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  • 1. Andersson, Siv G E
    et al.
    Alsmark, Cecilia
    Canbäck, Björn
    Davids, Wagied
    Frank, Carolin
    Karlberg, Olof
    Klasson, Lisa
    Antoine-Legault, Boris
    Mira, Alex
    Tamas, Ivica
    Comparative genomics of microbial pathogens and symbionts.2002In: Bioinformatics, ISSN 1367-4803, E-ISSN 1367-4811, Vol. 18 Suppl 2, p. S17-Article in journal (Refereed)
    Abstract [en]

    We are interested in quantifying the contribution of gene acquisition, loss, expansion and rearrangements to the evolution of microbial genomes. Here, we discuss factors influencing microbial genome divergence based on pair-wise genome comparisons of closely related strains and species with different lifestyles. A particular focus is on intracellular pathogens and symbionts of the genera Rickettsia, Bartonella and BUCHNERA: Extensive gene loss and restricted access to phage and plasmid pools may provide an explanation for why single host pathogens are normally less successful than multihost pathogens. We note that species-specific genes tend to be shorter than orthologous genes, suggesting that a fraction of these may represent fossil-orfs, as also supported by multiple sequence alignments among species. The results of our genome comparisons are placed in the context of phylogenomic analyses of alpha and gamma proteobacteria. We highlight artefacts caused by different rates and patterns of mutations, suggesting that atypical phylogenetic placements can not a priori be taken as evidence for horizontal gene transfer events. The flexibility in genome structure among free-living microbes contrasts with the extreme stability observed for the small genomes of aphid endosymbionts, in which no rearrangements or inflow of genetic material have occurred during the past 50 millions years (1). Taken together, the results suggest that genomic stability correlate with the content of repeated sequences and mobile genetic elements, and thereby indirectly with bacterial lifestyles.

  • 2.
    Baiao, Guilherme Costa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Schneider, Daniela I.
    Med Univ Vienna, Ctr Anat & Cell Biol, Lab Genome Dynam, Deparment Cell & Dev Biol, Schwarzspanierstr 17, A-1090 Vienna, Austria;Yale Univ, Dept Epidemiol Microbial Dis, 60 Coll St, New Haven, CT 06510 USA.
    Miller, Wolfgang J.
    Med Univ Vienna, Ctr Anat & Cell Biol, Lab Genome Dynam, Deparment Cell & Dev Biol, Schwarzspanierstr 17, A-1090 Vienna, Austria.
    Klasson, Lisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    The effect of Wolbachia on gene expression in Drosophila paulistorum and its implications for symbiont-induced host speciation2019In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 20, article id 465Article in journal (Refereed)
    Abstract [en]

    Background: The Neotropical fruit fly Drosophila paulistorum (Diptera: Drosophilidae) is a species complex in statu nascendi comprising six reproductively isolated semispecies, each harboring mutualistic Wolbachia strains. Although wild type flies of each semispecies are isolated from the others by both pre- and postmating incompatibilities, mating between semispecies and successful offspring development can be achieved once flies are treated with antibiotics to reduce Wolbachia titer. Here we use RNA-seq to study the impact of Wolbachia on D. paulistorum and investigate the hypothesis that the symbiont may play a role in host speciation. For that goal, we analyze samples of heads and abdomens of both sexes of the Amazonian, Centro American and Orinocan semispecies of D. paulistorum.

    Results: We identify between 175 and 1192 differentially expressed genes associated with a variety of biological processes that respond either globally or according to tissue, sex or condition in the three semispecies. Some of the functions associated with differentially expressed genes are known to be affected by Wolbachia in other species, such as metabolism and immunity, whereas others represent putative novel phenotypes involving muscular functions, pheromone signaling, and visual perception.

    Conclusions: Our results show that Wolbachia affect a large number of biological functions in D. paulistorum, particularly when present in high titer. We suggest that the significant metabolic impact of the infection on the host may cause several of the other putative and observed phenotypes. We also speculate that the observed differential expression of genes associated with chemical communication and reproduction may be associated with the emergence of pre- and postmating barriers between semispecies, which supports a role for Wolbachia in the speciation of D. paulistorum.

  • 3.
    Ellegaard, Kirsten Maren
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Klasson, Lisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Andersson, Siv G. E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Testing the Reproducibility of Multiple Displacement Amplification on Genomes of Clonal Endosymbiont Populations2013In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 11, p. e82319-Article in journal (Refereed)
    Abstract [en]

    The multiple displacement amplification method has revolutionized genomic studies of uncultured bacteria, where the extraction of pure DNA in sufficient quantity for next-generation sequencing is challenging. However, the method is problematic in that it amplifies the target DNA unevenly, induces the formation of chimeric reads and also amplifies contaminating DNA. Here, we have tested the reproducibility of the multiple displacement amplification method using serial dilutions of extracted genomic DNA and intact cells from the cultured endosymbiont Bartonella australis. The amplified DNA was sequenced with the Illumina sequencing technology, and the results were compared to sequence data obtained from unamplified DNA in this study as well as from a previously published genome project. We show that artifacts such as the extent of the amplification bias, the percentage of chimeric reads and the relative fraction of contaminating DNA increase dramatically for the smallest amounts of template DNA. The pattern of read coverage was reproducibly obtained for samples with higher amounts of template DNA, suggesting that the bias is non-random and genome-specific. A re-analysis of previously published sequence data obtained after amplification from clonal endosymbiont populations confirmed these predictions. We conclude that many of the artifacts associated with the use of the multiple displacement amplification method can be alleviated or much reduced by using multiple cells as the template for the amplification. These findings should be particularly useful for researchers studying the genomes of endosymbionts and other uncultured bacteria, for which a small clonal population of cells can be isolated.

  • 4.
    Ellegaard, Kirsten Maren
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Klasson, Lisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Näslund, Kristina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Bourtzis, Kostas
    Andersson, Siv G. E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Comparative Genomics of Wolbachia and the Bacterial Species Concept2013In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 9, no 4, p. e1003381-Article in journal (Refereed)
    Abstract [en]

    The importance of host-specialization to speciation processes in obligate host-associated bacteria is well known, as is also the ability of recombination to generate cohesion in bacterial populations. However, whether divergent strains of highly recombining intracellular bacteria, such as Wolbachia, can maintain their genetic distinctness when infecting the same host is not known. We first developed a protocol for the genome sequencing of uncultivable endosymbionts. Using this method, we have sequenced the complete genomes of the Wolbachia strains wHa and wNo, which occur as natural double infections in Drosophila simulans populations on the Seychelles and in New Caledonia. Taxonomically, wHa belong to supergroup A and wNo to supergroup B. A comparative genomics study including additional strains supported the supergroup classification scheme and revealed 24 and 33 group-specific genes, putatively involved in host-adaptation processes. Recombination frequencies were high for strains of the same supergroup despite different host-preference patterns, leading to genomic cohesion. The inferred recombination fragments for strains of different supergroups were of short sizes, and the genomes of the co-infecting Wolbachia strains wHa and wNo were not more similar to each other and did not share more genes than other A- and B-group strains that infect different hosts. We conclude that Wolbachia strains of supergroup A and B represent genetically distinct clades, and that strains of different supergroups can co-exist in the same arthropod host without converging into the same species. This suggests that the supergroups are irreversibly separated and that barriers other than host-specialization are able to maintain distinct clades in recombining endosymbiont populations. Acquiring a good knowledge of the barriers to genetic exchange in Wolbachia will advance our understanding of how endosymbiont communities are constructed from vertically and horizontally transmitted genes.

  • 5. Gottlieb, Yuval
    et al.
    Lalzar, Itai
    Klasson, Lisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Distinctive Genome Reduction Rates Revealed by Genomic Analyses of Two Coxiella-Like Endosymbionts in Ticks2015In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 7, no 6, p. 1779-1796Article in journal (Refereed)
    Abstract [en]

    Genome reduction is a hallmark of symbiotic genomes, and the rate and patterns of gene loss associated with this process have been investigated in several different symbiotic systems. However, in long-term host-associated coevolving symbiont clades, the genome size differences between strains are normally quite small and hence patterns of large-scale genome reduction can only be inferred from distant relatives. Here we present the complete genome of a Coxiella-like symbiont from Rhipicephalus turanicus ticks (CRt), and compare it with other genomes from the genus Coxiella in order to investigate the process of genome reduction in a genus consisting of intracellular host-associated bacteria with variable genome sizes. The 1.7-Mb CRt genome is larger than the genomes of most obligate mutualists but has a very low protein-coding content (48.5%) and an extremely high number of identifiable pseudogenes, indicating that it is currently undergoing genome reduction. Analysis of encoded functions suggests that CRt is an obligate tick mutualist, as indicated by the possible provisioning of the tick with biotin (B7), riboflavin (B2) and other cofactors, and by the loss of most genes involved in host cell interactions, such as secretion systems. Comparative analyses between CRt and the 2.5 times smaller genome of Coxiella from the lonestar tick Amblyomma americanum (CLEAA) show that many of the same gene functions are lost and suggest that the large size difference might be due to a higher rate of genome evolution in CLEAA generated by the loss of the mismatch repair genes mutSL. Finally, sequence polymorphisms in the CRt population sampled from field collected ticks reveal up to one distinct strain variant per tick, and analyses of mutational patterns within the population suggest that selection might be acting on synonymous sites. The CRt genome is an extreme example of a symbiont genome caught in the act of genome reduction, and the comparison between CLEAA and CRt indicates that losses of particular genes early on in this process can potentially greatly influence the speed of this process.

  • 6.
    Hotopp, Julie C. Dunning
    et al.
    Univ Maryland, Sch Med, Greenebaum Canc Ctr, Inst Genome Sci,Dept Microbiol & Immunol, Baltimore, MD 21201 USA..
    Klasson, Lisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    The Complexities and Nuances of Analyzing the Genome of Drosophila ananassae and Its Wolbachia Endosymbiont2018In: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 8, no 1, p. 373-374Article in journal (Refereed)
    Abstract [en]

    In "Retrotransposons Are the Major Contributors to the Expansion of the Drosophila ananassae Muller F Element," Leung et al. (2017) improved contigs attributed to the Muller F element from the original CAF1 assembly, and used them to conclude that most of the sequence expansion of the fourth chromosome of D. ananassae is due to a higher transposon load than previously thought, but is not due to Wolbachia DNA integrations. While we do not disagree with the first conclusion, the authors base their second conclusion on the lack of homology detected between their improved CAF1 genome assembly attributed to D. ananassae and reference Wolbachia genomes. While the consensus CAF1 genome assembly lacks any sequence similarity to the reference genome of the Wolbachia endosymbiont of Drosophila melanogaster (wMel), numerous studies from multiple laboratories provide experimental support for a large lateral/horizontal gene transfer (LGT) of a Wolbachia genome into this D. ananassae line. As such, we strongly suspect that the original whole genome assembly was either constructed after the removal of all Wolbachia reads, or that Wolbachia sequences were directly removed from the contigs in the CAF1 assembly. Hence, Leung et al. (2017) could not have identified the Wolbachia LGT using the CAF1 assembly. This manuscript by Leung et al. (2017) highlights that an assembly of the Wolbachia sequence reads and their mate pairs was erroneously attributed solely to the Wolbachia endosymbiont, albeit before we understood the extent of LGT in D. ananassae. As such, we recommend that the sequences deposited at the National Center for Biotechnology Information (NCBI) under PRJNA13365 should not be attributed to Wolbachia endosymbiont of D. ananassae, but should have their taxonomy reclassified by NCBI as "Unclassified sequences." As our knowledge about genome biology improves, we need to reconsider and reanalyze earlier genomes removing the prejudice introduced from now defunct paradigms.

  • 7.
    Kampfraath, A. A.
    et al.
    Vrije Univ Amsterdam, Dept Ecol Sci, Amsterdam, Netherlands.
    Klasson, Lisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Anvar, S. Y.
    Leiden Univ, Dept Human Genet, Med Ctr, Leiden, Netherlands;Leiden Univ, Leiden Genome Technol Ctr, Med Ctr, Leiden, Netherlands.
    Vossen, R. H. A. M.
    Leiden Univ, Leiden Genome Technol Ctr, Med Ctr, Leiden, Netherlands.
    Roelofs, D.
    Vrije Univ Amsterdam, Dept Ecol Sci, Amsterdam, Netherlands.
    Kraaijeveld, K.
    Vrije Univ Amsterdam, Dept Ecol Sci, Amsterdam, Netherlands.
    Ellers, J.
    Vrije Univ Amsterdam, Dept Ecol Sci, Amsterdam, Netherlands.
    Genome expansion of an obligate parthenogenesis-associated Wolbachia poses an exception to the symbiont reduction model2019In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 20, article id 106Article in journal (Refereed)
    Abstract [en]

    Background: Theory predicts that dependency within host-endosymbiont interactions results in endosymbiont genome size reduction. Unexpectedly, the largest Wolbachia genome was found in the obligate, parthenogenesis-associated wFol. In this study, we investigate possible processes underlying this genome expansion by comparing a re-annotated wFol genome to other Wolbachia genomes. In addition, we also search for candidate genes related to parthenogenesis induction (PI).

    Results: Within wFol, we found five phage WO regions representing 25.4% of the complete genome, few pseudogenized genes, and an expansion of DNA-repair genes in comparison to other Wolbachia. These signs of genome conservation were mirrored in the wFol host, the springtail F. candida, which also had an expanded DNA-repair gene family and many horizontally transferred genes. Across all Wolbachia genomes, there was a strong correlation between gene numbers of Wolbachia strains and their hosts. In order to identify genes with a potential link to PI, we assembled the genome of an additional PI strain, wLcla. Comparisons between four PI Wolbachia, including wFol and wLcla, and fourteen non-PI Wolbachia yielded a small set of potential candidate genes for further investigation.

    Conclusions: The strong similarities in genome content of wFol and its host, as well as the correlation between host and Wolbachia gene numbers suggest that there may be some form of convergent evolution between endosymbiont and host genomes. If such convergent evolution would be strong enough to overcome the evolutionary forces causing genome reduction, it would enable expanded genomes within long-term obligate endosymbionts.

  • 8.
    Klasson, Lisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    The unpredictable road to reduction2017In: Nature ecology and evolution, ISSN 2397-334X, Vol. 1, p. 1062-1063Article in journal (Other academic)
  • 9.
    Klasson, Lisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
    Andersson, Siv
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
    Evolution of minimal-gene-sets in host-dependent bacteria2004In: Trends in Microbiology, ISSN 0966-842X, E-ISSN 1878-4380, Vol. 12, no 1, p. 37-43Article in journal (Refereed)
    Abstract [en]

    Several attempts have been made to identify the minimal set of genes that is required for life using computational approaches or studies of deletion mutants. These experiments resemble those already performed by nature; a few hundred million years ago an ancestor of Escherichia coli was domesticated by aphids, which resulted in the elimination of 70–75% of the original bacterial genome. Amazingly, the small genomes of these imprisoned bacteria are more stable than those of their free-living relatives. Minimal-gene-sets that have evolved naturally are largely species-specific, with the exception of a small set of core genes that are required for information processing. Comparative genomics of host-dependent bacteria have shown that minimal-gene-sets can persist in nature for tens of millions of years provided that the environment is rich in nutrients, that the host population size is large and that there is a strong host-level selection for bacterial gene functions.

  • 10. Klasson, Lisa
    et al.
    Andersson, Siv G E
    Evolution of minimal-gene-sets in host-dependent bacteria.2004In: Trends in Microbiology, ISSN 0966-842X, E-ISSN 1878-4380, Vol. 12, no 1, p. 37-43Article in journal (Refereed)
    Abstract [en]

    Several attempts have been made to identify the minimal set of genes that is required for life using computational approaches or studies of deletion mutants. These experiments resemble those already performed by nature; a few hundred million years ago an ancestor of Escherichia coli was domesticated by aphids, which resulted in the elimination of 70-75% of the original bacterial genome. Amazingly, the small genomes of these imprisoned bacteria are more stable than those of their free-living relatives. Minimal-gene-sets that have evolved naturally are largely species-specific, with the exception of a small set of core genes that are required for information processing. Comparative genomics of host-dependent bacteria have shown that minimal-gene-sets can persist in nature for tens of millions of years provided that the environment is rich in nutrients, that the host population size is large and that there is a strong host-level selection for bacterial gene functions.

  • 11.
    Klasson, Lisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
    Andersson, Siv G. E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
    Research on small genomes: Implications for synthetic biology2010In: Bioessays, ISSN 0265-9247, E-ISSN 1521-1878, Vol. 32, no 4, p. 288-295Article, review/survey (Refereed)
    Abstract [en]

    Synthetic genomics is a new field of research in which small DNA pieces are assembled in a series of steps into whole genomes. The highly reduced genomes of host-associated bacteria are now being used as models for de novo synthesis of small genomes in the laboratory. Bacteria with the smallest genomes identified in nature provide nutrients to their hosts, such as amino acids, co-factors and vitamins. Comparative genomics of these bacteria enables predictions to be made about the gene sets required for core cellular functions and the associated metabolic network for the biosynthesis of host-selected compounds. Synthetic biology may ultimately enable researchers to make customized cell-specific organelles for the production and delivery of drugs to humans and domestic animals. Synthetic genomics may also become the method of choice for functional analyses of genes and genomes from bacteria that cannot be cultivated in the laboratory.

  • 12. Klasson, Lisa
    et al.
    Kambris, Zakaria
    Cook, Peter E
    Walker, Thomas
    Sinkins, Steven P
    Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti.2009In: BMC genomics, ISSN 1471-2164, Vol. 10, p. 33-Article in journal (Refereed)
    Abstract [en]

    BACKGROUND: The evolutionary importance of horizontal gene transfer (HGT) from Wolbachia endosymbiotic bacteria to their eukaryotic hosts is a topic of considerable interest and debate. Recent transfers of genome fragments from Wolbachia into insect chromosomes have been reported, but it has been argued that these fragments may be on an evolutionary trajectory to degradation and loss.

    RESULTS: We have discovered a case of HGT, involving two adjacent genes, between the genomes of Wolbachia and the currently Wolbachia-uninfected mosquito Aedes aegypti, an important human disease vector. The lower level of sequence identity between Wolbachia and insect, the transcription of all the genes involved, and the fact that we have identified homologs of the two genes in another Aedes species (Ae. mascarensis), suggest that these genes are being expressed after an extended evolutionary period since horizontal transfer, and therefore that the transfer has functional significance. The association of these genes with Wolbachia prophage regions also provides a mechanism for the transfer.

    CONCLUSION: The data support the argument that HGT between Wolbachia endosymbiotic bacteria and their hosts has produced evolutionary innovation.

  • 13.
    Klasson, Lisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Kumar, Nikhil
    Bromley, Robin
    Sieber, Karsten
    Flowers, Melissa
    Ott, Sandra H.
    Tallon, Luke J.
    Andersson, Siv G. E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Hotopp, Julie C. Dunning
    Extensive duplication of the Wolbachia DNA in chromosome four of Drosophila ananassae2014In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 15, p. 1097-Article in journal (Refereed)
    Abstract [en]

    Background: Lateral gene transfer (LGT) from bacterial Wolbachia endosymbionts has been detected in similar to 20% of arthropod and nematode genome sequencing projects. Many of these transfers are large and contain a substantial part of the Wolbachia genome. Results: Here, we re-sequenced three D. ananassae genomes from Asia and the Pacific that contain large LGTs from Wolbachia. We find that multiple copies of the Wolbachia genome are transferred to the Drosophila nuclear genome in all three lines. In the D. ananassae line from Indonesia, the copies of Wolbachia DNA in the nuclear genome are nearly identical in size and sequence yielding an even coverage of mapped reads over the Wolbachia genome. In contrast, the D. ananassae lines from Hawaii and India show an uneven coverage of mapped reads over the Wolbachia genome suggesting that different parts of these LGTs are present in different copy numbers. In the Hawaii line, we find that this LGT is underrepresented in third instar larvae indicative of being heterochromatic. Fluorescence in situ hybridization of mitotic chromosomes confirms that the LGT in the Hawaii line is heterochromatic and represents similar to 20% of the sequence on chromosome 4 (dot chromosome, Muller element F). Conclusions: This collection of related lines contain large lateral gene transfers composed of multiple Wolbachia genomes that constitute >2% of the D. ananassae genome (similar to 5 Mbp) and partially explain the abnormally large size of chromosome 4 in D. ananassae.

  • 14. Klasson, Lisa
    et al.
    Walker, Thomas
    Sebaihia, Mohammed
    Sanders, Mandy J
    Quail, Michael A
    Lord, Angela
    Sanders, Susanne
    Earl, Julie
    O'Neill, Scott L
    Thomson, Nicholas
    Sinkins, Steven P
    Parkhill, Julian
    Genome evolution of Wolbachia strain wPip from the Culex pipiens group.2008In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 25, no 9, p. 1877-87Article in journal (Refereed)
    Abstract [en]

    The obligate intracellular bacterium Wolbachia pipientis strain wPip induces cytoplasmic incompatibility (CI), patterns of crossing sterility, in the Culex pipiens group of mosquitoes. The complete sequence is presented of the 1.48-Mbp genome of wPip which encodes 1386 coding sequences (CDSs), representing the first genome sequence of a B-supergroup Wolbachia. Comparisons were made with the smaller genomes of Wolbachia strains wMel of Drosophila melanogaster, an A-supergroup Wolbachia that is also a CI inducer, and wBm, a mutualist of Brugia malayi nematodes that belongs to the D-supergroup of Wolbachia. Despite extensive gene order rearrangement, a core set of Wolbachia genes shared between the 3 genomes can be identified and contrasts with a flexible gene pool where rapid evolution has taken place. There are much more extensive prophage and ankyrin repeat encoding (ANK) gene components of the wPip genome compared with wMel and wBm, and both are likely to be of considerable importance in wPip biology. Five WO-B-like prophage regions are present and contain some genes that are identical or highly similar in multiple prophage copies, whereas other genes are unique, and it is likely that extensive recombination, duplication, and insertion have occurred between copies. A much larger number of genes encode ankyrin repeat (ANK) proteins in wPip, with 60 present compared with 23 in wMel, many of which are within or close to the prophage regions. It is likely that this pattern is partly a result of expansions in the wPip lineage, due for example to gene duplication, but their presence is in some cases more ancient. The wPip genome underlines the considerable evolutionary flexibility of Wolbachia, providing clear evidence for the rapid evolution of ANK-encoding genes and of prophage regions. This host-Wolbachia system, with its complex patterns of sterility induced between populations, now provides an excellent model for unraveling the molecular systems underlying host reproductive manipulation.

  • 15.
    Klasson, Lisa
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
    Westberg, Joakim
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
    Sapountzis, Panagiotis
    Näslund, Kristina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
    Lutnaes, Ylva
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
    Darby, Alistair C.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
    Veneti, Zoe
    Chen, Lanming
    Braig, R.
    Garrett, Roger
    Bourtzis, Kostas
    Andersson, Siv G. E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Molecular Evolution.
    The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans2009In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 106, no 14, p. 5725-5730Article in journal (Refereed)
    Abstract [en]

    The obligate intracellular bacterium Wolbachia pipientis infects around 20% of all insect species. It is maternally inherited and induces reproductive alterations of insect populations by male killing, feminization, parthenogenesis, or cytoplasmic incompatibility. Here, we present the 1,445,873-bp genome of W. pipientis strain wRi that induces very strong cytoplasmic incompatibility in its natural host Drosophila simulans. A comparison with the previously sequenced genome of W. pipientis strain wMeI from Drosophila melanogaster identified 35 breakpoints associated with mobile elements and repeated sequences that are stable in Drosophila lines transinfected with wRi. Additionally, 450 genes with orthologs in wRi and wMeI were sequenced from the W. pipientis strain wUni, responsible for the induction of parthenogenesis in the parasitoid wasp Muscidifurax uniraptor. The comparison of these A-group Wolbachia strains uncovered the most highly recombining intracellular bacterial genomes known to date. This was manifested in a 500-fold variation in sequence divergences at synonymous sites, with different genes and gene segments supporting different strain relationships. The substitution-frequency profile resembled that of Neisseria meningitidis, which is characterized by rampant intraspecies recombination, rather than that of Rickettsia, where genes mostly diverge by nucleotide substitutions. The data further revealed diversification of ankyrin repeat genes by short tandem duplications and provided examples of horizontal gene transfer across A- and B- group strains that infect D. simulans. These results suggest that the transmission dynamics of Wolbachia and the opportunity for coinfections have created a freely recombining intracellular bacterial community with mosaic genomes.

  • 16. Mira, Alex
    et al.
    Klasson, Lisa
    Andersson, Siv G E
    Microbial genome evolution: sources of variability.2002In: Current Opinion in Microbiology, ISSN 1369-5274, E-ISSN 1879-0364, Vol. 5, no 5, p. 506-12Article in journal (Refereed)
    Abstract [en]

    Comparative genome analyses of close relatives have yielded exciting insight into the sources of microbial genome variability with respect to gene content, gene order and evolution of genes with unknown functions. The genomes of free-living bacteria often carry phages and repetitive sequences that mediate genomic rearrangements in contrast to the small genomes of obligate host-associated bacteria. This suggests that genomic stability correlates with the genomic content of repeated sequences and movable genetic elements, and thereby with bacterial lifestyle. Genes with unknown functions present in a single species tend to be shorter than conserved, functional genes, indicating that the fraction of unique genes in microbial genomes has been overestimated.

  • 17. Nystedt, Bjorn
    et al.
    Street, Nathaniel R.
    Wetterbom, Anna
    Zuccolo, Andrea
    Lin, Yao-Cheng
    Scofield, Douglas G.
    Vezzi, Francesco
    Delhomme, Nicolas
    Giacomello, Stefania
    Alexeyenko, Andrey
    Vicedomini, Riccardo
    Sahlin, Kristoffer
    Sherwood, Ellen
    Elfstrand, Malin
    Gramzow, Lydia
    Holmberg, Kristina
    Hallman, Jimmie
    Keech, Olivier
    Klasson, Lisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Koriabine, Maxim
    Kucukoglu, Melis
    Kaller, Max
    Luthman, Johannes
    Lysholm, Fredrik
    Niittyla, Totte
    Olson, Ake
    Rilakovic, Nemanja
    Ritland, Carol
    Rossello, Josep A.
    Sena, Juliana
    Svensson, Thomas
    Talavera-Lopez, Carlos
    Theissen, Guenter
    Tuominen, Hannele
    Vanneste, Kevin
    Wu, Zhi-Qiang
    Zhang, Bo
    Zerbe, Philipp
    Arvestad, Lars
    Bhalerao, Rishikesh
    Bohlmann, Joerg
    Bousquet, Jean
    Gil, Rosario Garcia
    Hvidsten, Torgeir R.
    de Jong, Pieter
    MacKay, John
    Morgante, Michele
    Ritland, Kermit
    Sundberg, Bjorn
    Thompson, Stacey Lee
    Van de Peer, Yves
    Andersson, Bjorn
    Nilsson, Ove
    Ingvarsson, Par K.
    Lundeberg, Joakim
    Jansson, Stefan
    The Norway spruce genome sequence and conifer genome evolution2013In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 497, no 7451, p. 579-584Article in journal (Refereed)
    Abstract [en]

    Conifers have dominated forests for more than 200 million years and are of huge ecological and economic importance. Here we present the draft assembly of the 20-gigabase genome of Norway spruce (Picea abies), the first available for any gymnosperm. The number of well-supported genes (28,354) is similar to the >100 times smaller genome of Arabidopsis thaliana, and there is no evidence of a recent whole-genome duplication in the gymnosperm lineage. Instead, the large genome size seems to result from the slow and steady accumulation of a diverse set of long-terminal repeat transposable elements, possibly owing to the lack of an efficient elimination mechanism. Comparative sequencing of Pinus sylvestris, Abies sibirica, Juniperus communis, Taxus baccata and Gnetum gnemon reveals that the transposable element diversity is shared among extant conifers. Expression of 24-nucleotide small RNAs, previously implicated in transposable element silencing, is tissue-specific and much lower than in other plants. We further identify numerous long (>10,000 base pairs) introns, gene-like fragments, uncharacterized long non-coding RNAs and short RNAs. This opens up new genomic avenues for conifer forestry and breeding.

  • 18. Prior, R G
    et al.
    Klasson, L
    Larsson, P
    Williams, K
    Lindler, L
    Sjöstedt, A
    Svensson, T
    Tamas, I
    Wren, B W
    Oyston, P C
    Andersson, S G
    Titball, R W
    Preliminary analysis and annotation of the partial genome sequence of Francisella tularensis strain Schu 4.2001In: Journal of Applied Microbiology, ISSN 1364-5072, E-ISSN 1365-2672, Vol. 91, no 4, p. 614-20Article in journal (Refereed)
  • 19. Schneider, Daniela I.
    et al.
    Klasson, Lisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Lind, Anders E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Miller, Wolfgang J.
    More than fishing in the dark: PCR of a dispersed sequence produces simple but ultrasensitive Wolbachia detection2014In: BMC Microbiology, ISSN 1471-2180, E-ISSN 1471-2180, Vol. 14, p. 121-Article in journal (Refereed)
    Abstract [en]

    Background: Detecting intracellular bacterial symbionts can be challenging when they persist at very low densities. Wolbachia, a widespread bacterial endosymbiont of invertebrates, is particularly challenging. Although it persists at high titers in many species, in others its densities are far below the detection limit of classic end-point Polymerase Chain Reaction (PCR). These low-titer infections can be reliably detected by combining PCR with DNA hybridization, but less elaborate strategies based on end-point PCR alone have proven less sensitive or less general. Results: We introduce a multicopy PCR target that allows fast and reliable detection of A-supergroup Wolbachia -even at low infection titers -with standard end-point PCR. The target is a multicopy motif (designated ARM: A-supergroup repeat motif) discovered in the genome of wMel (the Wolbachia in Drosophila melanogaster). ARM is found in at least seven other Wolbachia A-supergroup strains infecting various Drosophila, the wasp Muscidifurax and the tsetse fly Glossina. We demonstrate that end-point PCR targeting ARM can reliably detect both high-and low-titer Wolbachia infections in Drosophila, Glossina and interspecific hybrids. Conclusions: Simple end-point PCR of ARM facilitates detection of low-titer Wolbachia A-supergroup infections. Detecting these infections previously required more elaborate procedures. Our ARM target seems to be a general feature of Wolbachia A-supergroup genomes, unlike other multicopy markers such as insertion sequences (IS).

  • 20. Siozios, Stefanos
    et al.
    Ioannidis, Panagiotis
    Klasson, Lisa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Andersson, Siv G. E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Braig, Henk R.
    Bourtzis, Kostas
    The Diversity and Evolution of Wolbachia Ankyrin Repeat Domain Genes2013In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 2, p. e55390-Article in journal (Refereed)
    Abstract [en]

    Ankyrin repeat domain-encoding genes are common in the eukaryotic and viral domains of life, but they are rare in bacteria, the exception being a few obligate or facultative intracellular Proteobacteria species. Despite having a reduced genome, the arthropod strains of the alphaproteobacterium Wolbachia contain an unusually high number of ankyrin repeat domain-encoding genes ranging from 23 in wMel to 60 in wPip strain. This group of genes has attracted considerable attention for their astonishing large number as well as for the fact that ankyrin proteins are known to participate in protein-protein interactions, suggesting that they play a critical role in the molecular mechanism that determines host-Wolbachia symbiotic interactions. We present a comparative evolutionary analysis of the wMel-related ankyrin repeat domain-encoding genes present in different Drosophila-Wolbachia associations. Our results show that the ankyrin repeat domain-encoding genes change in size by expansion and contraction mediated by short directly repeated sequences. We provide examples of intragenic recombination events and show that these genes are likely to be horizontally transferred between strains with the aid of bacteriophages. These results confirm previous findings that the Wolbachia genomes are evolutionary mosaics and illustrate the potential that these bacteria have to generate diversity in proteins potentially involved in the symbiotic interactions.

  • 21. Tamas, I
    et al.
    Klasson, L M
    Sandström, J P
    Andersson, S G
    Mutualists and parasites: how to paint yourself into a (metabolic) corner.2001In: FEBS Letters, ISSN 0014-5793, E-ISSN 1873-3468, Vol. 498, no 2-3, p. 135-9Article in journal (Refereed)
    Abstract [en]

    Eukaryotes have developed an elaborate series of interactions with bacteria that enter their bodies and/or cells. Genome evolution of symbiotic and parasitic bacteria multiplying inside eukaryotic cells results in both convergent and divergent changes. The genome sequences of the symbiotic bacteria of aphids, Buchnera aphidicola, and the parasitic bacteria of body louse and humans, Rickettsia prowazekii, provide insights into these processes. Convergent genome characteristics include reduction in genome sizes and lowered G+C content values. Divergent evolution was recorded for amino acid and cell wall biosynthetic genes. The presence of pseudogenes in both genomes provides examples of recent gene inactivation events and offers clues to the process of genome deterioration and host-cell adaptation.

  • 22. Tamas, Ivica
    et al.
    Klasson, Lisa
    Canbäck, Björn
    Näslund, A Kristina
    Eriksson, Ann-Sofie
    Wernegreen, Jennifer J
    Sandström, Jonas P
    Moran, Nancy A
    Andersson, Siv G E
    50 million years of genomic stasis in endosymbiotic bacteria.2002In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 296, no 5577, p. 2376-9Article in journal (Refereed)
    Abstract [en]

    Comparison of two fully sequenced genomes of Buchnera aphidicola, the obligate endosymbionts of aphids, reveals the most extreme genome stability to date: no chromosome rearrangements or gene acquisitions have occurred in the past 50 to 70 million years, despite substantial sequence evolution and the inactivation and loss of individual genes. In contrast, the genomes of their closest free-living relatives, Escherichia coli and Salmonella spp., are more than 2000-fold more labile in content and gene order. The genomic stasis of B. aphidicola, likely attributable to the loss of phages, repeated sequences, and recA, indicates that B. aphidicola is no longer a source of ecological innovation for its hosts.

  • 23. Walker, Thomas
    et al.
    Klasson, Lisa
    Sebaihia, Mohammed
    Sanders, Mandy J
    Thomson, Nicholas R
    Parkhill, Julian
    Sinkins, Steven P