Phylogenomics of the Reproductive Parasite Wolbachia pipientis wMel: A Streamlined Genome Overrun by Mobile Genetic Elements
Open accessAbstract
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 alpha-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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Wolbachia does not possess LPSs.
“which are molecules that are usually involved in bacterium-driven inflammation (421) and that Wolbachia does not possess (454).”
From Human and animal dirofilariasis: The emergence of a zoonotic mosaic (2012) · cites this paper as [454]
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“The only noteworthy DNA repair gene absent from w Mel and present in the more slowly evolving Rickettsia is mfd, which is involved in targeting DNA repair to the transcribed strand of actively transcribing genes in other species (Selby et al. 1991).”
A phylogenomic study of the MutS family of proteins
Eisen, J. A. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.18.4291 · Cited by 208 · cited 2× · see citing works
“…without high evolutionary rates have lost some of the same pathways lost in intracellular species, while many free-living species have lost key pathways resulting in high mutation rates (e.g., Helicobacter pylori has apparently lost mismatch repair [Eisen1997, Eisen 1998b; Bjorkholm et al. 2001]).”
Self-citationThe evolution of heritable symbionts
(1997) · doi:10.1093/oso/9780198577867.003.0001 · Cited by 197 · see citing works
In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line
O’Neill, S. L., Pettigrew, M. M., Sinkins, S. P., Braig, H. R., Andreadis, T. G., & Tesh, R. B. (1997) · Insect Molecular Biology · doi:10.1046/j.1365-2583.1997.00157.x · Cited by 184 · see citing works
Self-citationEvidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes
Wernegreen, J. J., & Moran, N. A. (1999) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026040 · Cited by 183 · see citing works
Type IVB Secretion by Intracellular Pathogens
Sexton, J. A., & Vogel, J. P. (2002) · Traffic · doi:10.1034/j.1600-0854.2002.030303.x · Cited by 181 · cited 1× · see citing works
“An increasing body of evidence has highlighted the importance of Type IV secretion systems for the successful infection, invasion, and persistence of intracellular bacteria within their hosts (Christie 2001; Sexton and Vogel 2002).”
BackgroundAcceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts
Itoh, T., Martin, W. F., & Nei, M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.192449699 · Cited by 151 · cited 1× · see citing works
“It has been suggested that the higher evolutionary rates in intracellular bacteria are the result of high mutation rates that are in turn due to the loss of genes for DNA repair processes (e.g., Itoh et al. 2002).”
Self-citationA clustering method for repeat analysis in DNA sequences
Volfovsky, N., Haas, B. J., & Salzberg, S. L. (2001) · Genome biology · doi:10.1186/gb-2001-2-8-research0027 · Cited by 149 · see citing works
Caturegli, P., Asanovich, K. M., Walls, J. J., Bakken, J., Madigan, J. E., Popov, V. L., & Dumler, J. S. (2000) · Infection and Immunity · doi:10.1128/iai.68.9.5277-5283.2000 · Cited by 144 · cited 3× · see citing works
“(Caturegli et al. 2000); (iii) some of the proteins that modify the activity of cell-cycle-regulating proteins in D.”
BackgroundInfluentialOptimized Multiplex PCR: Efficiently Closing a Whole-Genome Shotgun Sequencing Project
Tettelin, H., Radune, D., Kasif, S., Khouri, H. M., & Salzberg, S. L. (1999) · Genomics · doi:10.1006/geno.1999.6048 · Cited by 140 · cited 19× · see citing works
“PCR products were cloned into pGem-T vector (Promega, Madison, Wisconsin, United States) as previously described (Zhou et al. 1998) and sequenced (Genbank accession numbers AJ580921–AJ508923).”
InfluentialSelf-citationMitochondrial connection to the origin of the eukaryotic cell
Emelyanov, V. V. (2003) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2003.03499.x · Cited by 118 · cited 1× · see citing works
“…have further suggested that mitochondria are a sister taxa to the Rickettsia genus within the Rickettsiaceae family and thus more closely related to Rickettsia spp. than to species in the Anaplasma-taceae family such as Wolbachia (Karlin and Brocchieri 2000; Emelyanov 2001a, 2001b, 2003a, 2003b).”
Phylogenetic Analysis and Gene Functional Predictions: Phylogenomics in Action
Eisen, J. A., & Wu, M. (2002) · Theoretical Population Biology · doi:10.1006/tpbi.2002.1594 · Cited by 118 · cited 2× · see citing works
“The results of these searches were used (i) to analyze the phylogenetic profile (Pellegrini et al. 1999; Eisen and Wu 2002), (ii) to identify putative lineagespecific duplications (those proteins with a top E-value score to another protein from wMel), and (iii) to determine the presence of homologs in different specie…”
Self-citationThe chaperone connection to the origins of the eukaryotic organelles
Viale, A. M., & Arakaki, A. K. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)80446-x · Cited by 112 · cited 1× · see citing works
“Many studies have placed them in or near the Rickettsiales order (Viale and Arakaki 1994; Gupta 1995; Sicheritz-Ponten et al. 1998; Lang et al. 1999; Bazinet and Rollins 2003).”
BackgroundWolbachia Bacteria of Filarial Nematodes: A Target for Control?
Taylor, M. J., Bandi, C., Hoerauf, A. M., & Lazdins, J. K. (2000) · Parasitology Today · doi:10.1016/s0169-4758(00)01661-6 · Cited by 112 · cited 2× · see citing works
“…worms that cause filariasis have an obligate symbiosis with mutualistic Wolbachia , treatment of filariasis with simple antibiotics that target Wolbachia has been shown to eliminate microfilaria production as well as ultimately killing the adult worm (Taylor et al. 2000; Taylor and Hoerauf 2001).”
A new approach to the treatment of filariasis
Taylor, M. J., & Hoerauf, A. M. (2001) · Current Opinion in Infectious Diseases · doi:10.1097/00001432-200112000-00011 · Cited by 110 · cited 2× · see citing works
“…worms that cause filariasis have an obligate symbiosis with mutualistic Wolbachia , treatment of filariasis with simple antibiotics that target Wolbachia has been shown to eliminate microfilaria production as well as ultimately killing the adult worm (Taylor et al. 2000; Taylor and Hoerauf 2001).”
Wolbachia as a vehicle to modify insect populations
Sinkins, S. P., & O’Neill, S. L. (2000) · Cited by 106 · see citing works
Self-citationThe decaying genome ofMycobacterium leprae
Eiglmeier, K., Parkhill, J., Honoré, N., Garnier, T., Tekaia, F., Telenti, A., Klatser, P. R., James, K., THOMSON, N. R., Wheeler, P. R., et al. (2001) · Leprosy Review · doi:10.5935/0305-7518.20010047 · Cited by 100 · cited 1× · see citing works
“Such inefficiencies of natural selection are generally due to an increase in the relative contribution of genetic drift and mutation as compared to natural selection (Eiglmeier et al. 2001; Lawrence 2001; Parkhill et al. 2001).”
Wolbachia-mediated sperm modification is dependent on the host genotype inDrosophila
McGraw, E. A., Merritt, D. J., Droller, J. N., & O’Neill, S. L. (2001) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2001.1839 · Cited by 100 · cited 2× · see citing works
“[McGraw et al. 2001]) by altering or disrupting gene function”
Self-citationHansmann, S., & Martin, W. (2000) · International Journal of Systematic and Evolutionary Microbiology · doi:10.1099/00207713-50-4-1655 · Cited by 99 · cited 1× · see citing works
“When the data were iteratively purged of highly variable sites using the method described (Hansmann and Martin 2000), amino acid composition gradually came into better agreement with acid frequency distribution assumed by the model.”
MethodSelf-citationBacteriophage WO and Virus-like Particles in Wolbachia, an Endosymbiont of Arthropods
Masui, S., Kuroiwa, H., Sasaki, T., Inui, M., Kuroiwa, T., & Ishikawa, H. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.4906 · Cited by 96 · cited 8× · see citing works
“Putative proteins in wKue (Masui et al. 2001) were searched using TBLASTN against the wMel genome.”
InfluentialGenome deterioration: loss of repeated sequences and accumulation of junk DNA
Frank, A. C., Amiri, H., & Andersson, S. G. E. (2002) · Genetica · doi:10.1023/a:1016064511533 · Cited by 89 · cited 1× · see citing works
“The paucity of repetitive DNA in these and other intracellular species is thought to be due to a combination of lack of exposure to other species, thereby limiting introduction of mobile elements, and genome streamlining (Mira et al. 2001; Moran and Mira 2001; Frank et al. 2002).”
BackgroundDetermination ofWolbachiaGenome Size by Pulsed-Field Gel Electrophoresis
Sun, L. V., Foster, J. M., Tzertzinis, G., Ono, M., Bandi, C., Slatko, B. E., & O’Neill, S. L. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.7.2219-2225.2001 · Cited by 88 · cited 4× · see citing works
“was purified from young adult flies on pulsed-field gels as described previously (Sun et al. 2001).”
InfluentialSelf-citationEvolutionary relationship of Rickettsiae and mitochondria
Emelyanov, V. V. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02618-7 · Cited by 87 · cited 2× · see citing works
“…have further suggested that mitochondria are a sister taxa to the Rickettsia genus within the Rickettsiaceae family and thus more closely related to Rickettsia spp. than to species in the Anaplasma-taceae family such as Wolbachia (Karlin and Brocchieri 2000; Emelyanov 2001a, 2001b, 2003a, 2003b).”
A Comparative Genomics Approach to the Evolution of Eukaryotes and their Mitochondria1
Lang, B. F., Seif, E., Gray, M. W., O’Kelly, C. J., & Burger, G. (1999) · Journal of Eukaryotic Microbiology · doi:10.1111/j.1550-7408.1999.tb04611.x · Cited by 86 · cited 2× · see citing works
“Many studies have placed them in or near the Rickettsiales order (Viale and Arakaki 1994; Gupta 1995; Sicheritz-Ponten et al. 1998; Lang et al. 1999; Bazinet and Rollins 2003).”
Karlin, S., & Brocchieri, L. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.21.11348 · Cited by 82 · cited 2× · see citing works
“than to species in the Anaplasmataceae family such as Wolbachia (Karlin and Brocchieri 2000; Emelyanov 2001a, 2001b, 2003a, 2003b).”
Jamnongluk, W., Kittayapong, P., Baimai, V., & O’Neill, S. L. (2002) · Current Microbiology · doi:10.1007/s00284-002-3746-1 · Cited by 81 · cited 1× · see citing works
“…DNA was introduced via phage, given that three prophage elements are present; experimental studies have shown active phage in some Wolbachia (Masui et al. 2001) and Wolbachia super-infections occur in many hosts (e.g., Jamnongluk et al. 2002), which would allow phage to move between strains.”
Self-citationSicheritz‐Pontén, T., Kurland, C. G., & Andersson, S. G. E. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00099-1 · Cited by 80 · cited 1× · see citing works
“Many studies have placed them in or near the Rickettsiales order (Viale and Arakaki 1994; Gupta 1995; Sicheritz-Ponten et al. 1998; Lang et al. 1999; Bazinet and Rollins 2003).”
BackgroundRoelofs, J., & Haastert, P. J. M. V. (2001) · Nature · doi:10.1038/35082627 · Cited by 80 · cited 1× · see citing works
“In particular, claims of transfer from bacteria into the human genome (Lander et al. 2001) were later shown to be false (Roelofs and Van Haastert 2001; Salzberg et al. 2001; Stanhope et al. 2001).”
Masui, S., Sasaki, T., & Ishikawa, H. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.22.6529-6531.2000 · Cited by 71 · cited 1× · see citing works
“This has apparently occurred in one study of Wolbachia strain w KueYO, for which the reported wsp gene (gbAB045235) is actually an ortholog of wspB (99.8% sequence identity and located at the end of the virB operon [Masui et al. 2000]) and not an ortholog of the wsp gene.”
InfluentialCatalyzing Bacterial Speciation: Correlating Lateral Transfer with Genetic Headroom
Lawrence, J. G. (2001) · Systematic Biology · doi:10.1080/10635150120286 · Cited by 58 · cited 1× · see citing works
“Such inefficiencies of natural selection are generally due to an increase in the relative contribution of genetic drift and mutation as compared to natural selection (Eiglmeier et al. 2001; Lawrence 2001; Parkhill et al. 2001).”
Rickettsiaceae, Rickettsia-Like Endosymbionts, and the Origin of Mitochondria
Emelyanov, V. V. (2001) · Bioscience Reports · doi:10.1023/a:1010409415723 · Cited by 49 · cited 1× · see citing works
“…have further suggested that mitochondria are a sister taxa to the Rickettsia genus within the Rickettsiaceae family and thus more closely related to Rickettsia spp. than to species in the Anaplasma-taceae family such as Wolbachia (Karlin and Brocchieri 2000; Emelyanov 2001a, 2001b, 2003a, 2003b).”
Ankyrins, multifunctional proteins involved in many cellular pathways.
Hryniewicz‐Jankowska, A., Czogalla, A., Bok, E., & Sikorsk, A. F. (2002) · PubMed · Cited by 48 · see citing works
Roots: Mutation frequency decline revisited
Witkin, E. M. (1994) · BioEssays · doi:10.1002/bies.950160613 · Cited by 46 · cited 2× · see citing works
“However, this absence is unlikely to contribute significantly to the increased evolutionary rate in wMel, since defects in mfd do not lead to large increases in mutation rates in other species (Witkin 1994).”
Elfring, L. K., Axton, M., Fenger, D. D., Page, A. W., Carminati, J. L., & Orr‐Weaver, T. L. (1997) · Molecular Biology of the Cell · doi:10.1091/mbc.8.4.583 · Cited by 46 · cited 2× · see citing works
“…et al. 2000); (iii) some of the proteins that modify the activity of cell-cycle-regulating proteins in D. melanogaster contain ankyrin repeats (Elfring et al. 1997); and (iv) the Wolbachia strain that infects the wasp Nasonia vitripennis induces cytoplasmic incompatibility, likely by…”
BackgroundGastrogenomic delights: A movable feast
Eisen, J. A., Kaiser, D., & Myers, R. (1997) · Nature Medicine · doi:10.1038/nm1097-1076 · Cited by 45 · cited 1× · see citing works
“…without high evolutionary rates have lost some of the same pathways lost in intracellular species, while many free-living species have lost key pathways resulting in high mutation rates (e.g., Helicobacter pylori has apparently lost mismatch repair [Eisen1997, Eisen 1998b; Bjorkholm et al. 2001]).”
BackgroundSelf-citationDevelopment ofa Physical and Genetic Map of the VirulentWolbachiaStrainwMelPop
Sun, L. V., Riegler, M., & O’Neill, S. L. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.24.7077-7084.2003 · Cited by 29 · see citing works
Self-citationRickettsia‐like mitochondrial motility in Drosophila spermiogenesis
Bazinet, C. W., & Rollins, J. E. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03045.x · Cited by 26 · cited 1× · see citing works
“Many studies have placed them in or near the Rickettsiales order (Viale and Arakaki 1994; Gupta 1995; Sicheritz-Ponten et al. 1998; Lang et al. 1999; Bazinet and Rollins 2003).”
BackgroundEmelyanov, V. V. (2003) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(03)00598-6 · Cited by 25 · cited 2× · see citing works
“…have further suggested that mitochondria are a sister taxa to the Rickettsia genus within the Rickettsiaceae family and thus more closely related to Rickettsia spp. than to species in the Anaplasma-taceae family such as Wolbachia (Karlin and Brocchieri 2000; Emelyanov 2001a, 2001b, 2003a, 2003b).”
A New Insight into the Pathogenesis of Filarial Disease
Taylor, M. J. (2002) · Current Molecular Medicine · doi:10.2174/1566524024605662 · Cited by 23 · cited 2× · see citing works
“Thus, the reports that Wolbachia -derived LPS-like compounds is involved in the immunopathology of filarial nematode disease in mammals (Taylor 2002) either indicate that these Wolbachia have acquired genes for LPS synthesis or that the reported LPS-like compounds are not homologous to LPS.”
Ware, J., Moran, L. S., Foster, J. M., Pósfai, J., Vincze, T., Guiliano, D. B., Blaxter, M., Eisen, J. A., & Slatko, B. E. (2002) · International Journal for Parasitology · doi:10.1016/s0020-7519(01)00367-8 · Cited by 13 · cited 3× · see citing works
“malayi region is from a BAC clone (Ware et al. 2002).”
InfluentialSelf-citationEvolutionary inference from genomic data
Goldstein, D. B., & Harvey, P. (1999) · BioEssays · doi:10.1002/(sici)1521-1878(199902)21:2 · Cited by 9 · see citing works
Self-citationSignaling pathways in phagocytosis
Kwiatkowska (1999) · doi:10.1002/(sici)1521-1878(199905)21:5
Self-citation
Flagged first, then by citations
2 of the 104 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
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Sorted by citations
Identifying bacterial genes and endosymbiont DNA with Glimmer
Delcher, A. L., Bratke, K. A., Powers, E. C., & Salzberg, S. L. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm009 · Cited by 3,141 · see citing works
“This similarity often breaks down near the 50 end of the transcript, which also tends to be the region where gene finders disagree on the precise position of the start codon.”
BackgroundWolbachia: master manipulators of invertebrate biology
Werren, J. H., Baldo, L., & Clark, M. E. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1969 · Cited by 2,830 · see citing works
A Wolbachia Symbiont in Aedes aegypti Limits Infection with Dengue, Chikungunya, and Plasmodium
Moreira, L. A., Iturbe‐Ormaetxe, I., Jeffery, J. A. L., Lu, G., Pyke, A. T., Hedges, L. M., Rocha, B. C., Hall‐Mendelin, S., Day, A., Riegler, M., et al. (2009) · Cell · doi:10.1016/j.cell.2009.11.042 · Cited by 1,734 · see citing works
“, 2005) and that Wolbachia and related bacteria also lack the biosynthetic capability to synthesize cholesterol and need to obtain it from the host insect (Lin and Rikihisa, 2003; Wu et al., 2004).”
BackgroundSelf-citationGenomics and evolution of heritable bacterial symbionts.
Moran, N., McCutcheon, J., & Nakabachi, A. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.41.110306.130119 · Cited by 1,662 · see citing works
The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations
Walker, T., Johnson, P. H., Moreira, L. A., Iturbe‐Ormaetxe, I., Frentiu, F. D., McMeniman, C. J., Leong, Y. S., Dong, Y., Axford, J. K., Kriesner, P., et al. (2011) · Nature · doi:10.1038/nature10355 · Cited by 1,374 · see citing works
Self-citationTeixeira, L., Ferreira, Á., & Ashburner, M. (2008) · PLoS Biology · doi:10.1371/journal.pbio.1000002 · Cited by 1,220 · see citing works
“Genes encoding proteins with ankyrin repeats, involved in protein–protein interactions, are over-represented in the Wolbachia genome [46,58] and are good candidates for mediators of anti-viral resistance.”
BackgroundMethodInfluentialThe Origin and Diversification of Mitochondria
Roger, A. J., Muñoz-Gómez, S. A., & Kamikawa, R. (2017) · Current Biology · doi:10.1016/j.cub.2017.09.015 · Cited by 1,142 · see citing works
Multilocus Sequence Typing System for the Endosymbiont Wolbachia pipientis
Baldo, L., Hotopp, J. C. D., Jolley, K. A., Bordenstein, S. R., Biber, S., Choudhury, R. R., Hayashi, C. Y., Maiden, M. C. J., Tettelin, H., & Werren, J. H. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.00731-06 · Cited by 872 · see citing works
“by on January 30, 2010 aem.asm.org Downloaded from nogaster ( 60 ), and wBm, a supergroup D strain from the nematode host Brugia malayi (9).”
BackgroundSelf-citationBiochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes
Müller, M., Mentel, M., van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., Yu, R.-Y., van der Giezen, M., Tielens, A. G. M., & Martin, W. F. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05024-11 · Cited by 838 · see citing works
Self-citationHuman and animal dirofilariasis: The emergence of a zoonotic mosaic
Simón, F., Siles-Lucas, M., Morchón, R., González-Miguel, J., Mellado, I., Carretón, E., & Montoya-Alonso, J. A. (2012) · Clinical Microbiology Reviews · doi:10.1128/cmr.00012-12 · Cited by 834 · see citing works
Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes
Hotopp, J. C. D., Clark, M. E., Oliveira, D. C. S. G., Foster, J. M., Fischer, P., Torres, M. C. M., Giebel, J. D., Kumar, N., Ishmael, N., Wang, S., et al. (2007) · Science · doi:10.1126/science.1142490 · Cited by 818 · see citing works
Self-citationGenomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world
Koonin, E. V., & Wolf, Y. I. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn668 · Cited by 793 · see citing works
“Well-characterized cases in point are Rickettsia (247,248), Wolbachia (249), pathogenic Mycobacteria (250,251) and some lactobacilli (252).”
BackgroundCazalet, C., Rusniok, C., Brüggemann, H., Zidane, N., Magnier, A., Ma, L., Tichit, M., Jarraud, S., Bouchier, C., Vandenesch, F., et al. (2004) · Nature Genetics · doi:10.1038/ng1447 · Cited by 656 · see citing works
“So far, the only prokaryotic genomes known to encode large families of ankyrin domain proteins are those of Coxiella burnetii and Wolbachia pipientis , which encode 13 and 23 members, respectivel”
BackgroundMarine sponges and their microbial symbionts: love and other relationships
Webster, N. S., & Taylor, M. W. (2011) · Environmental Microbiology · doi:10.1111/j.1462-2920.2011.02460.x · Cited by 644 · see citing works
“These results are consistent with observations of intracellular symbionts in other hosts (Wu et al., 2004).”
ResultMetagenomics: DNA sequencing of environmental samples
Green, S., & Rubin, E. M. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1709 · Cited by 634 · see citing works
The Wolbachia genome of Brugia malayi: Endosymbiont evolution within a human pathogenic \nnematode
Foster, J. M., Ganatra, M. B., Kamal, I. H., Ware, J., Makarova, K. S., Ivanova, N., Bhattacharyya, A., Kapatral, V., Kumar, S., Pósfai, J., et al. (2005) · eScholarship (California Digital Library) · Cited by 626 · see citing works
Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications
Valdés, J., Pedroso, I., Quatrini, R., Dodson, R. J., Tettelin, H., Blake, R. C., Eisen, J. A., & Holmes, D. S. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-597 · Cited by 612 · see citing works
“The genome was sequenced and assembled using the whole genome shotgun method as previously described [135-137].”
MethodSelf-citationCytonuclear coevolution: the genomics of cooperation
Rand, D. M., Haney, R. A., & Fry, A. J. (2004) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2004.10.003 · Cited by 594 · see citing works
“As a result of gene redundancy, much of the evolution of bacterial endosymbiont genomes is reductive gene loss [4, 11 ].”
BackgroundArchaea and the origin of eukaryotes
Eme, L., Spang, A., Lombard, J., Stairs, C. W., & Ettema, T. J. G. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.133 · Cited by 549 · see citing works
Duan, Y., Zhou, L., Hall, D. G., Li, W., Doddapaneni, H., Lin, H., Liu, L., Vahling, C. M., Gabriel, D. W., Williams, K. P., et al. (2009) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-22-8-1011 · Cited by 554 · see citing works
Learning how to live together: genomic insights into prokaryote–animal symbioses
Moyá, A., Peretó, J. G., Gil, R., & Latorre, A. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2319 · Cited by 551 · see citing works
Molecular Interactions between Bacterial Symbionts and Their Hosts
Dale, C., & Moran, N. A. (2006) · Cell · doi:10.1016/j.cell.2006.07.014 · Cited by 547 · see citing works
“They use a simple transposase to effect " cut and paste " excision and insertion of transposon DNA in the bacterial genome.”
BackgroundInfluentialBlanc, G., Duncan, G. A., Agarkova, I., Borodovsky, M. Y., Gurnon, J. R., Kuo, A., Lindquist, E., Lucas, S. M., Pangilinan, J. L., Polle, J. E. W., et al. (2010) · The Plant Cell · doi:10.1105/tpc.110.076406 · Cited by 504 · see citing works
Symbiosis as an adaptive process and source of phenotypic complexity
Moran, N. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611659104 · Cited by 500 · see citing works
Comparative Genomics of Emerging Human Ehrlichiosis Agents
Hotopp, J. C. D., Lin, M., Madupu, R., Crabtree, J., Angiuoli, S. V., Eisen, J. A., Seshadri, R., Ren, Q., Wu, M., Utterback, T. R., et al. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020021 · Cited by 489 · see citing works
“APH, Anaplasma phagocytophilum; AMA, Anaplasma marginale [23]; ECH, Ehrlichia chaffeensis; ERU, Ehrlichia ruminantium [24]; WOL,Wolbachia pipientis wMel [19]; NSE, Neorickettsia sennetsu; RPR, Rickettsia prowazekii [18];”
BackgroundInfluentialSelf-citationProphage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility
LePage, D. P., Metcalf, J. A., Bordenstein, S. R., On, J., Perlmutter, J. I., Shropshire, J. D., Layton, E. M., Funkhouser-Jones, L. J., Beckmann, J. F., & Bordenstein, S. R. (2017) · Nature · doi:10.1038/nature21391 · Cited by 467 · see citing works
“6] 31 , wRi [NC_012416.”
Metabolic Complementarity and Genomics of the Dual Bacterial Symbiosis of Sharpshooters
Wu, D., Daugherty, S. C., Aken, S. E. V., Pai, G., Watkins, K. L., Khouri, H. M., Tallon, L. J., Zaborsky, J., Dunbar, H. E., Tran, P. L., et al. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040188 · Cited by 443 · see citing works
“GC skew and nucleotide composition analysis were performed as described previously [23].”
BackgroundMethodSelf-citationEvolutionary microbial genomics: insights into bacterial host adaptation
Toft, C., & Andersson, S. G. E. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2798 · Cited by 424 · see citing works
“The maternally inherited Wolbachia species that use insects as hosts (discussed further below) have the genomic feature of 30–50 genes that encode eukaryotic-like ankyrin repeat proteins, some of which are presumably secreted into the host cel”
BackgroundWolbachia.Bacterial Endosymbionts of Filarial Nematodes
Taylor, M. J., Bandi, C., & Hoerauf, A. M. (2005) · Advances in Parasitology/Advances in parasitology · doi:10.1016/s0065-308x(05)60004-8 · Cited by 425 · see citing works
Gene drive systems for insect disease vectors
Sinkins, S. P., & Gould, F. L. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1870 · Cited by 423 · see citing works
Wolbachia and the biological control of mosquito‐borne disease
Iturbe‐Ormaetxe, I., Walker, T., & Neill, S. L. O. (2011) · EMBO Reports · doi:10.1038/embor.2011.84 · Cited by 419 · see citing works
Bai, X., Zhang, J., Ewing, A. D., Miller, S. A., Radek, A. J., Shevchenko, D., Tsukerman, K., Walunas, T. L., Lapidus, A. L., Campbell, J. W., et al. (2006) · OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) · doi:10.1128/jb.188.10.3682-3696.2006 · Cited by 415 · see citing works
The Genetics and Cell Biology of Wolbachia-Host Interactions
Serbus, L. R., Casper-Lindley, C., Landmann, F., & Sullivan, W. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.41.110306.130354 · Cited by 415 · see citing works
“The wMel genome contains 23 proteins with ankyrin repeats (Ank proteins) (155).”
BackgroundInfluentialWolbachia -induced cytoplasmic incompatibility as a means for insect pest population control
Zabalou, S., Riegler, M., Theodorakopoulou, M., Stauffer, C., Savakis, C., & Bourtzis, K. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403853101 · Cited by 411 · see citing works
Self-citationDarmon, E., & Leach, D. R. F. (2014) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00035-13 · Cited by 409 · see citing works
Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens
Silby, M. W., Cerdeño-Tárraga, A. M., Vernikos, G. S., Giddens, S. R., Jackson, R. W., Preston, G. M., Zhang, X., Moon, C. D., Gehrig, S. M., Godfrey, S. A. C., et al. (2009) · Genome biology · doi:10.1186/gb-2009-10-5-r51 · Cited by 400 · see citing works
“This can be associated with a recent change in niche, and the resulting evolutionary bottleneck [42,43], or with reduced selection because of small effective population size and absence of recombination [44].”
Beyond insecticides: new thinking on an ancient problem
McGraw, E. A., & O'Neill, S. L. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro2968 · Cited by 381 · see citing works
Self-citationSymbiont-mediated protection in insect hosts
Jeremy, B., & Johnson, K. N. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2009.05.005 · Cited by 374 · see citing works
Genomic Insights into Methanotrophy: The Complete Genome Sequence of Methylococcus capsulatus (Bath)
Ward, N. L., Larsen, Ø., Sakwa, J., Bruseth, L. J., Khouri, H. M., Durkin, A. S., Dimitrov, G. I., Jiang, L., Scanlan, D., Kang, K. H., et al. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020303 · Cited by 361 · see citing works
“Sequence alignments and phylogenetic trees were refined using the methods described previously (Salzberg et al. 2001; Wu et al. 2004).”
MethodSelf-citationGenomic changes following host restriction in bacteria
Moran, N. A., & Plague, G. R. (2004) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2004.09.003 · Cited by 352 · see citing works
Living in the endosymbiotic world of Wolbachia: A centennial review
Kaur, R., Shropshire, J. D., Cross, K. L., Leigh, B. A., Mansueto, A. J., Stewart, V., Bordenstein, S. R., & Bordenstein, S. R. (2021) · Cell Host & Microbe · doi:10.1016/j.chom.2021.03.006 · Cited by 359 · see citing works
Moran, N. A. (2006) · Current Biology · doi:10.1016/j.cub.2006.09.019 · Cited by 358 · see citing works
Wolbachia Stimulates Immune Gene Expression and Inhibits Plasmodium Development in Anopheles gambiae
Kambris, Z., Blagborough, A. M., Pinto, S. B., Blagrove, M. S. C., Godfray, H. C. J., Sinden, R. E., & Sinkins, S. P. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001143 · Cited by 342 · see citing works
“Primers were designed using Vectorbase (www.vectorbase.org) mosquito gene sequences/ orthology criteria, and the w Mel genome sequence [39], since w Mel and w MelPop are closely related [40].”
MethodMicrobial evolution and transitions along the parasite–mutualist continuum
Drew, G., Stevens, E. J., & King, K. C. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-021-00550-7 · Cited by 342 · see citing works
Nowack, E. C. M., Melkonian, M., & Glöckner, G. (2008) · Current Biology · doi:10.1016/j.cub.2008.02.051 · Cited by 329 · see citing works
“For Wolbachia pipientis wMel, an obligate intracellular bacterium of Drosophila melanogaster, it was shown that reductive genome evolution was not accompanied by intracellular gene transfer, but missing metabolic functions seem to be compensated at the metabolite level [32].”
BackgroundEsser, C. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh160 · Cited by 324 · see citing works
“…mitochondria among a-proteobacteria because a few genes have produced that phylogenetic result (Kurland and Andersson 2000; Emelyanov 2003), although the genome sequence of Wolbachia pipientis wMel recently revealed that Rickettsia is the sister of Wolbachia, not of mitochondria (Wu et al. 2004).”
BackgroundThe players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes
Moran, N. A., Degnan, P. H., Santos, S. R., Dunbar, H. E., & Ochman, H. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507029102 · Cited by 318 · see citing works
Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics
Donadio, S., Monciardini, P., & Sosio, M. (2007) · Natural Product Reports · doi:10.1039/b514050c · Cited by 307 · see citing works
Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis
Thomas, T., Rusch, D. B., DeMaere, M. Z., Yung, P. Y., Lewis, M., Halpern, A. L., Heidelberg, K. B., Egan, S., Steinberg, P. D., & Kjelleberg, S. J. (2010) · The ISME Journal · doi:10.1038/ismej.2010.74 · Cited by 306 · see citing works
“The abundance of AR proteins has been noted in the genomes of obligate and facultative intracellular symbionts of eukaryotic cells (Wu et al., 2004).”
BackgroundInfluentialChrostek, E., Marialva, M. S. P., Esteves, S. S., Weinert, L. A., Martinez, J., Jiggins, F. M., & Teixeira, L. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003896 · Cited by 305 · see citing works
“Predicted protein domain analysis was based on the reference genome [58] or using NCBI CD-search [124]).”
BackgroundMethodInfluentialMetabolic Interdependence of Obligate Intracellular Bacteria and Their Insect Hosts
Zientz, E., Dandekar, T., & Gross, R. (2004) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.68.4.745-770.2004 · Cited by 293 · see citing works
Wolbachia Infections in Aedes aegypti Differ Markedly in Their Response to Cyclical Heat Stress
Ross, P. A., Wiwatanaratanabutr, I., Axford, J. K., White, V. L., Endersby‐Harshman, N. M., & Hoffmann, A. A. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006006 · Cited by 273 · see citing works
Ogata, H., Renesto, P., Audic, S., Robert, C., Blanc, G., Fournier, P., Parrinello, H., Claverie, J., & Raoult, D. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030248 · Cited by 280 · see citing works
“[14] reported slightly different numbers of ankyrin-repeatcontaining proteins for these species.”
BackgroundWolbachia: more than just a bug in insects genitals
Saridaki, A., & Bourtzis, K. (2009) · Current Opinion in Microbiology · doi:10.1016/j.mib.2009.11.005 · Cited by 277 · see citing works
“Wolbachia genomics Since 2004, when the first genome of Drosophila melanogaster wMel was released [30], three other Wolbachia genomes have been completed [31–33] and a number of other sequencing projects are in progress (reviewed in [1 ]).”
BackgroundRickettsial evolution in the light of comparative genomics
Merhej, V., & Raoult, D. (2010) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2010.00151.x · Cited by 276 · see citing works
“Ank- and TPR-repeat proteins have been found in several intracellular bacteria where these are implicated in host–pathogen interactions (Caturegli et al., 2000; Cazalet et al., 2004; Felsheim et al., 2009; Seshadri et al., 2003; Wu et al., 2004).”
BackgroundThe Complete Genome Sequence of Haloferax volcanii DS2, a Model Archaeon
Hartman, A., Norais, C. A., Badger, J. H., Delmas, S., Haldenby, S. T., Madupu, R., Robinson, J. M., Khouri, H. M., Ren, Q., Lowe, T. M., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009605 · Cited by 277 · see citing works
“Non-coding RNAs were identified as described previously [149].”
BackgroundMethodSelf-citationde Felipe, K. S., Pampou, S., Jovanovic, O. S., Pericone, C. D., Ye, S. F., Kalachikov, S. M., & Shuman, H. A. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.22.7716-7726.2005 · Cited by 274 · see citing works
“Also, the parasitic endosymbiont Wolbachia pipientis contains several proteins with ankyrin repeats speculated to play a role in its intracellular lifestyle (26, 62 ).”
BackgroundWolbachia Induces Density-Dependent Inhibition to Dengue Virus in Mosquito Cells
Lü, P., Bian, G., Pan, X., & Xi, Z. (2012) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0001754 · Cited by 274 · see citing works
“The Type IV Secretion System, which presents within Wolbachia [35,36], was reported to secret different factors into host to mediate interactions between the other intracellular bacteria and their hosts [37].”
BackgroundDietary Cholesterol Modulates Pathogen Blocking by Wolbachia
Caragata, E. P., Rancès, E., Hedges, L. M., Gofton, A. W., Johnson, K. N., O’Neill, S. L., & McGraw, E. A. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003459 · Cited by 273 · see citing works
“Wolbachia is known have limited lipid biosynthesis capabilities and relies heavily on the host cell to meet this requirement [16].”
Self-citationPlasmids and Rickettsial Evolution: Insight from Rickettsia felis
Gillespie, J. J., Beier, M. S., Rahman, M. S., Ammerman, N. C., Shallom, J. M., Purkayastha, A., Sobral, B., & Azad, A. F. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000266 · Cited by 268 · see citing works
Brayton, K. A., Kappmeyer, L. S., Herndon, D. R., Dark, M. J., Tibbals, D. L., Palmer, G. H., McGuire, T. C., & Knowles, D. P. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406656102 · Cited by 267 · see citing works
Wu, M., Ren, Q., Durkin, A. S., Daugherty, S. C., Brinkac, L. M., Dodson, R. J., Madupu, R., Sullivan, S. A., Kolonay, J. F., Nelson, W. C., et al. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0010065 · Cited by 261 · see citing works
“Cloning, sequencing, assembly, and closure were performed as described [51,52].”
MethodSelf-citationA Robust Species Tree for the Alphaproteobacteria
Williams, K. P., Sobral, B., & Dickerman, A. W. (2007) · Journal of Bacteriology · doi:10.1128/jb.00269-07 · Cited by 255 · see citing works
Raychoudhury, R., Baldo, L., Oliveira, D. C. S. G., & Werren, J. H. (2008) · Evolution · doi:10.1111/j.1558-5646.2008.00533.x · Cited by 249 · see citing works
“…do not show such extreme genome features (less genome streamlining, relatively more repetitive elements including phage, and less AT bias, Wu et al. 2004), and have a mixture of vertical and horizontal transmission and evidence of recombination among strains (Werren and Bartos 2001,…”
BackgroundGenome Evolution of Wolbachia Strain wPip from the Culex pipiens Group
Klasson, L., Walker, T., Sebaihia, M., Sanders, M., Quail, M. A., Lord, A., Sanders, S., Earl, J., O’Neill, S. L., Thomson, N. R., et al. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn133 · Cited by 249 · see citing works
Self-citationEvidence for a Global Wolbachia Replacement in Drosophila melanogaster
Riegler, M., Sidhu, M. S., Miller, W. J., & O’Neill, S. L. (2005) · Current Biology · doi:10.1016/j.cub.2005.06.069 · Cited by 246 · see citing works
Self-citationThe mosaic genome structure of the Wolbachia w Ri strain infecting Drosophila simulans
Klasson, L., Westberg, J., Sapountzis, P., Näslund, K., Lutnaes, Y., Darby, A. C., Veneti, Z., Chen, L., Braig, H. R., Garrett, R. A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810753106 · Cited by 243 · see citing works
“These genomes have a large repertoire of genes with ankyrin repeat motifs, 23 in wMel and 60 in wPip, several of which are associated with mobile elements (6, 7).”
BackgroundDegnan, P. H., Yu, Y., Sisneros, N., Wing, R. A., & Moran, N. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900194106 · Cited by 241 · see citing works
“defensa genome is similar to Wolbachia genomes, which are small, have highly reduced biosynthetic capabilities, and encode an abundance of mobile genetic elements (3, 5).”
BackgroundCho, N., Kim, H., Lee, J., Kim, S.-Y., Kim, J., Cha, S., Kim, S.-Y., Darby, A. C., Fuxelius, H., Yin, J., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611553104 · Cited by 238 · see citing works
Community genomics in microbial ecology and evolution
Allen, E. E., & Banfield, J. F. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1157 · Cited by 234 · see citing works
Pop, M. (2004) · Briefings in Bioinformatics · doi:10.1093/bib/5.3.237 · Cited by 232 · see citing works
“An example is shown in Another challenge is caused by short repeats that often flank polymorphisms (see, for example, Wu et al. 17 ).”
BackgroundMiller, W. J., Ehrman, L., & Schneider, D. I. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001214 · Cited by 227 · see citing works
“Diagnostic Wolbachia PCR, Cloning and Sequencing wPau Wolbachia was detected using primer specifically targeting the wsp locus, the transposon IS5 as well as VNTR-105 and VNTR141 locus. wsp-primer sets were taken from [52] and primers for VNTRs and IS5 PCR were taken from [57].”
MethodInfluentialDiverse Phage-Encoded Toxins in a Protective Insect Endosymbiont
Degnan, P. H., & Moran, N. A. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.01285-08 · Cited by 227 · see citing works
Nakabachi, A., Shigenobu, S., Sakazume, N., Shiraki, T., Hayashizaki, Y., Carninci, P., Ishikawa, H., Kudo, T., & Fukatsu, T. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409034102 · Cited by 226 · see citing works
Widespread Recombination Throughout Wolbachia Genomes
Baldo, L., Bordenstein, S. R., Wernegreen, J. J., & Werren, J. H. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj049 · Cited by 222 · see citing works
“Based on the wMel annotation (Wu et al. 2004), the complementary strand of this region is noncoding, thus excluding a pressure for conservation at the complementary strand.”
BackgroundInfluentialTaxonomic status of the intracellular bacterium Wolbachia pipientis
Lo, N. C., Paraskevopoulos, C., Bourtzis, K., O’Neill, S. L., Werren, J. H., Bordenstein, S. R., & Bandi, C. (2007) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.64515-0 · Cited by 221 · see citing works
“Genome sequencing studies show that W. pipientis has the genetic machinery for gene transfer (Wu et al., 2004) and a number of arthropods have been shown to be infected by both A and B representatives (Werren et al., 1995; Werren & Windsor, 2000), which would provide a means of gene flow.”
BackgroundSelf-citationFunctional diversity of ankyrin repeats in microbial proteins
Khodor, S. A., Price, C. T. D., Kalia, A., & Kwaik, Y. A. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2009.11.004 · Cited by 219 · see citing works
Polydnavirus genomes reflect their dual roles as mutualists and pathogens
Webb, B. A., Strand, M. R., Dickey, S. E., Beck, M. H., Hilgarth, R., Barney, W. E., Kadash, K., Kroemer, J. A., Lindstrom, K. G., Rattanadechakul, W., et al. (2005) · Virology · doi:10.1016/j.virol.2005.11.010 · Cited by 215 · see citing works
Heritable Endosymbionts of Drosophila
Mateos, M., Castrezana, S., Nankivell, B., Estes, A. M., Markow, T. A., & Moran, N. A. (2006) · Genetics · doi:10.1534/genetics.106.058818 · Cited by 215 · see citing works
“Screening with the 559F–35R universal primer set, which spans the intergenic spacer of the rRNA operon and thus excludes Wolbachia, which lacks an intact operon (Wu et al. 2004), revealed the presence of proteobacterial sequences in several ovary extracts.”
BackgroundMethodInfluentialThe rich somatic life of Wolbachia
Pietri, J. E., DeBruhl, H., & Sullivan, W. (2016) · MicrobiologyOpen · doi:10.1002/mbo3.390 · Cited by 215 · see citing works
“Sequence analysis reveals the Wolbachia genome contains several outer membrane proteins (WSPs, Wolbachia surface proteins) and these are likely to play a role in interacting with host cytoskeleton (Wu et al., 2004).”
BackgroundInfluentialImportance of widespread gene transfer agent genes in α-proteobacteria
Lang, A. S., & Beatty, J. T. (2006) · Trends in Microbiology · doi:10.1016/j.tim.2006.12.001 · Cited by 213 · see citing works
Anaplasma phagocytophilum and Ehrlichia chaffeensis: subversive manipulators of host cells
Rikihisa, Y. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2318 · Cited by 213 · see citing works
“By contrast, only a few omp1–p44 genes are found in the closely related genera Neorickettsia and Wolbachia”
BackgroundIntracellular pathogens go extreme: genome evolution in the Rickettsiales
Darby, A. C., Cho, N.-H., Fuxelius, H., Westberg, J., & Andersson, S. G. E. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.08.002 · Cited by 212 · see citing works
Bordenstein, S. R. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh211 · Cited by 199 · see citing works
The evolution of chronic infection strategies in the α-proteobacteria
Batut, J., Andersson, S. G. E., & O’Callaghan, D. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro1044 · Cited by 207 · see citing works
Wolbachia Infection Reduces Blood-Feeding Success in the Dengue Fever Mosquito, Aedes aegypti
Turley, A. P., Moreira, L. A., O’Neill, S. L., & McGraw, E. A. (2009) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0000516 · Cited by 207 · see citing works
“biosynthesis [15,16].”
Self-citationNikoh, N., Tanaka, K., Shibata, F., Kondo, N. I., Hizume, M., Shimada, M., & Fukatsu, T. (2007) · Genome Research · doi:10.1101/gr.7144908 · Cited by 202 · see citing works
“Exhaustive PCR detection of Wolbachia genes in the insect genome We designed 222 pairs of PCR primers for specific amplification of 222 Wolbachia genes that cover the whole genome of wMel, consisting of 1195 open reading frames (ORFs) (Wu et al. 2004).”
BackgroundMethodInfluentialComputational inference of scenarios for α-proteobacterial genome evolution
Boussau, B., Karlberg, E. O., Frank, A. C., Legault, B.-A., & Andersson, S. G. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400975101 · Cited by 199 · see citing works
Massive Genomic Decay in Serratia symbiotica, a Recently Evolved Symbiont of Aphids
Burke, G., & Moran, N. (2011) · Genome Biology and Evolution · doi:10.1093/gbe/evr002 · Cited by 201 · see citing works
“Key words: Serratia symbiotica, genome reduction, pseudogene, recent symbiont.”
BackgroundKiraga, J., Mackiewicz, P., Mackiewicz, D., Kowalczuk, M., Biecek, P., Polak, N., Smolarczyk, K., Dudek, M. R., & Cebrat, S. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-163 · Cited by 194 · see citing works
“It has been suggested that the higher rate of evolution results from enhanced mutation rate [36] and/or Muller's ratchet effect or the easier fixation of mutations by genetic drift in small asexual populations [37-46].”
BackgroundRos, V. I. D., Fleming, V. M., Feil, E. J., & Breeuwer, J. A. J. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.01109-08 · Cited by 194 · see citing works
“groEL was amplified using the primers groEL-F (5-CAACRGTRGSRRYAACTGCDGG-3) and groEL-R (5-GATADCCRCGRTCAAAYTGC-3), hand designed from available Wolbachia and Rickettsia genome sequences (2, 37, 62 ) and tested on isolates representative of supergroups A and B (samples kindly donated by Robert Butcher, University of Ba…”
MethodDarby, A. C., Armstrong, S. D., Bah, G. S., Kaur, G., HUGHES, M. A., Kay, S., Koldkjær, P., Rainbow, L., Radford, A. D., Blaxter, M., et al. (2012) · Genome Research · doi:10.1101/gr.138420.112 · Cited by 194 · see citing works
“To date, four Wolbachia genomes have been completed: two from group A (wMel, 1.3 Mb [Wu et al. 2004], and wRi, 1.5 Mb [Klasson et al. 2009] from Drosophila melanogaster and Drosophila simulans, respectively), one from group B (wPip, 1.5 Mb [Klasson et al. 2008] from the mosquito Culex pipiens), and…”
InfluentialMosaic Nature of theWolbachiaSurface Protein
Baldo, L., Lo, N. C., & Werren, J. H. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.15.5406-5418.2005 · Cited by 193 · see citing works
“As recently reported, the complete genome of wMel encodes the necessary apparatus for recombination, including RecA, and shows unusual features likely to be derived from frequent intragenomic recombination and lateral DNA transfers ( 67 ).”
BackgroundRevisiting horizontal transfer of transposable elements in Drosophila
Loreto, É. L. S., Carareto, C. M. A., & Capy, P. (2008) · Heredity · doi:10.1038/sj.hdy.6801094 · Cited by 192 · see citing works
Mobile DNA in obligate intracellular bacteria
Bordenstein, S. R., & Reznikoff, W. S. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1233 · Cited by 192 · see citing works
“Of particular interest are three intact RT genes that contain MATURASE DOMAINS (WD0693, WD0995 and WD1138”
Wolbachia Interferes with Ferritin Expression and Iron Metabolism in Insects
Kremer, N., Voronin, D., Charif, D., Mavingui, P., Mollereau, B., & Vavre, F. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000630 · Cited by 191 · see citing works
“suggested, since almost all the genes necessary for heme biosynthesis and also bacterioferritin, are retained by the Wolbachia infecting the nematode Brugia malayi [20], Drosophila melanogaster [37] and Culex quinquefasciatus [39].”
BackgroundPopulation Genomics of the Wolbachia Endosymbiont in Drosophila melanogaster
Richardson, M. F., Weinert, L. A., Welch, J. J., Linheiro, R. S., Magwire, M. M., Jiggins, F. M., & Bergman, C. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003129 · Cited by 191 · see citing works
“melanogaster (wMel) was the first Wolbachia strain to have its genome fully sequenced [28].”
BackgroundThe importance of culturing bacterioplankton in the 'omics' age
Giovannoni, S. J., & Stingl, U. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1752 · Cited by 187 · see citing works
“gov/sites/entrez?db=genomeprj&Cmd=search&term=Wolbachia pipientis"> Wolbachia pipientis”
Geoghegan, V., Stainton, K., Rainey, S. M., Ant, T. H., Dowle, A., Larson, T. R., Hester, S., Charles, P. D., Thomas, B., & Sinkins, S. P. (2017) · Nature Communications · doi:10.1038/s41467-017-00610-8 · Cited by 184 · see citing works
Nakayama, K., Yamashita, A., Kurokawa, K., Morimoto, T., Ogawa, M., Fukuhara, M., Urakami, H., Ohnishi, M., Uchiyama, I., Ogura, Y., et al. (2008) · DNA Research · doi:10.1093/dnares/dsn011 · Cited by 182 · see citing works
- Authors
- Wu, M., Sun, L. V., Vamathevan, J., Riegler, M., Deboy, R., Brownlie, J. C., McGraw, E. A., Martin, W., Esser, C., Ahmadinejad, N., Wiegand, C., Madupu, R., Beanan, M. J., Brinkac, L. M., Daugherty, S. C., Durkin, A. S., Kolonay, J. F., Nelson, W. C., Mohamoud, Y., Lee, P., Berry, K., Young, M. B., Utterback, T., Weidman, J., Nierman, W. C., Paulsen, I. T., Nelson, K. E., Tettelin, H., O'Neill, S. L., & Eisen, J. A.
- Affiliations
- J. Craig Venter Institute (US)
- Yale University (US)
- The University of Queensland (AU)
- Heinrich Heine University Düsseldorf (DE)
- Corresponding author
- Eisen, Jonathan A
- ORCID
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2004-03-16
- Volume
- 2
- Issue
- 3
- Pages
- e69
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC368164
- OpenAlex
- W2038357425
- Cited by
- 851
- References
- 104
- Citations by year
- 2026: 12 · 2025: 26 · 2024: 15 · 2023: 29 · 2022: 25 · 2021: 45 · 2020: 32 · 2019: 42 · 2018: 34 · 2017: 34 · 2016: 35 · 2015: 35 · 2014: 43 · 2013: 44 · 2012: 41
- FWCI
- 71.82
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Figshare (submittedVersion, cc-by)
- Griffith Research Online (submittedVersion, cc-by)
- Funders
- National Institutes of Health (1u01ai047409-01)
- National Institute of Allergy and Infectious Diseases (UO1-AI47409-01)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- Wolbachia, Drosophila melanogaster, genome sequence, mobile genetic elements, repetitive DNA, genome streamlining, intracellular bacteria, reproductive parasitism, symbiosis, Rickettsia, glycolysis, purine biosynthesis, lipopolysaccharide biosynthesis, ankyrin repeat domain, horizontal gene transfer, mitochondrial origin, Alphaproteobacteria, population bottleneck, natural selection
- MeSH terms
- Adenosine Triphosphate, Animals, DNA, Drosophila melanogaster, Genes, Bacterial, Glycolysis, Models, Genetic, Molecular Sequence Data, Parasites, Phylogeny, Purines, Gene Library, Polymerase Chain Reaction, Open Reading Frames, Genome, Genome, Bacterial, Gene Deletion, Protein Structure, Tertiary, DNA Primers, Cell Lineage, Evolution, Molecular, Interspersed Repetitive Sequences, Gene Duplication, Wolbachia, Genomics
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