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The Rickettsial Outer-Membrane Protein a and B Genes of Rickettsia

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The Rickettsial Outer-Membrane Protein a and B Genes of Rickettsia International Journal of Systematic and Evolutionary Microbiology (2000), 50, 1775–1779 Printed in Great Britain The rickettsial outer-membrane protein A and B NOTE genes of Rickettsia australis, the most divergent rickettsia of the spotted fever group John Stenos1,2 and David H. Walker1 Author for correspondence: John Stenos. Tel: j61 3 5226 7552. Fax: j61 3 5226 7940. e-mail: JOHNS!BarwonHealth.org.au 1 Department of Pathology, The genes for rickettsial outer-membrane protein A (rOmpA), a distinguishing University of Texas Medical feature of spotted fever group (SFG) rickettsiae, and rOmpB, a genus-specific Branch at Galveston, Galveston, TX 77550, USA protein, were identified and sequenced in Rickettsia australis. The amino acid sequences of domains I, III and IV of the R. australis rOmpA share close 2 The Australian Rickettsial Reference Laboratory, The homology with those of rOmpA of other SFG rickettsiae, but the repeat region Douglas Hocking Research (domain II) is dramatically different from that of other known SFG rOmpA. Institute, Geelong R. australis rOmpB is more similar to rOmpB of other SFG rickettsiae than to Hospital, Geelong, Victoria 3220, Australia that of typhus group rickettsiae. Keywords: Rickettsia australis, spotted fever group rickettsiae, rOmpA, rOmpB The genus Rickettsia contains 21 named species and domain (Fournier et al., 1998). Complete rOmpA the unnamed AB bacterium (Beati & Raoult, 1993; sequences have been reported only for Rickettsia Beati et al., 1993, 1997; Fournier et al., 1998; Kelly et rickettsii and Rickettsia conorii (Anderson et al., 1990; al., 1996; Roux & Raoult, 1995; Roux et al., 1997; Crocquet-Valdes et al., 1994). Previous attempts to Stenos et al., 1998; Stothard & Fuerst, 1995; Uchida et detect rompA in Rickettsia australis have been un- al., 1992; Weiss & Moulder, 1984; Werren et al., 1994). successful (Eremeeva et al., 1994; Fournier et al., Twelve named species are human pathogens. These 1998; Gilmore & Hackstadt, 1991). organisms belong to either the spotted fever group (SFG) or typhus group (TG). The SFG is characterized The major surface protein of all Rickettsia species, as having rickettsial outer-membrane protein A rickettsial outer-membrane protein B (rOmpB), pos- (rOmpA) and distinctive antigenic epitopes on its sesses conformational epitopes that have been used to lipopolysaccharide (Anacker et al., 1987; Feng et al., classify rickettsial species antigenically (Anacker et al., 1987; Walker et al., 1995; Xu & Raoult, 1998). rOmpA 1987; Carl et al., 1990; Dasch, 1981; Gilmore, 1990; contains a domain consisting of 6–15 near identical Gilmore et al., 1989; Walker et al., 1995; Xu & Raoult, tandem repeat units (Anderson et al., 1990; Crocquet- 1998; Yu et al., 1990). rOmpB is a protein of 167 kDa, Valdes et al., 1994; Gilmore, 1993; Walker et which is processed after translation to the mature 135 al., 1995). The main apparent explanation for anti- kDa S-layer protein (Carl et al., 1990; Gilmore et al., genic differences among SFG rickettsiae including 1991; Hackstadt et al., 1992; Palmer et al., 1974). The intraspecific diversity is the order and number of the complete sequence of rompB has been reported only repeat units of rOmpA (Crocquet-Valdes et al., for Rickettsia prowazekii, Rickettsia typhi, R. rickettsii 1994; Gilmore, 1993). The TG lacks rOmpA and and Rickettsia japonica (Carl et al., 1990; Gilmore et possesses its own distinctive lipopolysaccharide epi- al., 1991; GenBank accession no. AB003681). topes (Gilmore & Hackstadt, 1991; Walker et al., To determine their phylogenetic relationships, we 1997). sequenced rompA and rompB of R. australis and rompB A recent phylogenetic study of 15 strains of SFG of R. conorii. rickettsiae reported highly conserved DNA sequences for the regions of rOmpA outside the tandem repeat DNA was extracted from R. australis PHS and R. conorii Malish 7, cultivated in Vero cell culture and ................................................................................................................................................. purified by Renografin density-gradient centrifugation Abbreviations: SFG, spotted fever group; TG, typhus group. (Hanson et al., 1981). Among overlapping primer The GenBank accession numbers for the rompA sequence of Rickettsia australis PHS, the rompB sequence of R. australis PHS and the rompB pairs designed from sequences of the R. rickettsii sequence of Rickettsia conorii Malish 7 are AF149108, AF149109 and rompA gene, only one pair [F3-4936 (GGTGGTCA- AF149110, respectively. GGCTCTGAAGCTAAC) and B21-6324 (TGCAG- 01310 # 2000 IUMS 1775 J. Stenos and D. H. Walker ................................................................................................................................................................................................................................................................................................................. Fig. 1. Phylogenetic tree constructed using sequences of domain I (left) (194 amino acids) and domain II (right) (1000 amino acids) of rOmpA of SFG rickettsial species with bootstrap values that are greater than 50 at the nodes. A total of 17 rickettsial strains were compared. The scale indicates 5 amino acid changes between the species. TTTGATAACCGACAGTCTC)] yielded a PCR pro- duct of 1400 bp with the Advantage genomic PCR kit R. conorii (Malish 7) [AF149110] (Clontech) and 35 cycles of denaturation at 94 mC for 100 1 min, annealing at 55 mC for 1 min and extension at 68 C for 1 min. A 3903 bp PCR product of the rompB m R. rickettsii (R) [X18353] gene was amplified from R. australis and R. conorii 100 using primers designed from the R. rickettsii rompB gene, RA-120-1S (5h-CGG TCG ACA TGG TTA TAC AAA GTG CTA-3h) and RA-120-2S (5h-CCG R. japonica (YH) [AB003681] TCG ACA TTA GAA GTT TAC ACG GAC-3h). Both upstream and downstream sequences of the R. australis rompA gene were determined using a GenomeWalker kit (Clontech), with some modifi- R. australis (PHS) [AF149109] cations. All PCR products amplified in this study were cloned using the PCR2.1 TA Cloning kit (Invitrogen) and R. typhi (Wilmington) [L04661] STBL2 competent cells, which contain a unique set of genetic markers allowing for stable cloning of direct 100 repeats. The rickettsial DNA was excised from the PCR2.1 TA vector representing positions 2982–3099 R. prowazekii (Breinl) [M37647] using the flanking EcoRI restriction sites and sub- 50 amino acid changes cloned into pGEM7. The sequence of the repeat region ................................................................................................................................................. of the R. australis rompA was obtained by unidirec- Fig. 2. Phylogenetic tree constructed using amino acid tional deletion of the insert rompA gene in pGEM7 sequences of rOmpB and bootstrap values that are greater than 50 at the nodes. Amino acid sequence derived from a 3n9kb using the Erase-a-base kit (Promega). All PCR segment of the R. australis template was compared with five products were sequenced using an ABI PRISM 377 other rickettsial species. The scale indicates 50 amino acid sequencer. changes between the species. 1776 International Journal of Systematic and Evolutionary Microbiology 50 rOmpA and rOmpB genes of Rickettsia australis Table 1. Divergence of two rOmpA segments of R. australis and other SFG rickettsiae R. australis R. aeschlimannii R. africae R. conorii R. honei R. japonica R. massiliae R. montanensis R. parkeri R. rhipicephali R. rickettsii R. sibirica R. aeschlimannii 0n142857 R. africae 0n142857 0n048338 R. conorii 0n148936 0n05279 0n010574 R. honei 0n147416 0n048265 0n015106 0n019608 R. japonica 0n147416 0n051282 0n031722 0n036199 0n031674 R. massiliae 0n139818 0n034691 0n039275 0n043741 0n040724 0n045249 R. montanensis 0n144377 0n048338 0n039275 0n043807 0n043807 0n048338 0n031722 R. parkeri 0n153495 0n057315 0n012085 0n019608 0n024133 0n037707 0n045249 0n045317 R. rhipicephali 0n138298 0n031674 0n036254 0n040724 0n037707 0n042232 0n015060 0n033233 0n045249 R. rickettsii 0n151976 0n05287 0n019637 0n02568 0n021148 0n033233 0n045317 0n045317 0n027190 0n039275 R. sibirica 0n162614 0n063348 0n019637 0n027149 0n031674 0n048265 0n054299 0n055891 0n025641 0n051282 0n036254 R. slovaca 0n144377 0n048265 0n009063 0n013575 0n015083 0n031674 0n039216 0n039275 0n016591 0n036199 0n021148 0n025641 The deduced amino acid sequences were aligned using These data suggest a fundamental biological function the computer program (DNA Star, for this region. Madison, WI, USA) based upon residue homology. Phylogenetic analyses were performed using the maxi- GenBank accession numbers for the genes charac- mum-parsimony program of the 4.0 software terized in this study are as follows: R. australis (Sinauer Associates, Sunderland, MA, USA). Distance (strain PHS) rompA, AF149108; R. australis (strain matrix analyses were generated using the Kimura two- PHS) rompB, AF149109; and R. conorii (Malish correction for multiple substitutions. Bootstrap values 7 strain) rompB, AF149110. The GenBank acces- (Felsenstein, 1985) for the consensus tree were based sion numbers of all other rickettsial rompA on analysis of 1000 replicates. sequences compared are R. aeschlimannii (strain MC16), U43800 and U83443; R. africae (strain The R. australis rompA has a 6318 bp ORF with a ESF-5), U43790 and U83436; R. conorii (Moroccan repeat region of more than 2 kb composed of eight strain), U45244 and U83448; R. conorii (Astrakhan (255 bp) complete and one (63 bp)
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