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1 Department of Vegetable Crops, Agricultural Research Organization, Newe Ya'ar Research Center, Ramat Yishay, 30095, Israel
2 Department of Entomology, 410 Forbes Building, University of Arizona, Tucson, AZ 85721, USA
Correspondence
Einat Zchori-Fein
einat{at}volcani.agri.gov.il
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Published online ahead of print on 9 January 2004 as DOI 10.1099/ijs.0.02957-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA and gyrB gene sequences of ‘Candidatus Cardinium hertigii’ are AY331187 and AY332003, respectively.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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; Aksoy, 2000; Dolan, 2001; Moran et al., 2003). Whilst a few of these symbionts are reasonably well-characterized (Moran & Telang, 1998; Stouthamer et al., 1999), many others are undescribed and little is known about their influence on the phenotype of their hosts.
Bacterial symbionts that are transmitted strictly vertically from mother to offspring will increase in frequency if they directly enhance the fitness of their hosts or if they manipulate the reproduction of their hosts in ways that enhance their own transmission (Bull, 1983). The former include symbionts that supply nutrients that are missing from the host diet (Grenier et al., 1994; Douglas, 1998), increase heat tolerance (Montllor et al., 2002) or provide resistance to parasitoid wasps (Oliver et al., 2003). The latter type, of which the 
-group proteobacterium Wolbachia is the best-known example, has been shown to induce diverse reproductive alterations, such as: (i) cytoplasmic incompatibility, in which uninfected female hosts produce few or no offspring when mated with infected males; (ii) parthenogenesis induction, in which haploid host eggs are converted into viable diploid female offspring; (iii) feminization, in which genetic male hosts are converted into females; and (iv) male-killing, in which male hosts are killed during development (Stouthamer et al., 1999). Recently, a novel lineage of bacteria has been shown to be associated with several reproductive disorders, including parthenogenesis in a number of parasitoid wasps in the genus Encarsia (Zchori-Fein et al., 2001), feminization in the mite Brevipalpus phoenicis (Weeks et al., 2001) and cytoplasmic incompatibility in the wasp Encarsia pergandiella (Hunter et al., 2003). Phylogenetic analysis of the 16S rRNA gene placed these bacteria in the ‘Bacteroidetes’ group (=Cytophaga–Flexibacter–Bacteroides or CFB group) (Zchori-Fein et al., 2001), with ‘Candidatus Amoebophilus asiaticus’, an intracellular bacterium of acanthamoebae (Horn et al., 2001), as their closest described relative (88 % similarity). This symbiont has provisionally been called the Encarsia bacterium (Zchori-Fein et al., 2001), the CFB-BP (BP for B. phoenicis) (Weeks & Breeuwer, 2003) and the Cytophaga-like organism (Hunter et al., 2003; Weeks et al., 2003).
In this study, we characterize and describe this symbiont lineage by phylogenetic analyses of full-length 16S rDNA and gyrB sequences and electron microscopic observations of bacterial structure. Furthermore, we present evidence that the symbiont is the causal agent of parthenogenesis in Encarsia hispida.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). European E. hispida is also parthenogenetic and infected with the symbiont and has been shown to produce males after antibiotic treatment (Hunter, 1999; Giorgini, 2001). All Encarsia species were reared in the laboratory at the University of Arizona on the sweet potato whitefly, B. tabaci, on cowpea (Vigna unguiculata) under fluorescent and natural light at approximately 25 °C with a photoperiod of 14 h light : 10 h dark.
Electron microscopy.
Ovaries from adult, sexual E. pergandiella and E. hispida were fixed in 4 % glutaraldehyde in 0·1 M cacodylate buffer, pH 7·3, for 1 h. They were then embedded in 2 % agarose in 0·1 M cacodylate buffer, returned to the 4 % glutaraldehyde fixative and held overnight. Following post-fixation for 2 h in 2 % osmium tetroxide, specimens were washed and stained en bloc in 2 % uranyl acetate for 90 min. Subsequently, specimens were dehydrated serially in ethanol (50, 70, 95 and 100 %), transferred to propylene oxide and embedded in Epon. Thin sections were stained with saturated uranyl acetate, followed by Reynolds lead citrate, and examined with a JEOL 100CX II transmission electron microscope. Length and width of 139 bacteria from both host species were measured and recorded.
DNA amplification and sequencing.
In order to obtain protein-encoding DNA sequences for further characterization and evolutionary studies of the Encarsia symbionts, partial sequences of the gene that encodes gyrase B (gyrB) were determined. A series of ‘universal’ primers for this highly conserved, informational gene has been developed (Yamamoto & Harayama, 1995) and, in conjunction with 16S rDNA, this gene has been found to be a useful marker of bacterial diversity (Huang, 1996).
Wasp host and bacterial symbiont DNA was extracted by using a Qiagen DNeasy tissue extraction kit (protocol for animal tissues). A fragment of the gyrB gene from the asexual population of E. pergandiella was PCR-amplified by using the conserved universal gyrB primers UP-1 (5'-GAAGTCATCATGACCGTTCTGCAYGCNGGNGGNAARTTYGA-3') and UP-2r (5'-AGCAGGGTACGGATGTGCGAGCCRTCNACRTCNGCRTCNGTCTA-3'), designed by Yamamoto & Harayama (1995). PCR conditions were as recommended in the Identification and Classification of Bacteria (ICB) database (http://seasquirt.mbio.co.jp/icb); a MasterTaq kit (Eppendorf) was used. The PCR product was cloned into Escherichia coli by using a pGEM-T Easy plasmid (Promega) according to the manufacturer's protocol; three different clones were sequenced both ways by an automatic sequencer (ABI 3700 DNA analyser; Macrogen). In order to obtain gyrB sequences for the symbionts from E. hispida and from the sexual population of E. pergandiella, the universal gyrB primers UP-1 and 2Tr-SR1 (5'-CCATAGCTGCGTAGCATTCATYTCNCCNARNCCYTT-3') were used (http://seasquirt.mbio.co.jp/icb/). PCR conditions were as described above, except that the annealing temperature was 52 °C. This PCR product was then used as a template in a second PCR, using the internal sequencing primers gyr125F (5'-CCGTATACCGAAACGGAA-3') and gyr1023R (5'-TTAGCAGTACCACCAGCA-3'), which were designed to amplify a 900 bp fragment of the gyrB gene.
In order to determine whether there were any other symbionts in E. hispida, the 16S rRNA gene was PCR-amplified by using the universal primers 27F (5'-AGAGTTTGATCMTGGCTCAG-3' and 1513R (5'-ACGGYTACCTTGTTACGACTT-3' (Weisburg et al., 1991) from an extract of multiple E. hispida wasps. This single PCR product was cloned and 33 clones were sequenced, using methods described previously (Hunter et al., 2003).
Phylogenetic analysis of the Encarsia symbionts using 16S rDNA and gyrB.
In order to understand the relationships of the bacterial symbionts of Encarsia within the ‘Bacteroidetes’ group, we constructed a phylogenetic tree by using full-length 16S rDNA sequences. We used full-length sequences from the bacterial symbionts of both the asexual and sexual populations of E. pergandiella, from E. hispida (obtained in this study) and from the arthropods B. phoenicis and Ixodes scapularis. In addition, we used sequences from a diverse assemblage of ‘Bacteroidetes’ bacteria, representing all major divisions in this group. Finally, Chlorobium limicola was used as an outgroup.
Sequences were first aligned in CLUSTAL W (Thompson et al., 1994) by using default settings and then aligned manually in MacClade 4.0.1 (Maddison & Maddison, 2001). A small number of internal sequences (three regions that were <20 bp and two that were <40 bp) that were difficult to align were removed. PAUP* 4.0b6 (Swofford, 2001) was used for all phylogenetic analyses. Under maximum-parsimony (MP), heuristic searches with TBR (tree bisection–reconnection) branch-swapping and 100 random-addition replicates were performed, with Maxtrees set to increase without limit. All characters were weighted equally. Clade robustness was assessed by bootstrap analysis (Felsenstein, 1985), using heuristic searches with 1000 replicates and a random-addition sequence with n=1. Distance methods to reconstruct the 16S rDNA phylogeny were also applied, using both the HKY85 model of DNA evolution and a general time-reversible model of nucleotide substitution, with rate heterogeneity between sites (GTR+
+I). We used neighbour-joining (NJ) trees to estimate the six nucleotide transition parameters, the gamma shape parameter for rate heterogeneity () and the proportion of invariable sites (I). We performed heuristic distance searches with TBR branch-swapping. We also performed a bootstrap analysis, using heuristic searches with 1000 replicates under the HKY85 model.
In addition, we constructed a phylogenetic tree of gyrB sequences that represented diverse ‘Bacteroidetes’ taxa, with Flavobacterium ferrugineum and Chitinophaga pinensis as outgroups. Phylogenetic analysis was done as described above for 16S rDNA, except that no internal sequences were removed. In addition to MP and distance analyses, we also performed a maximum-likelihood (ML) analysis, using the GTR++I model of nucleotide substitution with parameters estimated from NJ and MP trees. Under ML, we performed a heuristic search, using TBR branch-swapping, a starting tree obtained by neighbour-joining and the ‘asis' stepwise-addition option.
Finally, we identified signature 16S rDNA sequences for the symbiont lineage. Nucleotide alignments were first scanned in MacClade, after which candidate sequences were checked in the Ribosomal Database Project (RDP II) (http://rdp.cme.msu.edu/html/) (Cole et al., 2003) by using probe match and were also BLAST-searched for short, nearly exact matches in GenBank.
Parthenogenesis induction in E. hispida by the ‘Bacteroidetes’ symbiont.
E. hispida females, less than 48 h old, were held in vials for 48 h with honey only, or 50 mg rifampicin ml–1 in honey. Females were then placed individually into 35 mm Petri dish arenas, where a leaf disc bearing 20 third- to early fourth-instar B. tabaci whitefly nymphs was embedded in agar [for details, see Hunter et al. (2003)]. After 4 h, females were removed and the dishes were incubated at 27 °C, 65 % relative humidity, until pupation of the wasp progeny. Pupae were then removed and isolated in 1·2 ml glass vials until adult emergence. Adults were sexed, then killed in alcohol and stored until a PCR assay of infection status was conducted. Extraction and PCR methods were as described previously (Hunter et al., 2003).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Bacteria were located in the cytoplasm of all host ovarian cells examined, including nurse cells, follicle cells and oocytes of E. hispida and sexual and asexual E. pergandiella ovaries. These bacteria were morphologically indistinguishable from bacteria observed in the ovaries of the asexual E. pergandiella, as described previously (Zchori-Fein et al., 2001). The bacteria appeared to vary greatly in size (range of lengths, 0·42–2·35 µm, n=139; range of widths, 0·31–0·66 µm, n=139). As serial sections were not examined, it was not possible to distinguish cross-sections of elongated individuals from spherical forms. The lack of serial sections also prevented us from establishing the mean dimensions of the bacterium.
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), a few issue from one end of the cell (Fig. 1c) and, in one bacterium, the MLSs are attached to two opposing sides, merging in the centre (Fig. 1b). MLSs could not be observed in all bacterial cells, although it is not clear whether cells are polymorphic or some MLSs were not detected because they were in a different plane.
MLSs have previously been observed only in several symbiotic bacteria of invertebrates, such as symbionts of the sweet potato whitefly, B. tabaci (Costa et al., 1995), the predatory mite Metaseiulus occidentalis (Hess & Hoy, 1982), the soybean cyst nematode, Heterodera glycines (Endo, 1979), the leafhopper Helochara communis (Chang & Musgrave, 1972) and a symbiont of the tick I. scapularis (Kurtti et al., 1996). In two of these host taxa, B. tabaci and M. occidentalis, a PCR product was amplified by using primers that were specific to the 16S rDNA of the novel symbiont lineage (Weeks & Breeuwer, 2003), and in a third, I. scapularis, the 16S rDNA GenBank sequence places it within the group. As yet, investigations of all symbionts with MLSs have yielded evidence that they are members of the novel symbiont lineage. It is at least possible, therefore, that the MLSs are not only characteristic, but distinguish this bacterium. Interestingly, the description of the sister lineage, ‘Candidatus A. asiaticus’, does not mention or show the presence of similar structures. The function of the MLSs remains unknown.
Sequence and phylogenetic analysis
16S rDNA.
We generated 1487 bp of the E. hispida symbiont 16S rRNA gene sequence (G+C content, 48 mol%). This sequence is 99 % similar to the sequence determined for symbionts in asexual and sexual E. pergandiella, 97 % similar to those of the Brevipalpus and Ixodes symbionts and 88 % similar to the sequence of the Acanthamoeba symbiont ‘Candidatus A. asiaticus’. Our aligned dataset was 1215–1221 bp long, except for the GenBank sequences of Blattabacterium sp. (1121 bp), Cytophaga aurantiaca (1163 bp) and Flammeovirga aprica (1170 bp). MP and distance analyses produced similar tree topologies (Fig. 2) and none of the nodes that differed in trees obtained by the different methods showed >50 % bootstrap support. MP analysis produced two most parsimonious trees (tree length, 3472; confidence interval, 0·30; 478 parsimony-informative characters out of a total of 1221 characters). Under ML and by using an NJ tree, the following nucleotide substitution parameters were estimated (nucleotide transition parameters): A–C, 0·81; A–G, 2·57; A–T, 1·65; C–G, 0·67; C–T, 3·69; and G–T, 1·00. The proportion of invariant sites was estimated to be 0·38 and the shape parameter of the gamma-distribution was estimated to be 0·63. The Encarsia symbionts form a monophyletic group with ‘Candidatus A. asiaticus' and the symbionts from Brevipalpus and Ixodes. This symbiont lineage is aligned with bacteria from the C. aurantiaca group, such as ‘Microscilla sericea’ and ‘Microscilla furvescens’ (Fig. 2).
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gyrB.
We generated a 1283 bp gyrB gene sequence from the asexual E. pergandiella symbiont (G+C content, 38 mol%), 924 bp from the sexual E. pergandiella symbiont (40 mol%) and 858 bp from the E. hispida symbiont (40 mol%). The symbionts from the two populations of E. pergandiella are 98 % similar and both are 95 % similar to the E. hispida symbiont. Our aligned dataset was 924–936 bp long, except for the E. hispida symbiont sequence. As in the 16S rDNA analysis, MP, ML and distance analyses produced similar tree topologies (Fig. 3) and none of the nodes that differed in trees obtained by the three methods showed >50 % bootstrap support. MP analysis produced three most parsimonious trees (tree length, 4854; confidence interval, 0·31; 618 parsimony-informative characters out of a total of 942 characters). Under ML and by using an NJ tree, the following parameters of nucleotide substitution were estimated (nucleotide transition parameters): A–C, 2·71; A–G, 3·84; A–T, 2·13; C–G, 2·23; C–T, 8·01; and G–T, 1·00. The proportion of invariant sites was estimated to be 0·25 and the shape parameter of the gamma-distribution was estimated to be 1·08.
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). There are currently no available gyrB sequences for the ‘Bacteroidetes’ symbionts of Acanthamoeba, Brevipalpus or Ixodes.
Parthenogenesis induction in E. hispida by the ‘Bacteroidetes’ symbiont
Here, we provide additional evidence that parthenogenesis in E. hispida is caused by the ‘Bacteroidetes’ symbiont. The attribution of effects on hosts to particular unculturable symbionts has necessarily been indirect. Stouthamer et al. (1999) suggested three types of evidence, ranked by increasing levels of stringency, that have been used to associate a phenotype with a particular symbiont. They are: (i) an association between phenotype and infection; (ii) antibiotic treatment stops the expression of the phenotype and cures the infection; (iii) artificial inoculation from an infected to an uninfected host causes an infection and the phenotype in the new host. Zchori-Fein et al. (2001) established an association between the Encarsia symbiont and parthenogenesis induction in Encarsia and, in E. hispida, antibiotic treatment has been shown to cause male production in a European population (Hunter, 1999; Giorgini, 2001). Here, we examined the population of E. hispida from California in more detail. We found that whilst untreated females produced only daughters, antibiotic treatment of E. hispida females caused them to produce only sons. Antibiotic-treated females produced 0·9±0·31 males (mean±SE, n=10), whereas untreated females produced 2·9±0·31 females (mean±SE, n=10). PCR assays of these offspring showed that daughters of infected females were infected, but the sons of treated females were uninfected. We also extended the criteria of Stouthamer et al. (1999) to better exclude the possibility that other symbionts within a host could be responsible for the phenotype observed. Sequencing of 33 16S rDNA bacterial clones from E. hispida yielded 33 identical products of 1487 bp, with 99 % sequence identity to the symbiont of parthenogenetic E. pergandiella (GenBank accession no. AF319783). These lines of evidence suggest strongly that the symbiont described here is the causal agent of parthenogenesis in E. hispida. Interestingly, the picture is somewhat less clear in other infected parthenogenetic Encarsia spp. For example, E. pergandiella females treated with antibiotics produced almost no offspring and no males, possibly as a result of accumulation of deleterious mutations in male function (Zchori-Fein et al., 2001).
Proposal of ‘Candidatus Cardinium hertigii’
In this paper, we describe a novel bacterial genus based on sequences of the gyrB and 16S rRNA genes, as well as electron microscopy observations. Results of both the gyrB- and the 16S rDNA-based phylogenies are broadly similar and suggest that the newly discovered symbiont lineage is allied with the C. aurantiaca group. 16S rDNA analysis shows the recently described ‘Candidatus A. asiaticus’, a symbiont of Acanthamoeba sp., to be the closest relative of the novel symbiont lineage, with 88 % sequence homology to the symbiont of E. pergandiella. As 95 % similarity of the 16S rRNA gene has been suggested as the limit under which bacteria genera are distinguished (Ludwig et al., 1998), the symbionts of Encarsia, as well as the symbionts found in I. scapularis and B. phoenicis, both with 97 % sequence similarity to the Encarsia symbiont, should all be included in a novel bacterial genus.
In accordance with the recommendations of the International Committee on Systematic Bacteriology, unculturable prokaryotic symbionts that cannot be characterized by using the International Code of Nomenclature of Bacteria should be regarded as Candidatus (Murray & Stackebrandt, 1995). We therefore propose to name the bacterium associated with species of the parasitoid wasp Encarsia as ‘Candidatus Cardinium’. The genus name (Car.di'ni.um. N.L. n. Cardinium) is derived from cardo (gen. cardinis), the main axis of a Roman town, typically flanked by columns. The name pertains to the brush-like structure of MLSs observed within the bacteria. ‘Candidatus Cardinium’ belongs to the phylum ‘Bacteroidetes’ of bacteria, to the class ‘Sphingobacteria’, to the order ‘Sphingobacteriales’ and to the family ‘Flexibacteraceae’ (Garrity & Holt, 2001) and is a Gram-negative, rod-shaped bacterium. ‘Candidatus Cardinium’ is a transovarially transmitted, intracellular symbiont of eukaryotes. The genus is assigned based on the 16S rRNA gene sequence (GenBank accession no. AY331187), the gyrB gene sequence (accession no. AY332003) and the array of MLSs that are observed with an electron microscope.
At the time of writing, ‘Candidatus Cardinium’ contains a single species, ‘Candidatus Cardinium hertigii’. The specific epithet (her.ti'gi.i. N.L. gen. masc. n. hertigii) refers to Marshall Hertig, the microbiologist who described Wolbachia (Hertig, 1936). The bacterium found in the parthenogenetic population of the parasitic wasp E. hispida from San Diego, California, is proposed as the type strain. The G+C content of 1487 bp of ‘Candidatus C. hertigii’ 16S rDNA is 48 mol%, with the signature sequence 5'-GTATTTTGCTACTTTG-3'. The level of 16S rDNA sequence similarity between the I. scapularis and B. phoenicis symbionts and the Encarsia symbionts (97 %) places them all within the genus ‘Candidatus Cardinium’, but this amount of sequence divergence between the taxa suggests that the tick and mite symbionts belong to a different, as yet undescribed species (Stackebrandt & Goebel, 1994).
In the brief period since its discovery, ‘Candidatus Cardinium’ has been associated with diverse effects on its arthropod hosts. Surveys of its distribution suggest that it may infect 6–7 % of arthropods and be found most commonly in the Hymenoptera, Hemiptera and Acari (Weeks et al., 2003). Whilst not as common as the same authors' estimates of Wolbachia frequency (22–24 %), these estimates nonetheless suggest that this symbiont may be found in thousands of arthropod species and has only begun to be explored.
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ACKNOWLEDGEMENTS |
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S. Schmitz-Esser, E. R. Toenshoff, S. Haider, E. Heinz, V. M. Hoenninger, M. Wagner, and M. Horn Diversity of Bacterial Endosymbionts of Environmental Acanthamoeba Isolates Appl. Envir. Microbiol., September 15, 2008; 74(18): 5822 - 5831. [Abstract] [Full Text] [PDF]
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 S. J. Perlman, S. E. Kelly, and M. S. Hunter Population Biology of Cytoplasmic Incompatibility: Maintenance and Spread of Cardinium Symbionts in a Parasitic Wasp Genetics, February 1, 2008; 178(2): 1003 - 1011. [Abstract] [Full Text] [PDF]
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 S. J Perlman, M. S Hunter, and E. Zchori-Fein The emerging diversity of Rickettsia Proc R Soc B, September 7, 2006; 273(1598): 2097 - 2106. [Abstract] [Full Text] [PDF]
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 G. R. Noel and N. Atibalentja 'Candidatus Paenicardinium endonii', an endosymbiont of the plant-parasitic nematode Heterodera glycines (Nemata: Tylenchida), affiliated to the phylum Bacteroidetes. Int J Syst Evol Microbiol, July 1, 2006; 56(Pt 7): 1697 - 1702. [Abstract] [Full Text] [PDF]
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M. Marzorati, A. Alma, L. Sacchi, M. Pajoro, S. Palermo, L. Brusetti, N. Raddadi, A. Balloi, R. Tedeschi, E. Clementi, et al. A Novel Bacteroidetes Symbiont Is Localized in Scaphoideus titanus, the Insect Vector of Flavescence Doree in Vitis vinifera Appl. Envir. Microbiol., February 1, 2006; 72(2): 1467 - 1475. [Abstract] [Full Text] [PDF]
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