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1.
  • Eme, Laura, et al. (author)
  • Inference and reconstruction of the heimdallarchaeial ancestry of eukaryotes
  • 2023
  • In: Nature. - : Springer Nature. - 0028-0836 .- 1476-4687. ; 618:7967, s. 992-
  • Journal article (peer-reviewed)abstract
    • In the ongoing debates about eukaryogenesis-the series of evolutionary events leading to the emergence of the eukaryotic cell from prokaryotic ancestors-members of the Asgard archaea play a key part as the closest archaeal relatives of eukaryotes(1). However, the nature and phylogenetic identity of the last common ancestor of Asgard archaea and eukaryotes remain unresolved(2-4). Here we analyse distinct phylogenetic marker datasets of an expanded genomic sampling of Asgard archaea and evaluate competing evolutionary scenarios using state-of-the-art phylogenomic approaches. We find that eukaryotes are placed, with high confidence, as a well-nested clade within Asgard archaea and as a sister lineage to Hodarchaeales, a newly proposed order within Heimdallarchaeia. Using sophisticated gene tree and species tree reconciliation approaches, we show that analogous to the evolution of eukaryotic genomes, genome evolution in Asgard archaea involved significantly more gene duplication and fewer gene loss events compared with other archaea. Finally, we infer that the last common ancestor of Asgard archaea was probably a thermophilic chemolithotroph and that the lineage from which eukaryotes evolved adapted to mesophilic conditions and acquired the genetic potential to support a heterotrophic lifestyle. Our work provides key insights into the prokaryote-to-eukaryote transition and a platform for better understanding the emergence of cellular complexity in eukaryotic cells.
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2.
  • Gentekaki, Eleni, et al. (author)
  • Extreme genome diversity in the hyper-prevalent parasitic eukaryote Blastocystis
  • 2017
  • In: PLoS biology. - : PUBLIC LIBRARY SCIENCE. - 1544-9173 .- 1545-7885. ; 15:9
  • Journal article (peer-reviewed)abstract
    • Blastocystis is the most prevalent eukaryotic microbe colonizing the human gut, infecting approximately 1 billion individuals worldwide. Although Blastocystis has been linked to intestinal disorders, its pathogenicity remains controversial because most carriers are asymptomatic. Here, the genome sequence of Blastocystis subtype (ST) 1 is presented and compared to previously published sequences for ST4 and ST7. Despite a conserved core of genes, there is unexpected diversity between these STs in terms of their genome sizes, guanine-cytosine (GC) content, intron numbers, and gene content. ST1 has 6,544 protein-coding genes, which is several hundred more than reported for ST4 and ST7. The percentage of proteins unique to each ST ranges from 6.2% to 20.5%, greatly exceeding the differences observed within parasite genera. Orthologous proteins also display extreme divergence in amino acid sequence identity between STs (i.e., 59%-61% median identity), on par with observations of the most distantly related species pairs of parasite genera. The STs also display substantial variation in gene family distributions and sizes, especially for protein kinase and protease gene families, which could reflect differences in virulence. It remains to be seen to what extent these inter-ST differences persist at the intra-ST level. A full 26% of genes in ST1 have stop codons that are created on the mRNA level by a novel polyadenylation mechanism found only in Blastocystis. Reconstructions of pathways and organellar systems revealed that ST1 has a relatively complete membrane-trafficking system and a near-complete meiotic toolkit, possibly indicating a sexual cycle. Unlike some intestinal protistan parasites, Blastocystis ST1 has near-complete de novo pyrimidine, purine, and thiamine biosynthesis pathways and is unique amongst studied stramenopiles in being able to metabolize alpha-glucans rather than beta-glucans. It lacks all genes encoding heme-containing cytochrome P450 proteins. Predictions of the mitochondrion-related organelle (MRO) proteome reveal an expanded repertoire of functions, including lipid, cofactor, and vitamin biosynthesis, as well as proteins that may be involved in regulating mitochondrial morphology and MRO/endoplasmic reticulum (ER) interactions. In sharp contrast, genes for peroxisome-associated functions are absent, suggesting Blastocystis STs lack this organelle. Overall, this study provides an important window into the biology of Blastocystis, showcasing significant differences between STs that can guide future experimental investigations into differences in their virulence and clarifying the roles of these organisms in gut health and disease.
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3.
  • Kang, Seungho, et al. (author)
  • The integrin-mediated adhesive complex in the ancestor of animals, fungi, and amoebae
  • 2021
  • In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 31:14, s. 3-3085
  • Journal article (peer-reviewed)abstract
    • Integrins are transmembrane receptors that activate signal transduction pathways upon extracellular matrix binding. The integrin-mediated adhesive complex (IMAC) mediates various cell physiological processes. Although the IMAC was thought to be specific to animals, in the past ten years these complexes were discovered in other lineages of Obazoa, the group containing animals, fungi, and several microbial eukaryotes. Very recently, many genomes and transcriptomes from Amoebozoa (the eukaryotic supergroup sister to Obazoa), other obazoans, orphan protist lineages, and the eukaryotes’ closest prokaryotic relatives, have become available. To increase the resolution of where and when IMAC proteins exist and have emerged, we surveyed these newly available genomes and transcriptomes for the presence of IMAC proteins. Our results highlight that many of these proteins appear to have evolved earlier in eukaryote evolution than previously thought and that co-option of this apparently ancient protein complex was key to the emergence of animal-type multicellularity. The role of the IMACs in amoebozoans is unknown, but they play critical adhesive roles in at least some unicellular organisms.
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4.
  • Aguilera-Campos, Karla Iveth, et al. (author)
  • Hydrogen metabolism : A eukaryote taps into the electron sink
  • 2022
  • In: Current biology : CB. - : Elsevier BV. - 1879-0445 .- 0960-9822. ; 32:1, s. 49-51
  • Journal article (peer-reviewed)abstract
    • The ability to harvest reducing power from molecular hydrogen was once considered a prokaryotic trait. New research challenges this notion by finding the first eukaryotic organism capable of oxidizing hydrogen.
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5.
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6.
  • Dharamshi, Jennah E., et al. (author)
  • Marine Sediments Illuminate Chlamydiae Diversity and Evolution
  • 2020
  • In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 30:6, s. 1032-1048.e7
  • Journal article (peer-reviewed)abstract
    • The bacterial phylum Chlamydiae is so far composed of obligate symbionts of eukaryotic hosts. Well known for Chlamydiaceae, pathogens of humans and other animals, Chlamydiae also include so-called environmental lineages that primarily infect microbial eukaryotes. Environmental surveys indicate that Chlamydiae are found in a wider range of environments than anticipated previously. However, the vast majority of this chlamydial diversity has been underexplored, biasing our current understanding of their biology, ecological importance, and evolution. Here, we report that previously undetected and active chlamydial lineages dominate microbial communities in deep anoxic marine sediments taken from the Arctic Mid-Ocean Ridge. Reaching relative abundances of up to 43% of the bacterial community, and a maximum diversity of 163 different species-level taxonomic units, these Chlamydiae represent important community members. Using genome-resolved metagenomics, we reconstructed 24 draft chlamydial genomes, expanding by over a third the known genomic diversity in this phylum. Phylogenomic analyses revealed several novel clades across the phylum, including a previously unknown sister lineage of the Chlamydiaceae, providing new insights into the origin of pathogenicity in this family. We were unable to identify putative eukaryotic hosts for these marine sediment chlamydiae, despite identifying genomic features that may be indicative of host-association. The high abundance and genomic diversity of Chlamydiae in these anoxic marine sediments indicate that some members could play an important, and thus far overlooked, ecological role in such environments and may indicate alternate lifestyle strategies.
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7.
  • Eme, Laura, et al. (author)
  • Archaea and the origin of eukaryotes
  • 2018
  • In: Nature Reviews Microbiology. - : Springer Nature. - 1740-1526 .- 1740-1534. ; 16:2
  • Journal article (peer-reviewed)abstract
    • This corrects the article DOI: 10.1038/nrmicro.2017.133.
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8.
  • Eme, Laura, et al. (author)
  • Archaea and the origin of eukaryotes
  • 2017
  • In: Nature Reviews Microbiology. - : Springer Science and Business Media LLC. - 1740-1526 .- 1740-1534. ; 15:12, s. 711-723
  • Research review (peer-reviewed)abstract
    • Woese and Fox's 1977 paper on the discovery of the Archaea triggered a revolution in the field of evolutionary biology by showing that life was divided into not only prokaryotes and eukaryotes. Rather, they revealed that prokaryotes comprise two distinct types of organisms, the Bacteria and the Archaea. In subsequent years, molecular phylogenetic analyses indicated that eukaryotes and the Archaea represent sister groups in the tree of life. During the genomic era, it became evident that eukaryotic cells possess a mixture of archaeal and bacterial features in addition to eukaryotic-specific features. Although it has been generally accepted for some time that mitochondria descend from endosymbiotic alphaproteobacteria, the precise evolutionary relationship between eukaryotes and archaea has continued to be a subject of debate. In this Review, we outline a brief history of the changing shape of the tree of life and examine how the recent discovery of a myriad of diverse archaeal lineages has changed our understanding of the evolutionary relationships between the three domains of life and the origin of eukaryotes. Furthermore, we revisit central questions regarding the process of eukaryogenesis and discuss what can currently be inferred about the evolutionary transition from the first to the last eukaryotic common ancestor.
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9.
  • Eme, Laura, et al. (author)
  • Life through the lens of metabolism
  • 2022
  • In: Nature Ecology and Evolution. - : Springer Science and Business Media LLC. - 2397-334X. ; 6:11, s. 1590-1590
  • Review (other academic/artistic)
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10.
  • Gallot-Lavallée, Lucie, et al. (author)
  • Massive intein content in Anaeramoeba reveals aspects of intein mobility in eukaryotes
  • 2023
  • In: Proceedings of the National Academy of Sciences of the United States of America. - : Proceedings of the National Academy of Sciences (PNAS). - 1091-6490 .- 0027-8424. ; 120:49
  • Journal article (peer-reviewed)abstract
    • Inteins are self-splicing protein elements found in viruses and all three domains of life. How the DNA encoding these selfish elements spreads within and between genomes is poorly understood, particularly in eukaryotes where inteins are scarce. Here, we show that the nuclear genomes of three strains of Anaeramoeba encode between 45 and 103 inteins, in stark contrast to four found in the most intein-rich eukaryotic genome described previously. The Anaeramoeba inteins reside in a wide range of proteins, only some of which correspond to intein-containing proteins in other eukaryotes, prokaryotes, and viruses. Our data also suggest that viruses have contributed to the spread of inteins in Anaeramoeba and the colonization of new alleles. The persistence of Anaeramoeba inteins might be partly explained by intragenomic movement of intein-encoding regions from gene to gene. Our intein dataset greatly expands the spectrum of intein-containing proteins and provides insights into the evolution of inteins in eukaryotes.
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11.
  • Gawryluk, Ryan M. R., et al. (author)
  • Diversity of electron transport chains in anaerobic protists
  • 2021
  • In: Biochimica et Biophysica Acta - Bioenergetics. - : Elsevier. - 0005-2728 .- 1879-2650. ; 1862:1
  • Journal article (peer-reviewed)abstract
    • Eukaryotic microbes (protists) that occupy low-oxygen environments often have drastically different mitochondrial metabolism compared to their aerobic relatives. A common theme among many anaerobic protists is the serial loss of components of the electron transport chain (ETC). Here, we discuss the diversity of the ETC across the tree of eukaryotes and review hypotheses for how ETCs are modified, and ultimately lost, in protists. We find that while protists have converged to some of the same metabolism as anaerobic animals, there are clear protist-specific strategies to thrive without oxygen.
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12.
  • Greening, Chris, et al. (author)
  • Minimal and hybrid hydrogenases are active from archaea
  • In: Cell. - 1097-4172. ; 187
  • Journal article (peer-reviewed)abstract
    • Microbial hydrogen (H 2) cycling underpins the diversity and functionality of diverse anoxic ecosystems. Among the three evolutionarily distinct hydrogenase superfamilies responsible, [FeFe] hydrogenases were thought to be restricted to bacteria and eukaryotes. Here, we show that anaerobic archaea encode diverse, active, and ancient lineages of [FeFe] hydrogenases through combining analysis of existing and new genomes with extensive biochemical experiments. [FeFe] hydrogenases are encoded by genomes of nine archaeal phyla and expressed by H 2-producing Asgard archaeon cultures. We report an ultraminimal hydrogenase in DPANN archaea that binds the catalytic H-cluster and produces H 2. Moreover, we identify and characterize remarkable hybrid complexes formed through the fusion of [FeFe] and [NiFe] hydrogenases in ten other archaeal orders. Phylogenetic analysis and structural modeling suggest a deep evolutionary history of hybrid hydrogenases. These findings reveal new metabolic adaptations of archaea, streamlined H 2 catalysts for biotechnological development, and a surprisingly intertwined evolutionary history between the two major H 2-metabolizing enzymes.
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13.
  • Jerlström-Hultqvist, Jon, 1982-, et al. (author)
  • A unique symbiosome in an anaerobic single-celled eukaryote
  • 2023
  • Other publication (other academic/artistic)abstract
    • Symbiotic relationships drive evolutionary change and are important sources of novelty. Here we demonstrate a highly structured syntrophic symbiosis between species of the anaerobic protist Anaeramoeba (Anaeramoebae, Metamonada) and bacterial ectosymbionts. We dissected this symbiosis with long-read metagenomics, transcriptomics of host and symbiont cells coupled with fluorescent in situ hybridization (FISH), and microscopy. Genome sequencing, phylogenomic analyses and FISH show that the symbionts belong to the Desulfobacteraceae and were acquired independently in two different Anaeramoeba species. We show that ectosymbionts likely reside deep within cell surface invaginations in a symbiosomal membrane network that is tightly associated with cytoplasmic hydrogenosomes. Metabolic reconstructions based on the genomes and transcriptomes of the symbionts suggest a highly evolved syntrophic interaction. Host hydrogenosomes likely produce hydrogen, acetate, and propionate that are consumed by the symbionts dissimilatory sulfate reduction, Wood-Ljungdahl and methylmalonyl pathways, respectively. Because the host genome sequences encode several vitamin B12-dependent enzymes but appear to lack the ability to biosynthesize this vitamin, we hypothesize that the symbionts supply their hosts with B12. We detected numerous lateral gene transfers from diverse bacteria to Anaeramoeba, including genes involved in oxygen defense and anaerobic metabolism. Gene families encoding membrane-trafficking components that regulate the phagosomal maturation machinery are notably expanded in Anaeramoeba spp. and may be involved in organizing and/or stabilizing the symbiosomal membrane system. Overall, the Anaeramoebae have evolved a dynamic symbiosome comprised of a vacuolar system that facilitates positioning and maintenance of sulfate-reducing bacterial ectosymbionts.
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14.
  • Jiménez-González, Alejandro, et al. (author)
  • The Hexamita inflata genome reveals new trends in diplomonads evolution
  • Other publication (other academic/artistic)abstract
    • Diplomonads are a group of flagellated protists found in oxygen-poor environments. The group is suitable to study transitions between lifestyles, because it contains both parasitic and free-living members. A transcriptome study of the free-living diplomonad Trepomonas sp. PC1 showed that many genes associated with the lifestyle had been acquired via lateral gene transfer, suggesting a reversion from a host-associated to a free-living lifestyle. Here, we present the draft genome of Hexamita inflata, the first of a free-living diplomonad. A comparative analysis of the metabolic capacity shows that H. inflata shares free-living adaptations with Trepomonas sp. PC. Important enzymes for the metabolism of nucleotides were acquired by their common ancestor, suggesting a shared reduced dependence on nucleotide salvage. We also find metabolic differences between the free-living diplomonads, suggesting that they have taken their own evolutionary paths. For example, H. inflata is the first diplomonad able to synthetize both the non-protein thiols L-cysteine and glutathione, and it has the most elaborate pathway for arsenic detoxification. These findings indicate that H. inflata is able to withstand higher levels of arsenic and reactive oxygen species than any other studied diplomonad.
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15.
  • Karnkowska, Anna, et al. (author)
  • The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion
  • 2019
  • In: Molecular biology and evolution. - : OXFORD UNIV PRESS. - 0737-4038 .- 1537-1719. ; 36:10, s. 2292-2312
  • Journal article (peer-reviewed)abstract
    • The discovery that the protist Monocercomonoides exilis completely lacks mitochondria demonstrates that these organelles are not absolutely essential to eukaryotic cells. However, the degree to which the metabolism and cellular systems of this organism have adapted to the loss of mitochondria is unknown. Here, we report an extensive analysis of the M. exilis genome to address this question. Unexpectedly, we find that M. exilis genome structure and content is similar in complexity to other eukaryotes and less "reduced" than genomes of some other protists from the Metamonada group to which it belongs. Furthermore, the predicted cytoskeletal systems, the organization of endomembrane systems, and biosynthetic pathways also display canonical eukaryotic complexity. The only apparent preadaptation that permitted the loss of mitochondria was the acquisition of the SUF system for Fe-S cluster assembly and the loss of glycine cleavage system. Changes in other systems, including in amino acid metabolism and oxidative stress response, were coincident with the loss of mitochondria but are likely adaptations to the microaerophilic and endobiotic niche rather than the mitochondrial loss per se. Apart from the lack of mitochondria and peroxisomes, we show that M. exilis is a fully elaborated eukaryotic cell that is a promising model system in which eukaryotic cell biology can be investigated in the absence of mitochondria.
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16.
  • Leger, Michelle M., et al. (author)
  • Demystifying Eukaryote Lateral Gene Transfer
  • 2018
  • In: Bioessays. - : Wiley. - 0265-9247 .- 1521-1878. ; 40:5
  • Journal article (peer-reviewed)abstract
    • In a recent BioEssays paper [W. F. Martin, BioEssays 2017, 39, 1700115], William Martin sharply criticizes evolutionary interpretations that involve lateral gene transfer (LGT) into eukaryotic genomes. Most published examples of LGTs in eukaryotes, he suggests, are in fact contaminants, ancestral genes that have been lost from other extant lineages, or the result of artefactual phylogenetic inferences. Martin argues that, except for transfers that occurred from endosymbiotic organelles, eukaryote LGT is insignificant. Here, in reviewing this field, we seek to correct some of the misconceptions presented therein with regard to the evidence for LGT in eukaryotes.
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17.
  • Leger, Michelle M., et al. (author)
  • Organelles that illuminate the origins of Trichomonas hydrogenosomes and Giardia mitosomes
  • 2017
  • In: NATURE ECOLOGY & EVOLUTION. - : Springer Science and Business Media LLC. - 2397-334X. ; 1:4
  • Journal article (peer-reviewed)abstract
    • Many anaerobic microbial parasites possess highly modified mitochondria known as mitochondrion-related organelles (MROs). The best-studied of these are the hydrogenosomes of Trichomonas vaginalis and Spironucleus salmonicida, which produce ATP anaerobically through substrate-level phosphorylation with concomitant hydrogen production; and the mitosomes of Giardia intestinalis, which are functionally reduced and lack any role in ATP production. Howewer, to understand the metabolic specializations that these MROs underwent in adaptation to parasitism, data from their free-living relatives are needed. Here, we present a large-scale comparative transcriptomic study of MROs across a major eukaryotic group, Metamonada, examining lineage-specific gain and loss of metabolic functions in the MROs of Trichomonas, Giardia, Spironucleus and their free-living relatives. Our analyses uncover a complex history of ATP production machinery in diplomonads such as Giardia, and their closest relative, Dysnectes; and a correlation between the glycine cleavage machinery and lifestyles. Our data further suggest the existence of a previously undescribed biochemical class of MRO that generates hydrogen but is incapable of ATP synthesis.
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18.
  • Milner, David S, et al. (author)
  • A functional bacteria-derived restriction modification system in the mitochondrion of a heterotrophic protist
  • 2021
  • In: PLoS Biology. - : Public Library of Science (PLoS). - 1545-7885. ; 19:4
  • Journal article (peer-reviewed)abstract
    • The overarching trend in mitochondrial genome evolution is functional streamlining coupled with gene loss; therefore, gene acquisition by mitochondria is considered to be exceedingly rare. Selfish elements in the form of self-splicing introns occur in many organellar genomes, but the wider diversity of selfish elements, and how they persist in the DNA of organelles, has not been explored. In the mitochondrial genome of a marine heterotrophic katablepharid protist, we identify a functional type II restriction modification (RM) system originating from a horizontal gene transfer (HGT) event involving bacteria related to flavobacteria. This RM system consists of an HpaII-like endonuclease and a cognate cytosine methyltransferase (CM). We demonstrate that these proteins are functional by heterologous expression in both bacterial and eukaryotic cells. These results suggest that a mitochondrial-encoded RM system can function as a toxin-antitoxin selfish element and that such elements could be co-opted by eukaryotic genomes to drive biased organellar inheritance.
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19.
  • Motyčková, Alžběta, et al. (author)
  • Adaptation of the late ISC pathway in the anaerobic mitochondrial organelles of Giardia intestinalis
  • 2023
  • In: PLoS Pathogens. - : Public Library of Science (PLoS). - 1553-7374 .- 1553-7366. ; 19:10
  • Journal article (peer-reviewed)abstract
    • Mitochondrial metabolism is entirely dependent on the biosynthesis of the [4Fe-4S] clusters, which are part of the subunits of the respiratory chain. The mitochondrial late ISC pathway mediates the formation of these clusters from simpler [2Fe-2S] molecules and transfers them to client proteins. Here, we characterized the late ISC pathway in one of the simplest mitochondria, mitosomes, of the anaerobic protist Giardia intestinalis that lost the respiratory chain and other hallmarks of mitochondria. In addition to IscA2, Nfu1 and Grx5 we identified a novel BolA1 homologue in G. intestinalis mitosomes. It specifically interacts with Grx5 and according to the high-affinity pulldown also with other core mitosomal components. Using CRISPR/Cas9 we were able to establish full bolA1 knock out, the first cell line lacking a mitosomal protein. Despite the ISC pathway being the only metabolic role of the mitosome no significant changes in the mitosome biology could be observed as neither the number of the mitosomes or their capability to form [2Fe-2S] clusters in vitro was affected. We failed to identify natural client proteins that would require the [2Fe-2S] or [4Fe-4S] cluster within the mitosomes, with the exception of [2Fe-2S] ferredoxin, which is itself part of the ISC pathway. The overall uptake of iron into the cellular proteins remained unchanged as also observed for the grx5 knock out cell line. The pull-downs of all late ISC components were used to build the interactome of the pathway showing specific position of IscA2 due to its interaction with the outer mitosomal membrane proteins. Finally, the comparative analysis across Metamonada species suggested that the adaptation of the late ISC pathway identified in G. intestinalis occurred early in the evolution this of supergroup of eukaryotes.
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20.
  • Najdrova, Vladimira, et al. (author)
  • The evolution of the Puf superfamily of proteins across the tree of eukaryotes
  • 2020
  • In: BMC Biology. - : Springer Science and Business Media LLC. - 1741-7007. ; 18:1
  • Journal article (peer-reviewed)abstract
    • BackgroundEukaryotic gene expression is controlled by a number of RNA-binding proteins (RBP), such as the proteins from the Puf (Pumilio and FBF) superfamily (PufSF). These proteins bind to RNA via multiple Puf repeat domains, each of which specifically recognizes a single RNA base. Recently, three diversified PufSF proteins have been described in model organisms, each of which is responsible for the maturation of ribosomal RNA or the translational regulation of mRNAs; however, less is known about the role of these proteins across eukaryotic diversity.ResultsHere, we investigated the distribution and function of PufSF RBPs in the tree of eukaryotes. We determined that the following PufSF proteins are universally conserved across eukaryotes and can be broadly classified into three groups: (i) Nop9 orthologues, which participate in the nucleolar processing of immature 18S rRNA; (ii) ‘classical’ Pufs, which control the translation of mRNA; and (iii) PUM3 orthologues, which are involved in the maturation of 7S rRNA. In nearly all eukaryotes, the rRNA maturation proteins, Nop9 and PUM3, are retained as a single copy, while mRNA effectors (‘classical’ Pufs) underwent multiple lineage-specific expansions. We propose that the variation in number of ‘classical’ Pufs relates to the size of the transcriptome and thus the potential mRNA targets. We further distinguished full set of PufSF proteins in divergent metamonad Giardia intestinalis and initiated their cellular and biochemical characterization.ConclusionsOur data suggest that the last eukaryotic common ancestor (LECA) already contained all three types of PufSF proteins and that ‘classical’ Pufs then underwent lineage-specific expansions.
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21.
  • Narrowe, Adrienne B., et al. (author)
  • Complex Evolutionary History of Translation Elongation Factor 2 and Diphthamide Biosynthesis in Archaea and Parabasalids
  • 2018
  • In: Genome Biology and Evolution. - : Oxford University Press (OUP). - 1759-6653. ; 10:9, s. 2380-2393
  • Journal article (peer-reviewed)abstract
    • Diphthamide is a modified histidine residue which is uniquely present in archaeal and eukaryotic elongation factor 2 (EF-2), an essential GTPase responsible for catalyzing the coordinated translocation of tRNA and mRNA through the ribosome. In part due to the role of diphthamide in maintaining translational fidelity, it was previously assumed that diphthamide biosynthesis genes (dph) are conserved across all eukaryotes and archaea. Here, comparative analysis of new and existing genomes reveals that some archaea (i.e., members of the Asgard superphylum, Geoarchaea, and Korarchaeota) and eukaryotes (i.e., parabasalids) lack dph. In addition, while EF-2 was thought to exist as a single copy in archaea, many of these dph-lacking archaeal genomes encode a second EF-2 paralog missing key residues required for diphthamide modification and for normal translocase function, perhaps suggesting functional divergence linked to loss of diphthamide biosynthesis. Interestingly, some Heimdallarchaeota previously suggested to be most closely related to the eukaryotic ancestor maintain dph genes and a single gene encoding canonical EF-2. Our findings reveal that the ability to produce diphthamide, once thought to be a universal feature in archaea and eukaryotes, has been lost multiple times during evolution, and suggest that anticipated compensatory mechanisms evolved independently.
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22.
  • Onuţ-Brännström, Ioana, et al. (author)
  • A Mitosome With Distinct Metabolism in the Uncultured Protist Parasite Paramikrocytos canceri (Rhizaria, Ascetosporea)
  • 2023
  • In: Genome Biology and Evolution. - : Oxford University Press. - 1759-6653. ; 15:3
  • Journal article (peer-reviewed)abstract
    • Ascetosporea are endoparasites of marine invertebrates that include economically important pathogens of aquaculture species. Owing to their often-minuscule cell sizes, strict intracellular lifestyle, lack of cultured representatives and minimal availability of molecular data, these unicellular parasites remain poorly studied. Here, we sequenced and assembled the genome and transcriptome of Paramikrocytos canceri, an endoparasite isolated from the European edible crab Cancer pagurus. Using bioinformatic predictions, we show that P. canceri likely possesses a mitochondrion-related organelle (MRO) with highly reduced metabolism, resembling the mitosomes of other parasites but with key differences. Like other mitosomes, this MRO is predicted to have reduced metabolic capacity and lack an organellar genome and function in iron–sulfur cluster (ISC) pathway-mediated Fe–S cluster biosynthesis. However, the MRO in P. canceri is uniquely predicted to produce ATP via a partial glycolytic pathway and synthesize phospholipids de novo through the CDP-DAG pathway. Heterologous gene expression confirmed that proteins from the ISC and CDP-DAG pathways retain mitochondrial targeting sequences that are recognized by yeast mitochondria. This represents a unique combination of metabolic pathways in an MRO, including the first reported case of a mitosome-like organelle able to synthesize phospholipids de novo. Some of these phospholipids, such as phosphatidylserine, are vital in other protist endoparasites that invade their host through apoptotic mimicry.
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23.
  • Sjöberg, Susanne, et al. (author)
  • Microbe-Mediated Mn Oxidation - A Proposed Model of Mineral Formation
  • 2021
  • In: Minerals. - : MDPI. - 2075-163X. ; 11:10
  • Journal article (peer-reviewed)abstract
    • Manganese oxides occur in a wide range of environmental settings either as coatings on rocks, sediment, and soil particles, or as discrete grains. Although the production of biologically mediated Mn oxides is well established, relatively little is known about microbial-specific strategies for utilizing Mn in the environment and how these affect the morphology, structure, and chemistry of associated mineralizations. Defining such strategies and characterizing the associated mineral properties would contribute to a better understanding of their impact on the local environment and possibly facilitate evaluation of biogenicity in recent and past Mn accumulations. Here, we supplement field data from a Mn rock wall deposit in the Ytterby mine, Sweden, with data retrieved from culturing Mn oxidizers isolated from this site. Microscopic and spectroscopic techniques are used to characterize field site products and Mn precipitates generated by four isolated bacteria (Hydrogenophaga sp., Pedobacter sp., Rhizobium sp., and Nevskia sp.) and one fungal-bacterial co-culture (Cladosporium sp.-Hydrogenophaga sp. Rhizobium sp.-Nevskia sp.). Two of the isolates (Pedobacter sp. and Nevskia sp.) are previously unknown Mn oxidizers. At the field site, the onset of Mn oxide mineralization typically occurs in areas associated with globular wad-like particles and microbial traces. The particles serve as building blocks in the majority of the microstructures, either forming the base for further growth into laminated dendrites-botryoids or added as components to an existing structure. The most common nanoscale structures are networks of Mn oxide sheets structurally related to birnessite. The sheets are typically constructed of very few layers and elongated along the octahedral chains. In places, the sheets bend and curl under to give a scroll-like appearance. Culturing experiments show that growth conditions (biofilm or planktonic) affect the ability to oxidize Mn and that taxonomic affiliation influences crystallite size, structure, and average oxidation state as well as the onset location of Mn precipitation.
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24.
  • Sjöberg, Susanne, et al. (author)
  • Microbiomes in a manganese oxide producing ecosystem in the Ytterby mine, Sweden : impact on metal mobility
  • 2020
  • In: FEMS Microbiology Ecology. - : Oxford University Press. - 0168-6496 .- 1574-6941. ; 96:11
  • Journal article (peer-reviewed)abstract
    • Microbe-mediated precipitation of Mn-oxides enriched in rare earth elements (REE) and other trace elements was discovered in tunnels leading to the main shaft of the Ytterby mine, Sweden. Defining the spatial distribution of microorganisms and elements in this ecosystem provide a better understanding of specific niches and parameters driving the emergence of these communities and associated mineral precipitates. Along with elemental analyses, high-throughput sequencing of the following four subsystems were conducted: (1) water seeping from a rock fracture into the tunnel, (2) Mn-oxides and associated biofilm; referred to as the Ytterby Black Substance (YBS) biofilm (3) biofilm forming bubbles on the Mn-oxides; referred to as the bubble biofilm, and (4) fracture water that has passed through the biofilms. Each subsystem hosts a specific collection of microorganisms. Differentially abundant bacteria in the YBS biofilm were identified within the Rhizobiales (e.g. Pedomicrobium), PLTA13 Gammaproteobacteria, Pirellulaceae, Hyphomonadaceae, Blastocatellia and Nitrospira. These taxa, likely driving the Mn-oxide production, were not detected in the fracture water. This biofilm binds Mn, REE and other trace elements in an efficient, dynamic process, as indicated by substantial depletion of these metals from the fracture water as it passes through the Mn deposit zone. Microbe-mediated oxidation of Mn(II) and formation of Mn(III/IV)-oxides can thus have considerable local environmental impact by removing metals from aquatic environments.
  •  
25.
  • Spang, Anja, et al. (author)
  • Evolving Perspective on the Origin and Diversification of Cellular Life and the Virosphere
  • 2022
  • In: Genome Biology and Evolution. - : Oxford University Press (OUP). - 1759-6653. ; 14:6
  • Journal article (peer-reviewed)abstract
    • The tree of life (TOL) is a powerful framework to depict the evolutionary history of cellular organisms through time, from our microbial origins to the diversification of multicellular eukaryotes that shape the visible biosphere today. During the past decades, our perception of the TOL has fundamentally changed, in part, due to profound methodological advances, which allowed a more objective approach to studying organismal and viral diversity and led to the discovery of major new branches in the TOL as well as viral lineages. Phylogenetic and comparative genomics analyses of these data have, among others, revolutionized our understanding of the deep roots and diversity of microbial life, the origin of the eukaryotic cell, eukaryotic diversity, as well as the origin, and diversification of viruses. In this review, we provide an overview of some of the recent discoveries on the evolutionary history of cellular organisms and their viruses and discuss a variety of complementary techniques that we consider crucial for making further progress in our understanding of the TOL and its interconnection with the virosphere.
  •  
26.
  • Spang, Anja, et al. (author)
  • Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism
  • 2019
  • In: Nature Microbiology. - : NATURE PUBLISHING GROUP. - 2058-5276. ; 4:7, s. 1138-1148
  • Journal article (peer-reviewed)abstract
    • The origin of eukaryotes represents an unresolved puzzle in evolutionary biology. Current research suggests that eukaryotes evolved from a merger between a host of archaeal descent and an alphaproteobacterial endosymbiont. The discovery of the Asgard archaea, a proposed archaeal superphylum that includes Lokiarchaeota, Thorarchaeota, Odinarchaeota and Heimdallarchaeota suggested to comprise the closest archaeal relatives of eukaryotes, has helped to elucidate the identity of the putative archaeal host. Whereas Lokiarchaeota are assumed to employ a hydrogen-dependent metabolism, little is known about the metabolic potential of other members of the Asgard superphylum. We infer the central metabolic pathways of Asgard archaea using comparative genomics and phylogenetics to be able to refine current models for the origin of eukaryotes. Our analyses indicate that Thorarchaeota and Lokiarchaeota encode proteins necessary for carbon fixation via the Wood-Ljungdahl pathway and for obtaining reducing equivalents from organic substrates. By contrast, Heimdallarchaeum LC2 and LC3 genomes encode enzymes potentially enabling the oxidation of organic substrates using nitrate or oxygen as electron acceptors. The gene repertoire of Heimdallarchaeum AB125 and Odinarchaeum indicates that these organisms can ferment organic substrates and conserve energy by coupling ferredoxin reoxidation to respiratory proton reduction. Altogether, our genome analyses suggest that Asgard representatives are primarily organoheterotrophs with variable capacity for hydrogen consumption and production. On this basis, we propose the 'reverse flow model', an updated symbiogenetic model for the origin of eukaryotes that involves electron or hydrogen flow from an organoheterotrophic archaeal host to a bacterial symbiont.
  •  
27.
  • Stairs, Courtney W, et al. (author)
  • Anaeramoebae are a divergent lineage of eukaryotes that shed light on the transition from anaerobic mitochondria to hydrogenosomes
  • 2021
  • In: Current Biology. - : Elsevier. - 0960-9822 .- 1879-0445. ; 31:24, s. 5605-5612.e5
  • Journal article (peer-reviewed)abstract
    • Discoveries of diverse microbial eukaryotes and their inclusion in comprehensive phylogenomic analyses have crucially re-shaped the eukaryotic tree of life in the 21st century.(1) At the deepest level, eukaryotic diversity comprises 9-10 "supergroups." One of these supergroups, the Metamonada, is particularly important to our understanding of the evolutionary dynamics of eukaryotic cells, including the remodeling of mitochondrial function. All metamonads thrive in low-oxygen environments and lack classical aerobic mitochondria, instead possessing mitochondrion-related organelles (MROs) with metabolisms that are adapted to low-oxygen conditions. These MROs lack an organellar genome, do not participate in the Krebs cycle and oxidative phosphorylation,(2) and often synthesize ATP by substrate-level phosphorylation coupled to hydrogen production.(3,4) The events that occurred during the transition from an oxygen-respiring mitochondrion to a functionally streamlined MRO early in metamonad evolution remain largely unknown. Here, we report transcriptomes of two recently described, enigmatic, anaerobic protists from the genus Anaeramoeba.(5) Using phylogenomic analysis, we show that these species represent a divergent, phylum-level lineage in the tree of metamonads, emerging as a sister group of the Parabasalia and reordering the deep branching order of the metamonad tree. Metabolic reconstructions of the Anaeramoeba MROs reveal many "classical" mitochondrial features previously not seen in metamonads, including a disulfide relay import system, propionate production, and amino acid metabolism. Our findings suggest that the cenancestor of Metamonada likely had MROs with more classical mitochondrial features than previously anticipated and demonstrate how discoveries of novel lineages of high taxonomic rank continue to transform our understanding of early eukaryote evolution.
  •  
28.
  • Stairs, Courtney W., et al. (author)
  • Chlamydial contribution to anaerobic metabolism during eukaryotic evolution
  • 2020
  • In: Science Advances. - : AMER ASSOC ADVANCEMENT SCIENCE. - 2375-2548. ; 6:35
  • Journal article (peer-reviewed)abstract
    • The origin of eukaryotes is a major open question in evolutionary biology. Multiple hypotheses posit that eukaryotes likely evolved from a syntrophic relationship between an archaeon and an alphaproteobacterium based on H-2 exchange. However, there are no strong indications that modern eukaryotic H-2 metabolism originated from archaea or alphaproteobacteria. Here, we present evidence for the origin of H-2 metabolism genes in eukaryotes from an ancestor of the Anoxychlamydiales-a group of anaerobic chlamydiae, newly described here, from marine sediments. Among Chlamydiae, these bacteria uniquely encode genes for H-2 metabolism and other anaerobiosis-associated pathways. Phylogenetic analyses of several components of H-2 metabolism reveal that Anoxychlamydiales homologs are the closest relatives to eukaryotic sequences. We propose that an ancestor of the Anoxychlamydiales contributed these key genes during the evolution of eukaryotes, supporting a mosaic evolutionary origin of eukaryotic metabolism.
  •  
29.
  • Stairs, Courtney W., et al. (author)
  • Oxygen induces the expression of invasion and stress response genes in the anaerobic salmon parasite Spironucleus salmonicida
  • 2019
  • In: BMC Biology. - : BioMed Central (BMC). - 1741-7007. ; 17:1
  • Journal article (peer-reviewed)abstract
    • Background: Spironucleus salmonicida is an anaerobic parasite that can cause systemic infections in Atlantic salmon. Unlike other diplomonad parasites, such as the human pathogen Giardia intestinalis, Spironucleus species can infiltrate the blood stream of their hosts eventually colonizing organs, skin and gills. How this presumed anaerobe can persist and invade oxygenated tissues, despite having a strictly anaerobic metabolism, remains elusive.Results: To investigate how S. salmonicida response to oxygen stress, we performed RNAseq transcriptomic analyses of cells grown in the presence of oxygen or antioxidant-free medium. We found that over 20% of the transcriptome is differentially regulated in oxygen (1705 genes) and antioxidant-depleted (2280 genes) conditions. These differentially regulated transcripts encode proteins related to anaerobic metabolism, cysteine and Fe-S cluster biosynthesis, as well as a large number of proteins of unknown function. S. salmonicida does not encode genes involved in the classical elements of oxygen metabolism (e.g., catalases, superoxide dismutase, glutathione biosynthesis, oxidative phosphorylation). Instead, we found that genes encoding bacterial-like oxidoreductases were upregulated in response to oxygen stress. Phylogenetic analysis revealed some of these oxygen-responsive genes (e.g., nadh oxidase, rubrerythrin, superoxide reductase) are rare in eukaryotes and likely derived from lateral gene transfer (LGT) events into diplomonads from prokaryotes. Unexpectedly, we observed that many host evasion- and invasion-related genes were also upregulated under oxidative stress suggesting that oxygen might be an important signal for pathogenesis.Conclusion: While oxygen is toxic for related organisms, such as G. intestinalis, we find that oxygen is likely a gene induction signal for host invasion- and evasion-related pathways in S. salmonicida. These data provide the first molecular evidence for how S. salmonicida could tolerate oxic host environments and demonstrate how LGT can have a profound impact on the biology of anaerobic parasites.
  •  
30.
  • Stairs, Courtney W., et al. (author)
  • The Archaeal Roots of the Eukaryotic Dynamic Actin Cytoskeleton
  • 2020
  • In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 30:10, s. R521-R526
  • Research review (peer-reviewed)abstract
    • It is generally well accepted that eukaryotes evolved from the symbiosis of an archaeal host cell and an alphaproteobacterium, a union that ultimately gave rise to the complex, eukaryotic cells we see today. However, the catalyst of this merger, the exact nature of the cellular biology of either partner, or how this event spawned the vast majority of complex life on Earth remains enigmatic. In recent years, the discovery of the Asgard archaea, the closest known prokaryotic relatives of eukaryotes, has been monumental for addressing these unanswered questions. These prokaryotes seem to encode an unprecedented number of genes related to features typically descriptive of eukaryotes, including intracellular trafficking, vesicular transport and a dynamic actin-based cytoskeleton. Collectively, these features imply that the Asgard archaea have the potential for cellular complexity previously thought to be unique to eukaryotes. Here, we review the most recent advances in our understanding of the archaeal cytoskeleton and its implications for determining the origin of eukaryotic cellular complexity.
  •  
31.
  • Williams, Shelby K., et al. (author)
  • Extreme mitochondrial reduction in a novel group of free-living metamonads
  • 2023
  • Other publication (other academic/artistic)abstract
    • Metamonads are a diverse group of heterotrophic microbial eukaryotes adapted to living in hypoxic environments. All metamonads but one harbour metabolically altered ‘mitochondrion-related organelles’ (MROs) with reduced functions relative to aerobic mitochondria, however the degree of reduction varies markedly over the metamonad tree. To further investigate metamonad MRO diversity, we generated high quality draft genomes, transcriptomes, and predicted proteomes for five recently discovered free-living metamonads. Phylogenomic analyses place these organisms in a clade sister to the Fornicata – a group of metamonads that includes parasitic and free-living diplomonads and Carpediemonas-like organisms. Extensive bioinformatic analyses of the manually curated gene models showed that these organisms have extremely reduced MROs in comparison to other free-living metamonads. Loss of the mitochondrial iron-sulfur cluster (ISC) assembly system in some organisms in this group appears to be linked to the acquisition in their common ancestral lineage of a SUF-like minimal system (SMS) Fe/S cluster pathway through lateral gene transfer (LGT). One of the isolates, named ‘RC’, appears to have undergone even more drastic mitochondrial reduction losing almost all other detectable MRO-related functions. The extreme mitochondrial reduction observed within this free-living anaerobic protistan clade is unprecedented and demonstrates that mitochondrial functions, under some conditions, can be almost completely lost even in free-living organisms.
  •  
32.
  • Zarsky, Vojtech, et al. (author)
  • The Mastigamoeba balamuthi Genome and the Nature of the Free-Living Ancestor of Entamoeba
  • 2021
  • In: Molecular biology and evolution. - : Oxford University Press. - 0737-4038 .- 1537-1719. ; 38:6, s. 2240-2259
  • Journal article (peer-reviewed)abstract
    • The transition of free-living organisms to parasitic organisms is a mysterious process that occurs in all major eukaryotic lineages. Parasites display seemingly unique features associated with their pathogenicity; however, it is important to distinguish ancestral preconditions to parasitism from truly new parasite-specific functions. Here, we sequenced the genome and transcriptome of anaerobic free-living Mastigamoeba balamuthi and performed phylogenomic analysis of four related members of the Archamoebae, including Entamoeba histolytica, an important intestinal pathogen of humans. We aimed to trace gene histories throughout the adaptation of the aerobic ancestor of Archamoebae to anaerobiosis and throughout the transition from a free-living to a parasitic lifestyle. These events were associated with massive gene losses that, in parasitic lineages, resulted in a reduction in structural features, complete losses of some metabolic pathways, and a reduction in metabolic complexity. By reconstructing the features of the common ancestor of Archamoebae, we estimated preconditions for the evolution of parasitism in this lineage. The ancestor could apparently form chitinous cysts, possessed proteolytic enzyme machinery, compartmentalized the sulfate activation pathway in mitochondrion-related organelles, and possessed the components for anaerobic energy metabolism. After the split of Entamoebidae, this lineage gained genes encoding surface membrane proteins that are involved in host-parasite interactions. In contrast, gene gains identified in the M. balamuthi lineage were predominantly associated with polysaccharide catabolic processes. A phylogenetic analysis of acquired genes suggested an essential role of lateral gene transfer in parasite evolution (Entamoeba) and in adaptation to anaerobic aquatic sediments (Mastigamoeba).
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