 4(2), 264-281; https://doi.org/10.3390/biology4020264 - 24 Mar 2015
Cited by 5 | Viewed by 7982
Abstract
The origin of the eukaryotic endomembrane system is still the subject of much speculation. We argue that the combination of two recent hypotheses addressing the eukaryotic endomembrane’s early evolution supports the possibility that the ancestral membranes were organised as a multi-functional tubulovesicular network. [...] Read more.
The origin of the eukaryotic endomembrane system is still the subject of much speculation. We argue that the combination of two recent hypotheses addressing the eukaryotic endomembrane’s early evolution supports the possibility that the ancestral membranes were organised as a multi-functional tubulovesicular network. One of the potential selective advantages provided by this organisation was the capacity to perform endocytosis. This possibility is illustrated by membrane organisations observed in current organisms in the three domains of life. Based on this, we propose a coherent model of autogenous eukaryotic endomembrane system evolution in which mitochondria are involved at a late stage. Full article
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43 pages, 768 KB  
Essay
Primal Eukaryogenesis: On the Communal Nature of Precellular States, Ancestral to Modern Life
by Richard Egel
Life 2012, 2(1), 170-212; https://doi.org/10.3390/life2010170 - 23 Jan 2012
Cited by 18 | Viewed by 20295
Abstract
This problem-oriented, exploratory and hypothesis-driven discourse toward the unknown combines several basic tenets: (i) a photo-active metal sulfide scenario of primal biogenesis in the porespace of shallow sedimentary flats, in contrast to hot deep-sea hydrothermal vent conditions; (ii) an inherently complex communal system [...] Read more.
This problem-oriented, exploratory and hypothesis-driven discourse toward the unknown combines several basic tenets: (i) a photo-active metal sulfide scenario of primal biogenesis in the porespace of shallow sedimentary flats, in contrast to hot deep-sea hydrothermal vent conditions; (ii) an inherently complex communal system at the common root of present life forms; (iii) a high degree of internal compartmentalization at this communal root, progressively resembling coenocytic (syncytial) super-cells; (iv) a direct connection from such communal super-cells to proto-eukaryotic macro-cell organization; and (v) multiple rounds of micro-cellular escape with streamlined reductive evolution—leading to the major prokaryotic cell lines, as well as to megaviruses and other viral lineages. Hopefully, such nontraditional concepts and approaches will contribute to coherent and plausible views about the origins and early life on Earth. In particular, the coevolutionary emergence from a communal system at the common root can most naturally explain the vast discrepancy in subcellular organization between modern eukaryotes on the one hand and both archaea and bacteria on the other. Full article
(This article belongs to the Special Issue Origin of Life - Feature Papers)
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