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1 Department of Biology, Box 355325, University of Washington, Seattle, WA 98195-5325, USA
2 Microbiology Section, University of California, Davis, CA 95616-8665, USA
3 Division of Microbial Ecology, Institute of Ecology and Conservation Biology, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria
4 University of Georgia, Athens, GA 30602, USA
Correspondence
Karin D. E. Everett
kdeeverett{at}hotmail.com or
kdee2004{at}u.washington.edu or
keverett{at}uga.edu
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The GenBank/EMBL/DDBJ accession numbers for genomic fragments containing the rRNA operons of ‘Candidatus F. bemisiae’ Falk and ‘Candidatus F. eriococci’ Elm are respectively AY140910 and AY140911.
An extended neighbour-joining tree is available as supplementary material in IJSEM Online.
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). Two have been characterized, including rRNA gene sequence analyses (Clark et al., 1992; Thao & Baumann, 2004a; Zchori-Fein & Brown, 2002). The third endosymbiont, when examined using electron microscopy (EM), has a biphasic appearance (Fig. 1). The electron-dense globular bodies of the biphasic endosymbiont are 0·2–0·25 µm wide and the less dense morphological forms are 0·7–0·8 µm wide and 0·7–2·5 µm long (Costa et al., 1995). The chlamydial nature of the biphasic endosymbiont is suggested by PCR amplification of extracted total insect DNA using 23S rRNA gene signature sequence primers (Thao et al., 2003; Everett et al., 1999a). Analysing a 16·6 kb XhoI–EcoRV genome segment from the organism, Thao et al. (2003) found that the full-length 16S rRNA and 23S rRNA gene sequences were 91 % identical to rRNA genes in Simkania negevensis ZT, the type strain, species and genus of the Simkaniaceae (Table 1), and that, like S. negevensis, the 23S rRNA gene contained an intron (Everett et al., 1999b). Although the endosymbiont was not isolated, Thao et al. (2003) proposed the names ‘Fritschea bemisiae’ for the endosymbiont and ‘Fritschea eriococci’ for a related endosymbiont.
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). In an effort to culture this endosymbiont, we used an Acanthamoeba co-cultivation method that we use routinely to isolate strains of the Parachlamydiaceae. This method has been shown to work for culture of S. negevensis (Kahane et al., 2001). In the present study, co-cultivation of disrupted Bemisia with amoebae in trypticase soy yeast broth did not result in chlamydial growth in the broth or amoebae. Each time we thought the endosymbiont might be growing, it was lost from the amoeba culture, perhaps due to extremely slow growth. We have not been able to confirm growth by fluorescent in situ hybridization or by sequencing and have not tried to culture the endosymbiont by other means. The category Candidatus accommodates more than two dozen bacterial taxa not yet isolated or cultivated in vitro. For these reasons, we propose that ‘Fritschea’ and similar endosymbionts belong to a new genus designated ‘Candidatus Fritschea’.
The cloned and sequenced 16·6 kb genomic fragment from the endosymbiont contained 10 predicted open reading frames (ORFs) and an rRNA operon. To characterize the relationship of the endosymbiont to chlamydiae, we compared these sequences to the genome sequences of four species of the Chlamydiaceae and strain UWE25 from the Parachlamydiaceae (Horn et al., 2004; Kalman et al., 1999; Read et al., 2000, 2003; Stephens et al., 1998). In the genomes from the Chlamydiaceae, three of the endosymbiont ORFs were absent from all four sequenced species: glycosylhydrolase, transposase and GTP-binding protein (Table 2). Six ORFs were present in the species from the Chlamydiaceae, but were more similar to UWE25 (Parachlamydiaceae) ORFs (Table 2). None was located in the vicinity of an rRNA operon, but the tenth ORF was an endonuclease in the 23S rRNA gene intron. The endosymbiont 16S and 23S rRNA gene sequences were more than 80 % identical to chlamydial rRNA genes (Table 1
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). The six ORFs that were clustered downstream of the endosymbiont rRNA genes were also clustered in UWE25 (Locus Tags pc0231–39; Table 2), although not in the vicinity of an rRNA operon. Two of the endosymbiont genes upstream of the rRNA genes, yaeL and a putative transposase, were also in close proximity in UWE25. These transposase ORFs were located in large predicted, complementary hairpins (not shown). The endosymbiont transposase was related to an IS982 element in Photorhabdus luminescens, a broad-spectrum insect pathogen and gammaproteobacterial symbiont of nematodes (Duchaud et al., 2003). Between yaeL and the transposase gene in the endosymbiont was a glycosylhydrolase gene. UWE25 had three different ORFs between yaeL and the transposase (pc0262–64); a glycosylhydrolase ORF (pc1825) was located 1562 ORFs away on the UWE25 chromosome. Only the intron ORF of the endosymbiont was absent from UWE25, which did not have a 23S rRNA gene intron. The ORF, however, did share 55 % amino acid sequence identity with the endonuclease in the 23S rRNA group I intron of S. negevensis ZT. Both introns were located in the I-CpaI restriction site (position 1910, by Escherichia coli numbering; data not shown).
Chlamydiae are increasingly being identified and classified on the basis of rRNA gene sequence, but as yet there are few well-characterized chlamydial genera. Current standards rely on percentage rRNA gene sequence identity to facilitate orderly discovery, comparison and eventual classification of novel species (Everett et al., 1999a). Parachlamydiaceae and Chlamydiaceae, for example, are separate families because they have <90 % 16S rRNA gene sequence identity. In fact, we now know that their 85 % 16S rRNA gene sequence identities correlate with great genomic, pathogenic and evolutionary differences (Horn et al., 2004). Despite clear standards for the taxonomic placement of novel chlamydiae, errors are sometimes made. For example, the 16S rRNA gene sequence of ‘Candidatus Rhabdochlamydia’ is 91 % identical to the environmental chlamydiae lineage (ECL) VI of chlamydiae and only 84 % identical to S. negevensis (Kostanj
ek et al., 2004). Nonetheless, solely based on a neighbour-joining analysis of 16S rRNA gene sequences, ‘Candidatus Rhabdochlamydia’ was placed in the family Simkaniaceae (Kostanjek et al., 2004). Phylogenetic instability increases with the addition of novel, deeply branching 16S rRNA gene sequences, and branch points lose bootstrap and treepuzzle support. Phylogenetic analysis alone does not resolve chlamydial relationships.
To delineate the relationship between chlamydiae and the B. tabaci biphasic endosymbiont, two 16S rRNA gene sequence datasets were aligned. The first contained only full-length or nearly full-length sequences; it was analysed for percentage identity. The result was consistent with previous analyses of chlamydiae and in Fig. 2 provided a backbone for the analysis of the second dataset. The second dataset comprised 331 chlamydia-like 16S rRNA gene signature sequences. Bootstrap analysis of the aligned sequences identified the most strongly supported similarity clusters. The signature sequences correspond to nucleotide positions 40–337 (E. coli numbering) and contain the highest proportion of differences in the chlamydial 16S rRNA gene (Everett et al., 1999a) (Fig. 2 and Supplementary Fig. S1 available in IJSEM Online). A reliably aligned 202-base segment of this dataset contained 43 identical positions. Bootstrap analysis identified six reliably clustered families and 92 lineages containing only one or two sequences (Fig. 2). Of all of them, the endosymbiont signature sequence was most similar to the S. negevensis signature sequence. The next closest were CRG26 (from human tissue) and CRG34 (from fertilizer) (Meijer & Ossewaarde, 2002). Bootstrapping placed S. negevensis with ‘Candidatus Fritschea’, but not with any other sequences. Clusters that were identified had varying traits, including pathogenicity, endosymbiosis, human infectivity and host specificity (see Supplementary Fig. S1). Obtained from many continents, these groups showed no evidence of geographical specificity.
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). The E. spurius 16S rRNA gene sequence (presumably from another endosymbiont) was 97 % identical to the B. tabaci endosymbiont sequence (Table 1). The full-length 16S rRNA gene sequence of the endosymbiont was also nearly identical to a DNA sequence obtained from B. tabaci biotype Jatropha. E. spurius did not have a 23S rRNA gene intron.
This study brings together evidence for a chlamydial endosymbiont in the whitefly B. tabaci (Sternorrhyncha, Aleyrodidae): it lives inside cells, is biphasic, has >80 % full-length rRNA gene sequence identity with species of the Chlamydiales, clusters with 91 % rRNA gene sequence identity in the family Simkaniaceae and has nine ORFs most closely related to members of the Parachlamydiaceae, compared with Chlamydiaceae or any other available lineage. Chlamydiae are often pathogenic, whereas primary endosymbionts typically benefit their hosts. Indeed, three observations indicate that the biphasic endosymbiont of B. tabaci may be pathogenic: (i) the 18S rRNA gene sequences of B. tabaci and B. argentifolii are indistinguishable, indicating that these whiteflies are closely related; (ii) EM and PCR show that B. argentifolii lacks the chlamydial endosymbiont of B. tabaci (Costa et al., 1995; Thao et al., 2003); and (iii) B. argentifolii causes serious disorders not caused by B. tabaci and is more vigorous with respect to growth and progeny production (Costa et al., 1995). Thus, Costa et al. (1995) proposed that the lower fecundity and narrower host range of B. tabaci may be due to the chlamydial endosymbiont. The prevalence of chlamydiae in insects is not known. Thao et al. (2003) studied a strain of B. tabaci that is maintained by Bryce Falk at the University of California, Davis. Zchori-Fein & Brown (2002) examined 20 B. tabaci strains and placed a chlamydiae-like ‘jatropha’ sequence from B. tabaci in GenBank, but B. tabaci ‘Jatropha’ was not described in their publication. Although B. tabaci is less pathogenic than B. argentifolii, many agricultural crops are severely infested with B. tabaci, including watermelons, pumpkins, squash, tomatoes, cotton, soybeans and peanuts, as are numerous weeds (R. Sprenkel and S. Olson, unpublished; http://n-fl-bugs.ifas.ufl.edu/more/Insect_week/2-18.htm). Due to its status as a pest, the availability of B. tabaci for research is restricted.
Symbionts in general belong to many bacterial phyla, including the Proteobacteria, Bacteroidetes, Firmicutes and Chlamydiae, and the Archaea. Endosymbiont phyla in insects are similarly diverse (Wernegreen, 2002). The primary and secondary non-chlamydial endosymbionts in B. tabaci collections are gammaproteobacteria (Clark et al., 1992; Thao & Baumann, 2004a, b; Zchori-Fein & Brown, 2002). The primary gammaproteobacterial endosymbionts have been designated ‘Candidatus Portiera aleyrodidarum’ (Thao & Baumann, 2004a). They are obligate and group with Zymobacter in the Halomonadaceae. The secondary endosymbionts group with Enterobacteriaceae, are not obligate and are thought to have been recently acquired (Clark et al., 1992; Thao & Baumann, 2004b; Zchori-Fein & Brown, 2002). Chlamydial endosymbionts and intracellular bacteria live in many host lineages: mammals, marsupials, birds, reptiles, amphibians, amoebae, the crustacean Porcellio scaber and now insects (for up-to-date reviews see http://www.chlamydiae.com). Crustaceans and insects are sister taxa (Roehrdanz et al., 2002). This suggests that an ancestor of both might have acquired chlamydiae long ago, but there is also evidence that chlamydiae may have played an ancestral role in the evolution of plants (Greub & Raoult, 2003; Horn et al., 2004). The strongest support for this is that 11 % of the ORFs in the UWE25 genome (Parachlamydiaceae) are most closely related to sequences from chloroplasts, cyanobacteria and plants (Horn et al., 2004); 4 % of the ORFs in the genomes from the Chlamydiaceae are closely related to sequences from plants (Brinkman et al., 2002). In addition, the 23S rRNA gene group I introns of the endosymbiont and S. negevensis are most closely related to chloroplast rRNA gene introns (Everett et al., 1999b). Chlamydiae have not yet been found in plants, but B. tabaci and E. spurius feed on plant phloem, so it may be that plant genes were acquired by chlamydiae via horizontal transfer through insect feeding activity.
We propose that the chlamydia-like endosymbionts of B. tabaci (Sternorrhyncha, Aleyrodidae) and E. spurius (Sternorrhyncha, Eriococcidae) should be given Candidatus status (Murray & Schleifer, 1994). The 16S rRNA gene sequences of these endosymbionts are 
95 % identical to each other and have 90 % identity to the 16S rRNA gene sequence of S. negevensis ZT, so they belong to a separate genus in the family Simkaniaceae (Everett et al., 1999a). They should be specifically detectable with the labelled 16S rRNA-targeted oligonucleotide probe 5'-TTCTCTTTCCGCAAGGCC-3' (showing at least four mismatches with all other 16S rRNA sequences currently available). PCR using primers U23F (5'-GATGCCTTGGCATTGATAGGCGATGAAGGA-3') and 23SIGR (5'-TGGCTCATCATGCAAAAGGCA-3') amplifies ‘Candidatus Fritschea’ endosymbionts but not gammaproteobacteria (Everett et al., 1999a; Thao et al., 2003).
Description of ‘Candidatus Fritschea bemisiae’
‘Candidatus Fritschea bemisiae’ (Frit'sche.a. N.L. fem. n. Fritschea after Thomas R. Fritsche, American physician and parasitologist, whose studies initiated a major change in our perception of the natural history and diversity of the Chlamydiae. be.mi'si.ae. N.L. gen. fem. n. bemisiae of Bemisia, the genus of whitefly insects in which it was first discovered).
The host range currently includes the whitefly Bemisia tabaci (Sternorrhyncha, Aleyrodidae). ‘Candidatus Fritschea bemisiae’ can be detected and identified using EM, PCR amplification and DNA sequence analysis. EM detection of ‘Ca. F. bemisiae’ in the bacteriocytes of B. tabaci shows intracellular growth, small rod-like reticulate bodies and electron-dense elementary bodies (0·2–0·8 µm). There is evidence for a single ribosomal operon in ‘Ca. F. bemisiae’. The G+C content is 40 mol% in a 16·6 kb ‘Ca. F. bemisiae’ genome fragment containing the rRNA operon (GenBank accession no. AY140910). Gene organization in this fragment is most similar to gene organization in strain UWE25 from the Parachlamydiaceae, the only genome sequenced to date from an organism in the order Chlamydiales not belonging to the Chlamydiaceae. The rRNA operon does not include a tRNA. Like S. negevensis, ‘Ca. F. bemisiae’ has a group I intron in the 23S rRNA gene (position 1910, E. coli numbering). Strain Falk is the reference strain of the species ‘Ca. F. bemisiae’ and was reared in the laboratory of B. W. Falk at UC Davis, CA, USA.
Description of ‘Candidatus Fritschea eriococci’
‘Candidatus Fritschea eriococci’ (e.ri.o.coc'ci. N.L. gen. masc. n. eriococci of Eriococcus, the genus of scale insects in which it was first discovered).
The host range currently includes the scale insect Eriococcus spurius (Sternorrhyncha, Eriococcidae). ‘Candidatus Fritschea eriococci’ is currently known only by PCR and sequencing of DNA extracted from Eriococcus collected from an elm tree in Davis, CA, USA. The rRNA operon does not include a tRNA (GenBank accession no. AY140911); unlike ‘Ca. F. bemisiae’ and S. negevensis, ‘Ca. F. eriococci’ strain Elm does not have a 23S rRNA gene group I intron. Strain Elm is the reference strain of the species ‘Ca. F. eriococci’.
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ACKNOWLEDGEMENTS |
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