Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: A streamlined genome overrun by mobile genetic elements

Martin Wu, Ling V. Sun, Jessica Vamathevan, Markus Riegler, Robert Deboy, Jeremy C. Brownlie, Elizabeth A. McGraw, William Martin, Christian Esser, Nahal Ahmadinejad, Christian Wiegand, Ramana Madupu, Maureen J. Beanan, Lauren M. Brinkac, Sean C. Daugherty, A. Scott Durkin, James F. Kolonay, William C. Nelson, Yasmin Ali Mohamoud, Perris LeeKristi Berry, M. Brook Young, Teresa Utterback, Janice Weidman, William C. Nierman, Ian T. Paulsen, Karen E. Nelson, Hervé Tettelin, Scott L. O'Neill, Jonathan A. Eisen

Research output: Contribution to journalArticle

514 Citations (Scopus)

Abstract

The complete sequence of the 1,267,782 bp genome of Wolbachia pipientis wMel, an obligate intracellular bacteria of Drosophila melanogaster, has been determined. Wolbachia, which are found in a variety of invertebrate species, are of great interest due to their diverse interactions with different hosts, which range from many forms of reproductive parasitism to mutualistic symbioses. Analysis of the wMel genome, in particular phylogenomic comparisons with other intracellular bacteria, has revealed many insights into the biology and evolution of wMel and Wolbachia in general. For example, the wMel genome is unique among sequenced obligate intracellular species in both being highly streamlined and containing very high levels of repetitive DNA and mobile DNA elements. This observation, coupled with multiple evolutionary reconstructions, suggests that natural selection is somewhat inefficient in wMel, most likely owing to the occurrence of repeated population bottlenecks. Genome analysis predicts many metabolic differences with the closely related Rickettsia species, including the presence of intact glycolysis and purine synthesis, which may compensate for an inability to obtain ATP directly from its host, as Rickettsia can. Other discoveries include the apparent inability of wMel to synthesize lipopolysaccharide and the presence of the most genes encoding proteins with ankyrin repeat domains of any prokaryotic genome yet sequenced. Despite the ability of wMel to infect the germline of its host, we find no evidence for either recent lateral gene transfer between wMel and D. melanogaster or older transfers between Wolbachia and any host. Evolutionary analysis further supports the hypothesis that mitochondria share a common ancestor with the α-Proteobacteria, but shows little support for the grouping of mitochondria with species in the order Rickettsiales. With the availability of the complete genomes of both species and excellent genetic tools for the host, the wMel-D. melanogaster symbiosis is now an ideal system for studying the biology and evolution of Wolbachia infections.

Original languageEnglish
JournalPLoS Biology
Volume2
Issue number3
DOIs
Publication statusPublished - 29 Sep 2004
Externally publishedYes

Fingerprint

Wolbachia pipientis
Wolbachia
Interspersed Repetitive Sequences
Parasites
Genes
Genome
parasites
genome
Drosophila melanogaster
Rickettsia
Mitochondria
Symbiosis
symbiosis
Bacteria
mitochondria
Ankyrin Repeat
Rickettsiales
ankyrins
Gene transfer
Biological Sciences

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Phylogenomics of the reproductive parasite Wolbachia pipientis wMel : A streamlined genome overrun by mobile genetic elements. / Wu, Martin; Sun, Ling V.; Vamathevan, Jessica; Riegler, Markus; Deboy, Robert; Brownlie, Jeremy C.; McGraw, Elizabeth A.; Martin, William; Esser, Christian; Ahmadinejad, Nahal; Wiegand, Christian; Madupu, Ramana; Beanan, Maureen J.; Brinkac, Lauren M.; Daugherty, Sean C.; Durkin, A. Scott; Kolonay, James F.; Nelson, William C.; Ali Mohamoud, Yasmin; Lee, Perris; Berry, Kristi; Young, M. Brook; Utterback, Teresa; Weidman, Janice; Nierman, William C.; Paulsen, Ian T.; Nelson, Karen E.; Tettelin, Hervé; O'Neill, Scott L.; Eisen, Jonathan A.

In: PLoS Biology, Vol. 2, No. 3, 29.09.2004.

Research output: Contribution to journalArticle

Wu, M, Sun, LV, Vamathevan, J, Riegler, M, Deboy, R, Brownlie, JC, McGraw, EA, Martin, W, Esser, C, Ahmadinejad, N, Wiegand, C, Madupu, R, Beanan, MJ, Brinkac, LM, Daugherty, SC, Durkin, AS, Kolonay, JF, Nelson, WC, Ali Mohamoud, Y, Lee, P, Berry, K, Young, MB, Utterback, T, Weidman, J, Nierman, WC, Paulsen, IT, Nelson, KE, Tettelin, H, O'Neill, SL & Eisen, JA 2004, 'Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: A streamlined genome overrun by mobile genetic elements', PLoS Biology, vol. 2, no. 3. https://doi.org/10.1371/journal.pbio.0020069
Wu, Martin ; Sun, Ling V. ; Vamathevan, Jessica ; Riegler, Markus ; Deboy, Robert ; Brownlie, Jeremy C. ; McGraw, Elizabeth A. ; Martin, William ; Esser, Christian ; Ahmadinejad, Nahal ; Wiegand, Christian ; Madupu, Ramana ; Beanan, Maureen J. ; Brinkac, Lauren M. ; Daugherty, Sean C. ; Durkin, A. Scott ; Kolonay, James F. ; Nelson, William C. ; Ali Mohamoud, Yasmin ; Lee, Perris ; Berry, Kristi ; Young, M. Brook ; Utterback, Teresa ; Weidman, Janice ; Nierman, William C. ; Paulsen, Ian T. ; Nelson, Karen E. ; Tettelin, Hervé ; O'Neill, Scott L. ; Eisen, Jonathan A. / Phylogenomics of the reproductive parasite Wolbachia pipientis wMel : A streamlined genome overrun by mobile genetic elements. In: PLoS Biology. 2004 ; Vol. 2, No. 3.
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abstract = "The complete sequence of the 1,267,782 bp genome of Wolbachia pipientis wMel, an obligate intracellular bacteria of Drosophila melanogaster, has been determined. Wolbachia, which are found in a variety of invertebrate species, are of great interest due to their diverse interactions with different hosts, which range from many forms of reproductive parasitism to mutualistic symbioses. Analysis of the wMel genome, in particular phylogenomic comparisons with other intracellular bacteria, has revealed many insights into the biology and evolution of wMel and Wolbachia in general. For example, the wMel genome is unique among sequenced obligate intracellular species in both being highly streamlined and containing very high levels of repetitive DNA and mobile DNA elements. This observation, coupled with multiple evolutionary reconstructions, suggests that natural selection is somewhat inefficient in wMel, most likely owing to the occurrence of repeated population bottlenecks. Genome analysis predicts many metabolic differences with the closely related Rickettsia species, including the presence of intact glycolysis and purine synthesis, which may compensate for an inability to obtain ATP directly from its host, as Rickettsia can. Other discoveries include the apparent inability of wMel to synthesize lipopolysaccharide and the presence of the most genes encoding proteins with ankyrin repeat domains of any prokaryotic genome yet sequenced. Despite the ability of wMel to infect the germline of its host, we find no evidence for either recent lateral gene transfer between wMel and D. melanogaster or older transfers between Wolbachia and any host. Evolutionary analysis further supports the hypothesis that mitochondria share a common ancestor with the α-Proteobacteria, but shows little support for the grouping of mitochondria with species in the order Rickettsiales. With the availability of the complete genomes of both species and excellent genetic tools for the host, the wMel-D. melanogaster symbiosis is now an ideal system for studying the biology and evolution of Wolbachia infections.",
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