Bordenstein Seth R.

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Bordenstein
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Seth R.
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  • Article
    New criteria for selecting the origin of DNA replication in Wolbachia and closely related bacteria
    (BioMed Central, 2007-06-20) Ioannidis, Panagiotis ; Dunning Hotopp, Julie C. ; Sapountzis, Panagiotis ; Siozios, Stefanos ; Tsiamis, Georgios ; Bordenstein, Seth R. ; Baldo, Laura ; Werren, John H. ; Bourtzis, Kostas
    Background: The annotated genomes of two closely related strains of the intracellular bacterium Wolbachia pipientis have been reported without the identifications of the putative origin of replication (ori). Identifying the ori of these bacteria and related alpha-Proteobacteria as well as their patterns of sequence evolution will aid studies of cell replication and cell density, as well as the potential genetic manipulation of these widespread intracellular bacteria. Results: Using features that have been previously experimentally verified in the alpha-Proteobacterium Caulobacter crescentus, the origin of DNA replication (ori) regions were identified in silico for Wolbachia strains and eleven other related bacteria belonging to Ehrlichia, Anaplasma, and Rickettsia genera. These features include DnaA-, CtrA- and IHF-binding sites as well as the flanking genes in C. crescentus. The Wolbachia ori boundary genes were found to be hemE and COG1253 protein (CBS domain protein). Comparisons of the putative ori region among related Wolbachia strains showed higher conservation of bases within binding sites. Conclusion: The sequences of the ori regions described here are only similar among closely related bacteria while fundamental characteristics like presence of DnaA and IHF binding sites as well as the boundary genes are more widely conserved. The relative paucity of CtrA binding sites in the ori regions, as well as the absence of key enzymes associated with DNA replication in the respective genomes, suggest that several of these obligate intracellular bacteria may have altered replication mechanisms. Based on these analyses, criteria are set forth for identifying the ori region in genome sequencing projects.
  • Preprint
    Towards a Wolbachia Multilocus Sequence Typing system : discrimination of Wolbachia strains present in Drosophila species
    ( 2006-03-28) Paraskevopoulos, Charalampos ; Bordenstein, Seth R. ; Wernegreen, Jennifer J. ; Werren, John H. ; Bourtzis, Kostas
    Among the diverse maternally inherited symbionts in arthropods, Wolbachia are the most common and infect over 20% of all species. In a departure from traditional genotyping or phylogenetic methods relying on single Wolbachia genes, the present study represents an initial Multilocus Sequence Typing (MLST) analysis to discriminate closely related Wolbachia pipientis strains, and additional data on sequence diversity in Wolbachia. We report new phylogenetic characterization of four genes (aspC, atpD, sucB and pdhB), and provide an expanded analysis of markers described in previous studies (16S rDNA, ftsZ, groEL, dnaA and gltA). MLST analysis of the bacterial strains present in sixteen different Drosophila-Wolbachia associations detected four distinct clonal complexes that also corresponded to maximum-likelihood identified phylogenetic clades. Among the sixteen associations analyzed, six could not be assigned to MLST clonal complexes and were also shown to be in conflict with relationships predicted by maximum-likelihood phylogenetic inferences. The results demonstrate the discriminatory power of MLST for identifying strains and clonal lineages of Wolbachia and provide a robust foundation for studying the ecology and evolution of this widespread endosymbiont.
  • Preprint
    Bidirectional incompatibility among divergent Wolbachia and incompatibility level differences among closely related Wolbachia in Nasonia
    ( 2007-03-07) Bordenstein, Seth R. ; Werren, John H.
    Most insect groups harbor obligate bacterial symbionts from the alphaproteobacterial genus Wolbachia. These bacteria alter insect reproduction in ways that enhance their cytoplasmic transmission. One of the most common alterations is cytoplasmic incompatibility (CI) - a post-fertilization modification of the paternal genome that renders embryos inviable or unable to complete diploid development in crosses between infected males and uninfected females or infected females harboring a different strain. The parasitic wasp species complex Nasonia (N. vitripennis, N. longicornis, and N. giraulti) harbor at least six different Wolbachia that cause cytoplasmic incompatibility. Each species have double infections with a representative from both the A and B Wolbachia subgroups. CI relationships of the A and B Wolbachia of N. longicornis with those of N. giraulti and N. vitripennis are investigated here. We demonstrate that all pairwise crosses between the divergent A strains are bidirectionally incompatible. We were unable to characterize incompatibility between the B Wolbachia, but we establish that the B strain of N. longicornis induces no or very weak CI in comparison to the closely related B strain in N. giraulti that expresses complete CI. Taken together with previous studies, we show that independent acquisition of divergent A Wolbachia has resulted in three mutually incompatible strains, while codivergence of B Wolbachia in N. longicornis and N. giraulti is associated with differences in CI level. Understanding the diversity and evolution of new incompatibility strains will contribute to a fuller understanding of Wolbachia invasion dynamics and Wolbachia-assisted speciation in certain groups of insects.
  • Preprint
    Discovery of a novel Wolbachia supergroup in Isoptera
    ( 2005-05-23) Bordenstein, Seth R. ; Rosengaus, Rebeca B.
    Wolbachia are one of the most abundant groups of bacterial endosymbionts in the biosphere. Interest in these heritable microbes has expanded with the discovery of wider genetic diversity in undersampled host species. Here, we report on the putative discovery of a new genetic lineage, denoted supergroup H, which infects the Isopteran species Zootermopsis angusticollis and Z. nevadensis. Evidence for this novel supergroup is based on portions of new Wolbachia gene sequences from each species spanning 3.5 kilobases of DNA and the following genes: 16S rDNA, dnaA, gltA, groEL, and ftsZ. Single-gene and concatenated maximum likelihood phylogenies establish this new supergroup and validate the positioning of the other Wolbachia supergroups. This discovery is the first example of a termite Wolbachia that is highly divergent from the Isopteran Wolbachia previously described in supergroup F. This study highlights the importance of multilocus approaches to resolving Wolbachia supergroup relationships. It also suggests that surveys of Wolbachia in more earlier-originating (and undersampled) groups of arthropods are more apt to reveal novel genetic diversity.
  • Article
    Comparative sequence analysis of IS50/Tn5 transposase
    (American Society for Microbiology, 2004-12) Reznikoff, William S. ; Bordenstein, Seth R. ; Apodaca, Jennifer
    Comparative sequence analysis of IS50 transposase-related protein sequences in conjunction with known structural, biochemical, and genetic data was used to determine domains and residues that play key roles in IS50 transposase function. BLAST and ClustalW analyses have been used to find and analyze six complete protein sequences that are related to the IS50 transposase. The protein sequence identity of these six homologs ranged from 25 to 55% in comparison to the IS50 transposase. Homologous motifs were found associated with each of the three catalytic residues. Residues that play roles in transposase-DNA binding, protein autoregulation, and DNA hairpin formation were also found to be conserved in addition to other residues of unknown function. On the other hand, some homologous sequences did not appear to be competent to encode the inhibitor regulatory protein. The results were also used to compare the IS50 transposase with the more distantly related transposase encoded by IS10.
  • Article
    The tripartite associations between bacteriophage, Wolbachia, and arthropods
    (Public Library of Science (PLoS), 2006-05-19) Bordenstein, Seth R. ; Marshall, Michelle L. ; Fry, Adam J. ; Kim, Ulandt ; Wernegreen, Jennifer J.
    By manipulating arthropod reproduction worldwide, the heritable endosymbiont Wolbachia has spread to pandemic levels. Little is known about the microbial basis of cytoplasmic incompatibility (CI) except that bacterial densities and percentages of infected sperm cysts associate with incompatibility strength. The recent discovery of a temperate bacteriophage (WO-B) of Wolbachia containing ankyrin-encoding genes and virulence factors has led to intensifying debate that bacteriophage WO-B induces CI. However, current hypotheses have not considered the separate roles that lytic and lysogenic phage might have on bacterial fitness and phenotype. Here we describe a set of quantitative approaches to characterize phage densities and its associations with bacterial densities and CI. We enumerated genome copy number of phage WO-B and Wolbachia and CI penetrance in supergroup A- and B-infected males of the parasitoid wasp Nasonia vitripennis. We report several findings: (1) variability in CI strength for A-infected males is positively associated with bacterial densities, as expected under the bacterial density model of CI, (2) phage and bacterial densities have a significant inverse association, as expected for an active lytic infection, and (3) CI strength and phage densities are inversely related in A-infected males; similarly, males expressing incomplete CI have significantly higher phage densities than males expressing complete CI. Ultrastructural analyses indicate that approximately 12% of the A Wolbachia have phage particles, and aggregations of these particles can putatively occur outside the Wolbachia cell. Physical interactions were observed between approximately 16% of the Wolbachia cells and spermatid tails. The results support a low to moderate frequency of lytic development in Wolbachia and an overall negative density relationship between bacteriophage and Wolbachia. The findings motivate a novel phage density model of CI in which lytic phage repress Wolbachia densities and therefore reproductive parasitism. We conclude that phage, Wolbachia, and arthropods form a tripartite symbiotic association in which all three are integral to understanding the biology of this widespread endosymbiosis. Clarifying the roles of lytic and lysogenic phage development in Wolbachia biology will effectively structure inquiries into this research topic.
  • Preprint
    Disruption of termite gut-microbiota and its prolonged fitness consequences
    ( 2011-05) Rosengaus, Rebeca B. ; Zecher, Courtney N. ; Schultheis, Kelley F. ; Brucker, Robert M. ; Bordenstein, Seth R.
    The disruption of host-symbiont interactions through the use of antibiotics can help elucidate microbial functions that go beyond short-term nutritional value. Termite gut symbionts have been studied extensively, but little is known about their impact on the termite’s reproductive output. Here we describe the effect that the antibiotic rifampin has not only on the gut microbial diversity, but also on the longevity, fecundity, and weight of two termite species - Zootermopsis angusticollis and Reticulitermes flavipes. We report three key findings: (i) the antibiotic rifampin, when fed to primary reproductives during the incipient stages of colony foundation, causes a permanent reduction in the diversity of gut bacteria, and a transitory effect on the density of the protozoan community, (ii) rifampin treatment reduces oviposition rates of queens, translating into delayed colony growth and ultimately reduced colony fitness and (iii) the initial dosages of rifampin on reproduction and colony fitness had severe longterm fitness effects on Z. angusticollis survivorship and colony size. Taken together, our findings demonstrate that the antibiotic-induced perturbation of the microbial community associates with prolonged reductions in longevity and fecundity. A causal relationship between these changes in the gut microbial population structures and fitness is suggested by the acquisition of opportunistic pathogens and incompetence of the termites to restore a pre-treatment, native microbiota. Our results indicate that antibiotic treatment significantly alters the termite’s microbiota, reproduction, colony establishment and ultimately, colony growth and development. We discuss the implications for antimicrobials as a new application to the control of termite pest species.