58
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Palaeosymbiosis Revealed by Genomic Fossils of Wolbachia in a Strongyloidean Nematode

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Wolbachia are common endosymbionts of terrestrial arthropods, and are also found in nematodes: the animal-parasitic filaria, and the plant-parasite Radopholus similis. Lateral transfer of Wolbachia DNA to the host genome is common. We generated a draft genome sequence for the strongyloidean nematode parasite Dictyocaulus viviparus, the cattle lungworm. In the assembly, we identified nearly 1 Mb of sequence with similarity to Wolbachia. The fragments were unlikely to derive from a live Wolbachia infection: most were short, and the genes were disabled through inactivating mutations. Many fragments were co-assembled with definitively nematode-derived sequence. We found limited evidence of expression of the Wolbachia-derived genes. The D. viviparus Wolbachia genes were most similar to filarial strains and strains from the host-promiscuous clade F. We conclude that D. viviparus was infected by Wolbachia in the past, and that clade F-like symbionts may have been the source of filarial Wolbachia infections.

          Author Summary

          Bovine lungworms are economically important nematode parasites of cattle. We have sequenced the genome of the bovine lungworm to provide information for drug and vaccine discovery. Within the lungworm genome we found extensive evidence of an ancient association between the lungworm and a bacterium called Wolbachia. The lungworm Wolbachia is now a “fossil” in the genome, but tells of an ancient infection. Association between lungworms, and related nematode worms, and Wolbachia was not known previously. We have used the lungworm Wolbachia sequence to explore the history of nematode- Wolbachia interactions, particularly the jumping of these symbionts between arthropods and nematodes.

          Related collections

          Most cited references46

          • Record: found
          • Abstract: found
          • Article: not found

          Genome sequence of the nematode C. elegans: a platform for investigating biology.

          (1999)
          The 97-megabase genomic sequence of the nematode Caenorhabditis elegans reveals over 19,000 genes. More than 40 percent of the predicted protein products find significant matches in other organisms. There is a variety of repeated sequences, both local and dispersed. The distinctive distribution of some repeats and highly conserved genes provides evidence for a regional organization of the chromosomes.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Wolbachia as a bacteriocyte-associated nutritional mutualist.

            Many insects are dependent on bacterial symbionts that provide essential nutrients (ex. aphid-Buchnera and tsetse-Wiglesworthia associations), wherein the symbionts are harbored in specific cells called bacteriocytes that constitute a symbiotic organ bacteriome. Facultative and parasitic bacterial symbionts like Wolbachia have been regarded as evolutionarily distinct from such obligate nutritional mutualists. However, we discovered that, in the bedbug Cimex lectularius, Wolbachia resides in a bacteriome and appears to be an obligate nutritional mutualist. Two bacterial symbionts, a Wolbachia strain and an unnamed gamma-proteobacterium, were identified from different strains of the bedbug. The Wolbachia symbiont was detected from all of the insects examined whereas the gamma-proteobacterium was found in a part of them. The Wolbachia symbiont was specifically localized in the bacteriomes and vertically transmitted via the somatic stem cell niche of germalia to oocytes, infecting the incipient symbiotic organ at an early stage of the embryogenesis. Elimination of the Wolbachia symbiont resulted in retarded growth and sterility of the host insect. These deficiencies were rescued by oral supplementation of B vitamins, confirming the essential nutritional role of the symbiont for the host. The estimated genome size of the Wolbachia symbiont was around 1.3 Mb, which was almost equivalent to the genome sizes of parasitic Wolbachia strains of other insects. These results indicate that bacteriocyte-associated nutritional mutualism can evolve from facultative and prevalent microbial associates like Wolbachia, highlighting a previously unknown aspect of the parasitism-mutualism evolutionary continuum.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes.

              Although common among bacteria, lateral gene transfer-the movement of genes between distantly related organisms-is thought to occur only rarely between bacteria and multicellular eukaryotes. However, the presence of endosymbionts, such as Wolbachia pipientis, within some eukaryotic germlines may facilitate bacterial gene transfers to eukaryotic host genomes. We therefore examined host genomes for evidence of gene transfer events from Wolbachia bacteria to their hosts. We found and confirmed transfers into the genomes of four insect and four nematode species that range from nearly the entire Wolbachia genome (>1 megabase) to short (<500 base pairs) insertions. Potential Wolbachia-to-host transfers were also detected computationally in three additional sequenced insect genomes. We also show that some of these inserted Wolbachia genes are transcribed within eukaryotic cells lacking endosymbionts. Therefore, heritable lateral gene transfer occurs into eukaryotic hosts from their prokaryote symbionts, potentially providing a mechanism for acquisition of new genes and functions.
                Bookmark

                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                June 2014
                5 June 2014
                : 10
                : 6
                : e1004397
                Affiliations
                [1 ]Institute of Evolutionary Biology, The University of Edinburgh, Edinburgh, United Kingdom
                [2 ]Institute of Infection and Global Health, The University of Liverpool, Liverpool, United Kingdom
                [3 ]Institut de Recherche Agricole pour le Développement, Regional Centre of Wakwa, Ngaoundéré, Adamawa Region, Cameroon
                University of Utah School of Medicine, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MB GK BM VNT. Performed the experiments: VNT BM GK MB. Analyzed the data: GK MB. Contributed reagents/materials/analysis tools: VNT BM. Wrote the paper: MB GK BM.

                Article
                PGENETICS-D-14-00228
                10.1371/journal.pgen.1004397
                4046930
                24901418
                a99b16ec-4011-418a-aee2-80250697c8f0
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 February 2014
                : 6 April 2014
                Page count
                Pages: 15
                Funding
                GK is supported by the BBSRC through a PhD studentship, and the School of Biological Sciences, University of Edinburgh. This work was supported in part by the EU EPIAF programme (contract HEALTH-F3-2010-242131). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Computational Biology
                Comparative Genomics
                Genome Evolution
                Evolutionary Biology
                Genetics
                Genomics
                Molecular Biology
                Molecular Biology Techniques
                Sequencing Techniques
                Genome Sequencing
                Parasitology
                Zoology

                Genetics
                Genetics

                Comments

                Comment on this article