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Kampfraath, A. A., Klasson, L., Anvar, S. Y., Vossen, R. H., Roelofs, D., Kraaijeveld, K. & Ellers, J. (2019). Genome expansion of an obligate parthenogenesis-associated Wolbachia poses an exception to the symbiont reduction model. BMC Genomics, 20, Article ID 106.
Öppna denna publikation i ny flik eller fönster >>Genome expansion of an obligate parthenogenesis-associated Wolbachia poses an exception to the symbiont reduction model
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2019 (Engelska)Ingår i: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 20, artikel-id 106Artikel i tidskrift (Refereegranskat) Published
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.

Ort, förlag, år, upplaga, sidor
BMC, 2019
Nyckelord
Folsomia candida, Leptopilina clavipes, wFol, wLcla, Parthenogenesis induction
Nationell ämneskategori
Evolutionsbiologi
Identifikatorer
urn:nbn:se:uu:diva-378385 (URN)10.1186/s12864-019-5492-9 (DOI)000458370700001 ()30727958 (PubMedID)
Tillgänglig från: 2019-03-05 Skapad: 2019-03-05 Senast uppdaterad: 2019-03-05Bibliografiskt granskad
Baiao, G. C., Schneider, D. I., Miller, W. J. & Klasson, L. (2019). The effect of Wolbachia on gene expression in Drosophila paulistorum and its implications for symbiont-induced host speciation. BMC Genomics, 20, Article ID 465.
Öppna denna publikation i ny flik eller fönster >>The effect of Wolbachia on gene expression in Drosophila paulistorum and its implications for symbiont-induced host speciation
2019 (Engelska)Ingår i: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 20, artikel-id 465Artikel i tidskrift (Refereegranskat) Published
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.

Nyckelord
Speciation, symbiosis, Wolbachia, transcriptome, Drosophila paulistorum, host-symbiont interactions
Nationell ämneskategori
Genetik Evolutionsbiologi
Identifikatorer
urn:nbn:se:uu:diva-389597 (URN)10.1186/s12864-019-5816-9 (DOI)000470715200001 ()31174466 (PubMedID)
Forskningsfinansiär
Vetenskapsrådet, 2014-4353
Tillgänglig från: 2019-07-24 Skapad: 2019-07-24 Senast uppdaterad: 2019-07-24Bibliografiskt granskad
Hotopp, J. C. D. & Klasson, L. (2018). The Complexities and Nuances of Analyzing the Genome of Drosophila ananassae and Its Wolbachia Endosymbiont. G3: Genes, Genomes, Genetics, 8(1), 373-374
Öppna denna publikation i ny flik eller fönster >>The Complexities and Nuances of Analyzing the Genome of Drosophila ananassae and Its Wolbachia Endosymbiont
2018 (Engelska)Ingår i: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 8, nr 1, s. 373-374Artikel i tidskrift (Refereegranskat) Published
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.

Ort, förlag, år, upplaga, sidor
GENETICS SOCIETY AMERICA, 2018
Nationell ämneskategori
Biologiska vetenskaper
Identifikatorer
urn:nbn:se:uu:diva-341310 (URN)10.1534/g3.117.300164 (DOI)000419333800033 ()29301977 (PubMedID)
Tillgänglig från: 2018-02-09 Skapad: 2018-02-09 Senast uppdaterad: 2018-02-09Bibliografiskt granskad
Klasson, L. (2017). The unpredictable road to reduction. Nature ecology and evolution, 1, 1062-1063
Öppna denna publikation i ny flik eller fönster >>The unpredictable road to reduction
2017 (Engelska)Ingår i: Nature ecology and evolution, ISSN 2397-334X, Vol. 1, s. 1062-1063Artikel i tidskrift, Editorial material (Övrigt vetenskapligt) Published
Nationell ämneskategori
Mikrobiologi Evolutionsbiologi
Identifikatorer
urn:nbn:se:uu:diva-342160 (URN)10.1038/s41559-017-0263-y (DOI)000417188600009 ()29046587 (PubMedID)
Tillgänglig från: 2018-02-19 Skapad: 2018-02-19 Senast uppdaterad: 2018-03-09Bibliografiskt granskad
Gottlieb, Y., Lalzar, I. & Klasson, L. (2015). Distinctive Genome Reduction Rates Revealed by Genomic Analyses of Two Coxiella-Like Endosymbionts in Ticks. Genome Biology and Evolution, 7(6), 1779-1796
Öppna denna publikation i ny flik eller fönster >>Distinctive Genome Reduction Rates Revealed by Genomic Analyses of Two Coxiella-Like Endosymbionts in Ticks
2015 (Engelska)Ingår i: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 7, nr 6, s. 1779-1796Artikel i tidskrift (Refereegranskat) Published
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.

Nyckelord
symbiosis, genome reduction, Coxiella
Nationell ämneskategori
Biologiska vetenskaper
Identifikatorer
urn:nbn:se:uu:diva-261324 (URN)10.1093/gbe/evv108 (DOI)000358800100028 ()26025560 (PubMedID)
Forskningsfinansiär
Forskningsrådet Formas
Tillgänglig från: 2015-09-02 Skapad: 2015-09-01 Senast uppdaterad: 2017-12-04Bibliografiskt granskad
Klasson, L., Kumar, N., Bromley, R., Sieber, K., Flowers, M., Ott, S. H., . . . Hotopp, J. C. D. (2014). Extensive duplication of the Wolbachia DNA in chromosome four of Drosophila ananassae. BMC Genomics, 15, 1097
Öppna denna publikation i ny flik eller fönster >>Extensive duplication of the Wolbachia DNA in chromosome four of Drosophila ananassae
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2014 (Engelska)Ingår i: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 15, s. 1097-Artikel i tidskrift (Refereegranskat) Published
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.

Nyckelord
Drosophila ananassae, Wolbachia, Lateral gene transfer, Horizontal gene transfer, Symbiosis, Underreplication, Heterochromatin
Nationell ämneskategori
Biologiska vetenskaper
Identifikatorer
urn:nbn:se:uu:diva-243684 (URN)10.1186/1471-2164-15-1097 (DOI)000347575100001 ()25496002 (PubMedID)
Tillgänglig från: 2015-02-18 Skapad: 2015-02-11 Senast uppdaterad: 2017-12-04Bibliografiskt granskad
Schneider, D. I., Klasson, L., Lind, A. E. & Miller, W. J. (2014). More than fishing in the dark: PCR of a dispersed sequence produces simple but ultrasensitive Wolbachia detection. BMC Microbiology, 14, 121
Öppna denna publikation i ny flik eller fönster >>More than fishing in the dark: PCR of a dispersed sequence produces simple but ultrasensitive Wolbachia detection
2014 (Engelska)Ingår i: BMC Microbiology, ISSN 1471-2180, E-ISSN 1471-2180, Vol. 14, s. 121-Artikel i tidskrift (Refereegranskat) Published
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).

Nyckelord
Wolbachia, Drosophila, Glossina, Hybrid, High- and low-titer endosymbiont infection, Limit of detection, A-supergroup repeat motif (ARM)
Nationell ämneskategori
Mikrobiologi
Identifikatorer
urn:nbn:se:uu:diva-227254 (URN)10.1186/1471-2180-14-121 (DOI)000336179000001 ()
Tillgänglig från: 2014-07-02 Skapad: 2014-06-24 Senast uppdaterad: 2017-12-05Bibliografiskt granskad
Ellegaard, K. M., Klasson, L., Näslund, K., Bourtzis, K. & Andersson, S. G. E. (2013). Comparative Genomics of Wolbachia and the Bacterial Species Concept. PLOS Genetics, 9(4), e1003381
Öppna denna publikation i ny flik eller fönster >>Comparative Genomics of Wolbachia and the Bacterial Species Concept
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2013 (Engelska)Ingår i: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 9, nr 4, s. e1003381-Artikel i tidskrift (Refereegranskat) Published
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.

Nationell ämneskategori
Genetik
Identifikatorer
urn:nbn:se:uu:diva-200821 (URN)10.1371/journal.pgen.1003381 (DOI)000318073300004 ()
Tillgänglig från: 2013-06-04 Skapad: 2013-06-04 Senast uppdaterad: 2017-12-06Bibliografiskt granskad
Ellegaard, K. M., Klasson, L. & Andersson, S. G. E. (2013). Testing the Reproducibility of Multiple Displacement Amplification on Genomes of Clonal Endosymbiont Populations. PLoS ONE, 8(11), e82319
Öppna denna publikation i ny flik eller fönster >>Testing the Reproducibility of Multiple Displacement Amplification on Genomes of Clonal Endosymbiont Populations
2013 (Engelska)Ingår i: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, nr 11, s. e82319-Artikel i tidskrift (Refereegranskat) Published
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.

Nationell ämneskategori
Naturvetenskap
Identifikatorer
urn:nbn:se:uu:diva-214040 (URN)10.1371/journal.pone.0082319 (DOI)000327652100111 ()
Tillgänglig från: 2014-01-07 Skapad: 2014-01-07 Senast uppdaterad: 2017-12-06Bibliografiskt granskad
Siozios, S., Ioannidis, P., Klasson, L., Andersson, S. G. E., Braig, H. R. & Bourtzis, K. (2013). The Diversity and Evolution of Wolbachia Ankyrin Repeat Domain Genes. PLoS ONE, 8(2), e55390
Öppna denna publikation i ny flik eller fönster >>The Diversity and Evolution of Wolbachia Ankyrin Repeat Domain Genes
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2013 (Engelska)Ingår i: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, nr 2, s. e55390-Artikel i tidskrift (Refereegranskat) Published
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.

Nationell ämneskategori
Naturvetenskap
Identifikatorer
urn:nbn:se:uu:diva-197401 (URN)10.1371/journal.pone.0055390 (DOI)000314691100051 ()
Tillgänglig från: 2013-04-01 Skapad: 2013-03-25 Senast uppdaterad: 2017-12-06Bibliografiskt granskad
Organisationer
Identifikatorer
ORCID-id: ORCID iD iconorcid.org/0000-0002-5874-7153

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