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      Wolbachia: Evolutionary novelty in a rickettsial bacteria

      research-article
      1 , 2 , ,
      BMC Evolutionary Biology
      BioMed Central

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          Abstract

          Background

          Although closely related, the alpha-proteobacteria Wolbachia and the Rickettsiacae ( Rickettsia and Ehrlichia), employ different evolutionary life history strategies. Wolbachia are obligate endocellular symbionts that infect an extraordinary host range and, in contrast to the infectious and pathogenic Rickettsia and Ehrlichia, profoundly influence host reproductive biology.

          Results

          Phylogenies of the Rickettsia, Ehrlichia, and Wolbachia were independently inferred from 16S rDNA sequences and GroEL amino acid sequences. Topologies inferred from both sets of sequence data were consistent with one another, and both indicate the genus Wolbachia shared a common ancestor most recently with Ehrlichia. These two genera are a sister group to the genus Rickettsia. Mapping biological properties onto this phylogeny reveals that manipulation of host reproduction, characteristic of Wolbachia strains, is a derived characteristic. This evolutionary novelty is accompanied by the loss of the ability to infect vertebrate hosts.

          Conclusions

          Because of the contrasting transmission strategies employed by each, Wolbachia is expected to maximize efficiency of vertical transmission, while Ehrlichia and Rickettsia will optimize horizontal transfer of infection. Wolbachia manipulation of host reproduction could thus be viewed as strategy employed by this bacterium to foster its own propagation via vertical transmission.

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          Most cited references14

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          Molecular identification of microorganisms associated with parthenogenesis.

          Cytoplasmically interited microorganisms are widespread in insects and have been implicated as causes of female parthenogenesis (females developing from unfertilized eggs) and cytoplasmic incompatibility. Normal sexual reproduction can be restored by treatment with antibiotics. Sequence analysis of the DNA encoding 16S ribosomal RNA has shown that cytoplasmic incompatibility bacteria from diverse insect taxa are closely related (they share >95% sequence sililarity) and belong to the alpha subdivision of Proteobacteria. Here we show that parthenogenesis-associated bacteria from parasitoid Hymenoptera also fall into this bacterial group, having up to 99% sequence similarity to some incompatibility microorganisms. Both incompatibility and parthenogenesis microorganisms alter host chromosome behaviour during early mitotic divisions of the egg. Incompatibility bacteria act by interfering with paternal chromosome incorporation in fertilized eggs, whereas parthenogenesis bacteria prevent segregation of chromosomes in unfertilized eggs. These traits are adaptive for the microorganisms. On the basis of their sequence similarities, we conclude that parthenogenesis bacteria and cytoplasmic incompatibility bacteria form a monophyletic group of microorganisms that 'specialize' in manipulating chromosome behaviour and reproduction of insects.
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            Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila.

            Cytoplasmic incompatibility (CI) in Drosophila simulans is related to infection of the germ line by a rickettsial endosymbiont (genus Wolbachia). Wolbachia were transferred by microinjection of egg cytoplasm into uninfected eggs of both D. simulans and D. melanogaster to generate infected populations. Transinfected strains of D. melanogaster with lower densities of Wolbachia than the naturally infected D. simulans strain did not express high levels of CI. However, transinfected D. melanogaster egg cytoplasm, transferred back into D. simulans, generated infected populations that expressed CI at levels near those of the naturally infected strain. A transinfected D. melanogaster line selected for increased levels of CI expression also displayed increased symbiont densities. These data suggest that a threshold level of infection is required for normal expression of CI and that host factors help determine the density of the symbiont in the host.
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              A new rickettsia from a herbivorous insect, the pea aphid Acyrthosiphon pisum (Harris).

              An undescribed, maternally heritable, rod-shaped bacterium (or "tertiary symbiont") was detected by microscopy in hemolymph of about half (59/122) of pea aphid [Acyrthosiphon pisum (Harris)] clones collected from widely separated locations in California. On the basis of molecular phylogenetic analysis of 16S rDNA sequences, the bacterium was clearly placed among other Rickettsia in the alpha-subgroup of Proteobacteria, close to Rickettsia bellii-a rickettsia found in ticks. A PCR assay was developed to detect this bacterium in pea aphid clones with specific 16S rDNA PCR primers. Results of PCR-based assays completely correlated with detection by microscopy. This is the first confirmed detection of a Rickettsia in a herbivorous insect.
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                Author and article information

                Journal
                BMC Evol Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                2001
                9 November 2001
                : 1
                : 10
                Affiliations
                [1 ]Department of Organismal Biology and Anatomy, University of Chicago, 1027 E. 57 th Street, Chicago, II 60637 USA
                [2 ]Laboratory for Ecological and Conservation Genetics, College of Natural Resources, University of Idaho, Moscow, ID 83843-1136 USA
                Article
                1471-2148-1-10
                10.1186/1471-2148-1-10
                60491
                11734058
                52c8807c-0fdd-4d21-adc1-f7fd6ef90fe1
                Copyright © 2001 Anderson and Karr; licensee BioMed Central Ltd. Verbatim copying and redistribution of this article are permitted in any medium for any non-commercial purpose, provided this notice is preserved along with the article's original URL. For commercial use, contact info@biomedcentral.com
                History
                : 30 August 2001
                : 9 November 2001
                Categories
                Research Article

                Evolutionary Biology
                Evolutionary Biology

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