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  • 1.
    Hoeppner, Marc P.
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    White, Simon
    Jeffares, Daniel C.
    Poole, Anthony M.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Evolutionarily Stable Assiciation of Intronic snoRNAs and microRNAs with Their Host Genes2009In: Genome Biology and Evolution, ISSN 1759-6653, Vol. 1, no 1, p. 420-428Article in journal (Refereed)
    Abstract [en]

    Small nucleolar RNAs (snoRNAs) and microRNAs (miRNAs) are integral to a range of processes, including ribosome biogenesis and gene regulation. Some are intron encoded, and this organization may facilitate coordinated coexpression of host gene and RNA. However, snoRNAs and miRNAs are known to be mobile, so intron-RNA associations may not be evolutionarily stable. We have used genome alignments across 11 mammals plus chicken to examine positional orthology of snoRNAs and miRNAs and report that 21% of annotated snoRNAs and 11% of miRNAs are positionally conserved across mammals. Among RNAs traceable to the bird–mammal common ancestor, 98% of snoRNAs and 76% of miRNAs are intronic. Comparison of the most evolutionarily stable mammalian intronic snoRNAs with those positionally conserved among primates reveals that the former are more overrepresented among host genes involved in translation or ribosome biogenesis and are more broadly and highly expressed. This stability is likely attributable to a requirement for overlap between host gene and intronic snoRNA expression profiles, consistent with an ancestral role in ribosome biogenesis. In contrast, whereas miRNA positional conservation is comparable to that observed for snoRNAs, intronic miRNAs show no obvious association with host genes of a particular functional category, and no statistically significant differences in host gene expression are found between those traceable to mammalian or primate ancestors. Our results indicate evolutionarily stable associations of numerous intronic snoRNAs and miRNAs and their host genes, with probable continued diversification of snoRNA function from an ancestral role in ribosome biogenesis.

  • 2.
    Hoeppner, Marc Patrick
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Gardner, Paul P.
    Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus.
    Poole, Anthony M.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Comparative analysis of RNA families reveals distinct repertoires for each domain of lifeManuscript (preprint) (Other academic)
    Abstract [en]

    Some RNAs may date back to an RNA-rich period in the early evolution of life, butmany RNAs are thought to have more recent evolutionary origins. To chart the broadevolutionary history of known RNA families, we performed comparative genomicanalysis of over 3 million RNA annotations spanning 1446 families from the Rfam 10database. We report that 99% of known RNA families are restricted to a singledomain of life, revealing discrete repertoires for each domain. For the 1% of RNAfamilies/clans present in more than one domain, over half show evidence ofhorizontal gene transfer (HGT), and only six RNAs directly trace to the LastUniversal Common Ancestor (LUCA). These results indicate that cellular RNAinfrastructure evolves in a domain-specific manner.

  • 3.
    Hoeppner, Marc Patrick
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Poole, Anthony M.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Comparative Genomics of Eukaryotic Small Nucleolar RNAs Reveals Deep Evolutionary Roots Amidst Ongoing Intragenomic MobilityManuscript (preprint) (Other academic)
    Abstract [en]

    Small nucleolar (sno)RNAs are required for posttranscriptional processing andmodification of ribosomal, spliceosomal and messenger RNAs. There are two broadclasses (C/D and H/ACA), both of which have been characterized in eukaryotes andarchaea. The association with ribosomal RNA processing and modification has led tothe suggestion that snoRNAs are evolutionarily ancient, and date back to the RNAworld. That numerous snoRNAs have been identified in the introns of ribosomalprotein genes has led to alternate views on the origin of this organization. Oneproposal is that intronic snoRNAs predate their surrounding protein-coding exons,the latter being recruited as messenger RNA following the origin of geneticallyencodedprotein synthesis. Another is that intron position reflects selection forcoexpression of snoRNAs and ribosomal components. To gain a clearer insight intothe antiquity of individual snoRNA families and the stability of their genomic location,we examined the evolutionary history of snoRNA families across 44 eukaryotegenomes. Our analysis reveals that dozens of snoRNA families can be traced backto the Last Eukaryotic Common Ancestor (LECA). However, none of the snoRNA1families placed in the LECA are sufficiently similar to characterized archaeal sno-likeRNAs, for us to confidently place specific snoRNA families in the common ancestorof archaea and eukaryotes. In agreement with earlier studies, we can tracenumerous introns to the LECA. However, snoRNAs housed within such positionallyconserved introns are not themselves orthologs. Morevover, our comparativegenomics analysis argues against evolutionarily-stable association betweensnoRNAs and individual host genes — analysis of host gene expression dataindicates that the primary requirement being for hosting intronic snoRNAs is a broadexpression profile. Consistent with mobility over antiquity, we report a case ofdemonstrable intronic snoRNA gain, where an evolutionarily ancient snoRNA hasmigrated into the intron of a mammalian mitochondrial ribosomal protein gene.Together, these data best fit a model wherein snoRNAs are intragenomically mobile,frequently residing in the introns of broadly-expressed protein-coding genes.

  • 4.
    Hoeppner, Marc Patrick
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Poole, Anthony M.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Maintenance of redundant small RNA gene copies over evolutionarytimescales via a retrotransposition motor?Manuscript (preprint) (Other academic)
    Abstract [en]

    We analysed the stability of duplicated, essential RNAs on the backdrop of theirexpression profiles to test whether the data is compatible with functional redundancy ordiversification. Under the former model, the expectation is that copies are equallyexpressed across tissues and subject to high turn-over. The latter model, in contrast,predicts that sub- or neofunctionalization following duplication may lead to a range ofcomplementary expression profiles across tissues. By example of the spliceosomal RNAU1 and snoRNA U3, we find that only few loci are stable over the course of vertebrateevolution and that the majority of copies show little or no expression. We conclude thatthese findings are most compatible with the redundancy model. Interestingly, the deepestloci are associated with a testis-expressed gene, suggesting a possible driving forcebehind the ongoing proliferation that we observe.

  • 5.
    Neumann, Nadja
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Jeffares, Daniel C.
    Poole, Anthony
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Outsourcing the Nucleus: Nuclear Pore Complex Genes are no Longer Encoded in Nucleomorph Genomes2006In: Evolutionary Bioinformatics, ISSN 1176-9343, E-ISSN 1176-9343, Vol. 2, p. 23-34Article in journal (Refereed)
    Abstract [en]

    The nuclear pore complex (NPC) facilitates transport between nucleus and cytoplasm. The protein constituents of the NPC, termed nucleoporins (Nups), are conserved across a wide diversity of eukaryotes. In apparent exception to this, no nucleoporin genes have been identified in nucleomorph genomes. Nucleomorphs, nuclear remnants of once free-living eukaryotes, took up residence as secondary endosymbionts in cryptomonad and chlorarachniophyte algae. As these genomes are highly reduced, Nup genes may have been lost, or relocated to the host nucleus. However, Nup genes are often poorly conserved between species, so absence may be an artifact of low sequence similarity. We therefore constructed an evolutionary bioinformatic screen to establish whether the apparent absence of Nup genes in nucleomorph genomes is due to genuine absence or the inability of current methods to detect homologues. We searched green plant (Arabidopsis and rice), green alga (Chlamydomonas reinhardtii) and red alga (Cyanidioschyzon merolae) genomes, plus two nucleomorph genomes (Bigelowiella natans and Guillardia theta) with profile hidden Markov models (HMMs) from curated alignments of known vertebrate/yeast Nups. Since the plant, algal and nucleomorph genomes all belong to the kingdom Plantae, and are evolutionarily distant from the outgroup (vertebrate/yeast) training set, we use the plant and algal genomes as internal positive controls for the sensitivity of the searches in nucleomorph genomes. We find numerous Nup homologues in all plant and free-living algal species, but none in either nucleomorph genome. BLAST searches using identified plant and algal Nups also failed to detect nucleomorph homologues. We conclude that nucleomorph Nup genes have either been lost, being replaced by host Nup genes, or, that nucleomorph Nup genes have been transferred to the host nucleus twice independently; once in the evolution of the red algal nucleomorph and once in the green algal nucleomorph.

  • 6.
    Neumann, Nadja
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Lundin, Daniel
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Poole, Anthony M.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Comparative Genomic Evidence for a Complete Nuclear Pore Complex in the Last Eukaryotic Common Ancestor2010In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 5, no 10, p. e13241-Article in journal (Refereed)
    Abstract [en]

    Background: The Nuclear Pore Complex (NPC) facilitates molecular trafficking between nucleus and cytoplasm and is an integral feature of the eukaryote cell. It exhibits eight-fold rotational symmetry and is comprised of approximately 30 nucleoporins (Nups) in different stoichiometries. Nups are broadly conserved between yeast, vertebrates and plants, but few have been identified among other major eukaryotic groups. Methodology/Principal Findings: We screened for Nups across 60 eukaryote genomes and report that 19 Nups (spanning all major protein subcomplexes) are found in all eukaryote supergroups represented in our study (Opisthokonts, Amoebozoa, Viridiplantae, Chromalveolates and Excavates). Based on parsimony, between 23 and 26 of 31 Nups can be placed in LECA. Notably, they include central components of the anchoring system (Ndc1 and Gp210) indicating that the anchoring system did not evolve by convergence, as has previously been suggested. These results significantly extend earlier results and, importantly, unambiguously place a fully-fledged NPC in LECA. We also test the proposal that transmembrane Pom proteins in vertebrates and yeasts may account for their variant forms of mitosis (open mitoses in vertebrates, closed among yeasts). The distribution of homologues of vertebrate Pom121 and yeast Pom152 is not consistent with this suggestion, but the distribution of fungal Pom34 fits a scenario wherein it was integral to the evolution of closed mitosis in ascomycetes. We also report an updated screen for vesicle coating complexes, which share a common evolutionary origin with Nups, and can be traced back to LECA. Surprisingly, we find only three supergroup-level differences (one gain and two losses) between the constituents of COPI, COPII and Clathrin complexes. Conclusions/Significance: Our results indicate that all major protein subcomplexes in the Nuclear Pore Complex are traceable to the Last Eukaryotic Common Ancestor (LECA). In contrast to previous screens, we demonstrate that our conclusions hold regardless of the position of the root of the eukaryote tree.

  • 7.
    Neumann, Nadja
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Poole, Anthony
    Is the bouquet arrangement in meiosis an ancient solution to the hotspot conversion paradox?Manuscript (preprint) (Other academic)
  • 8. Penny, D
    et al.
    Hendy, M D
    Poole, A
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Testing fundamental evolutionary hypotheses2003In: The Journal of Theoretical Biology, Vol. 223, p. 377-385Article in journal (Refereed)
  • 9. Penny, D
    et al.
    Poole, A
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Lateral Gene Transfer: Some Theoretical Aspects2003In: NZ BioScience, p. 32-35Article in journal (Other (popular science, discussion, etc.))
  • 10. Penny, David
    et al.
    Hoeppner, Marc P.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Poole, Anthony M.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Jeffares, Daniel C.
    An Overview of the Introns-First Theory2009In: Journal of Molecular Evolution, ISSN 0022-2844, E-ISSN 1432-1432, Vol. 69, p. 527-540Article in journal (Refereed)
    Abstract [en]

    We review the introns-first hypothesis a decade after it was first proposed. It is that exons emerged from

    non-coding regions interspersed between RNA genes in an early RNA world, and is a subcomponent of a more general ‘RNA-continuity’ hypothesis. The latter is that some RNA based systems, especially in RNA processing, are ‘relics’ that can be traced back either to the RNA world that preceded both DNA and encoded protein synthesis or to the later ribonucleoprotein (RNP) world (before DNA took over the main coding role). RNA-continuity is based on independent evidence—in particular, the relative inefficiency of RNA catalysis compared with protein catalysis— and leads to a wide range of predictions, ranging from the origin of the ribosome, the spliceosome, small nucleolar RNAs, RNases P and MRP, and mRNA, and it is consistent with the wide involvement of RNA-processing and regulation of RNA in modern eukaryotes. While there may still

    be cause to withhold judgement on intron origins, there is strong evidence against introns being uncommon in the last eukaryotic common ancestor (LECA), and expanding only within extant eukaryotic groups—the ‘very-late’ intron invasion model. Similarly, it is clear that there are selective forces on numbers and positions of introns; their existence may not always be neutral. There is still a range of viable alternatives, including introns first, early, and ‘latish’ (i.e. well established in LECA), and regardless of which is ultimately correct, it pays to separate out various questions and to focus on testing the predictions of sub-theories.

  • 11.
    Poole, A
    Stockholm University.
    Did group II proliferation in an endosymbiont-bearing archaeon create eukaryotes?2006In: Biology DirectArticle in journal (Refereed)
  • 12.
    Poole, A
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Getting from an RNA world to modern cells just got a little easier2006In: BioEssays, Vol. 28, no 2, p. 105-108Article in journal (Other academic)
  • 13.
    Poole, A
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Hode, T
    Brandenburg, A
    Holm, N G
    Life Up North: Meeting Report: Nordic Astrobiology 2006: Origins & Distribution of Life in the Universe2006In: Astrobiology, Vol. 6, no 6, p. 815-818Article in journal (Other academic)
  • 14.
    Poole, A
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Logan, D T
    Modern mRNA Proofreading and Repair: Clues that the last Universal Common Ancestor Possessed an RNA Genome?2005In: Mol. Biol. Evol, Vol. 22, no 6, p. 1444-1455Article in journal (Refereed)
  • 15.
    Poole, A
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Phillips, M
    Penny, D
    Prokaryote and eukaryote evolvability2003In: BioSystems, Vol. 69, p. 163-185Article in journal (Refereed)
  • 16.
    Poole, Anthony
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Does endosymbiosis explain the origin of the nucleus?2001In: Nature Cell Biology, Vol. 3, p. E173-Article, book review (Other academic)
  • 17.
    Poole, Anthony
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    My name is LUCA - The Last Universal Common Ancestor2002In: Action BioscienceArticle in journal (Other (popular science, discussion, etc.))
  • 18.
    Poole, Anthony
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Logan, Derek T
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Sjöberg, Britt-Marie
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    The evolution of the ribonucleotide reductases: much ado about oxygen.2002In: J Mol Evol, ISSN 0022-2844, Vol. 55, no 2, p. 180-96Article in journal (Other academic)
    Abstract [en]

    Ribonucleotide reduction is the only known biological means for de novo production of deoxyribonucleotides, the building blocks of DNA. These are produced from ribonucleotides, the building blocks of RNA, and the direction of this reaction has been taken to support the idea that, in evolution, RNA preceded DNA as genetic material. However, an understanding of the evolutionary relationships among the three modern-day classes of ribonucleotide reductase and how the first reductase arose early in evolution is still far off. We propose that the diversification of this class of enzymes is inherently tied to microbial colonization of aerobic and anaerobic niches. The work is of broader interest, as it also sheds light on the process of adaptation to oxygenic environments consequent to the evolution of atmospheric oxygen.

  • 19.
    Poole, Anthony M
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Horizontal gene transfer and the earliest stages of the evolution of life2009In: Research in Microbiology, ISSN 0923-2508, E-ISSN 1769-7123, Vol. 160, no 7, p. 473-480Article in journal (Refereed)
    Abstract [en]

    Horizontal gene transfer (HGT) has been suggested to be the dominant hereditary process at the earliest stages of evolution. I examine this suggestion within the context of the problem of genetic parasites and suggest that extreme rates of transfer may in fact negatively impact evolutionary transitions. In regard to the proposal that HGT is Lamarckian, the apparent conflict between HGT and Darwinian evolution is easily avoided by considering HGT at the appropriate level of selection.

  • 20.
    Poole, Anthony M
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    How the endosymbiont got its cell2009In: New Zeeland Science Review, Vol. 66, no 1, p. 28-33Article, book review (Other academic)
    Abstract [en]

    Despite fundamental advances in cellular, molecular and genome biology, there is still surprisingly little consensus concerning the evolutionary origins of the eukaryote cell. While it is clear that the mitochondrion (responsible for generating much of the energy requirements of the eukaryote cell) has evolved from an endosymbiont cell of bacterial origin, the recent literature has borne witness to a tidal wave of speculative theories regarding the nature of the cell in which this bacterium took up residence. David Penny and I recently argued that much of this confusion can be avoided if models are grounded in known biological processes, and if speculation is tempered by formulating testable hypotheses. The most fanciful hypotheses are an inevitable casualty of a pragmatic approach, but what remains is a productive framework wherein biologically plausible alternatives can be evaluated without the need to invoke ad hoc events or processes, such as biological ‘big bangs’ or hitherto unobserved cell biological phenomena.

  • 21.
    Poole, Anthony M.
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Neumann, Nadja
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the Eocyte hypothesis2011In: Research in Microbiology, ISSN 0923-2508, E-ISSN 1769-7123, Vol. 162, no 1, p. 71-76Article in journal (Refereed)
    Abstract [en]

    An archaeal origin of eukaryotes is often equated with the engulfment of the bacterial ancestor of mitochondria by an archaeon. Such an event is problematic in that it is not supported by archaeal cell biology. We show that placing phylogenetic results within a stem-and-crown framework eliminates such incompatibilities, and that an archaeal origin for eukaryotes (as suggested from recent phylogenies) can be uncontroversially reconciled with phagocytosis as the mechanism for engulfment of the mitochondrial ancestor. This is significant because it eliminates a perceived problem with eukaryote origins: that an archaeal origin of eukaryotes (as under the Eocyte hypothesis) cannot be reconciled with existing cell biological mechanisms through which bacteria may take up residence inside eukaryote cells.

  • 22.
    Poole, Anthony M.
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Willerslev, Eske
    Can identification of a fourth domain of life be made from sequence data alone, and could it be done on mars?2007In: Astrobiology, ISSN 1531-1074, E-ISSN 1557-8070, Vol. 7, no 5, p. 801-814Article, review/survey (Refereed)
    Abstract [en]

    A central question in astrobiology is whether life exists elsewhere in the universe. If so, is it related to Earth life? Technologies exist that enable identification of DNA- or RNA-based microbial life directly from environmental samples here on Earth. Such technologies could, in principle, be applied to the search for life elsewhere; indeed, efforts are underway to initiate such a search. However, surveying for nucleic acid-based life on other planets, if attempted, must be carried out with caution, owing to the risk of contamination by Earth-based life. Here we argue that the null hypothesis must be that any DNA discovered and sequenced from samples taken elsewhere in the universe are Earth-based contaminants. Experience from studies of low-biomass ancient DNA demonstrates that some results, by their very nature, will not enable complete rejection of the null hypothesis. In terms of eliminating contamination as an explanation of the data, there may be value in identification of sequences that lie outside the known diversity of the three domains of life. We therefore have examined whether a fourth domain could be readily identified from environmental DNA sequence data alone. We concluded that, even on Earth, this would be far from trivial, and we illustrate this point by way of examples drawn from the literature. Overall, our conclusions do not bode well for planned PCR-based surveys for life on Mars, and we argue that other independent biosignatures will be essential in corroborating any claims for the presence of life based on nucleic acid sequences.

  • 23.
    Poole, Anthony
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Penny, David
    Sjöberg, Britt-Marie
    Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
    Confounded cytosine! Tinkering and the evolution of DNA2001In: Nature Reviews, Vol. 2, p. 147-151Article, book review (Other academic)
1 - 23 of 23
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