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1 Japan Collection of Micro-organisms, RIKEN BioResource Center, Wako, Saitama 351-0198, Japan
2 Institute of Biology, Romanian Academy, Splaiul Independentei 296, PO Box 56-53, Bucharest 060031, Romania
3 Bio-Nano Electronics Research Centre, Toyo University, 2100 Kujirai, Kawagoe, Saitama 350-8585, Japan
4 Halophiles Research Institute, 677-1 Shimizu, Noda, Chiba 278-0043, Japan
Correspondence
Madalin Enache
madalin.enache{at}ibiol.ro
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. The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Haloferax sp. BV2 is AB258304. Alignments of deduced RpoB amino acid sequences are available as supplementary material with the online version of this paper.
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; Castillo et al., 2006). Although the majority are neutrophilic, 16 alkaliphilic species have been isolated from soda lakes in Kenya, China, India, Egypt, etc. (Horikoshi, 1999; Rees et al., 2004). Strains isolated in the early 1980s are classified in the genera Natronobacterium, Natronococcus and Natronomonas (Kamekura et al., 1997), and some recent isolates are accommodated in Halalkalicoccus (Xue et al., 2005) and Natronolimnobius (Itoh et al., 2005). These five genera are so far composed exclusively of alkaliphilic strains. On the other hand, the genera Halobiforma, Halorubrum, Natrialba and Natronorubrum consist of both neutrophilic and alkaliphilic species. Since the haloalkaliphilic members lack detectable amounts of glycolipids (Grant et al., 2001), analysis of the 16S rRNA genes has been a major criterion for their classification at the genus level. Thus, there is a need for other targets for chemotaxonomy and complementary molecular markers for the phylogeny of the Halobacteriaceae (Wright, 2006).
The DNA-dependent RNA polymerase subunit 
(in bacteria) or B (in archaea) gene (rpoB) has become a popular phylogenetic marker in recent years (Adékambi et al., 2003; Case et al., 2007; Dahllöf et al., 2000; Korczak et al., 2004). rpoB fulfils the following criteria to be useful in the phylogenetic analyses of archaea (Klenk & Zillig, 1994): (i) it is present in all archaea, and is a single-copy conserved gene, (ii) it is one of the important components of the transcription apparatus and therefore highly constrained to evolve at a reasonably slow rate and (iii) subunit B is the largest component of the RNA polymerase, approximately 1100 amino acids, in archaea; it is therefore large enough to guarantee high confidence in the phylogenetic analysis. The order of subunits in decreasing size is B, A', A'', D, E, F, G, H, I, K, L, M and N (Langer et al., 1995). The fact that only a single copy of each subunit is present in all bacteria and archaea is a tremendous advantage over the 16S rRNA gene for phylogenetic analyses (Acinas et al., 2004; Cilia et al., 1996). In the case of the Halobacteriaceae, species of some genera possess multiple copies of the 16S rRNA gene that exhibit very large divergence, which may lead to paralogous phylogeny. For example, Haloarcula marismortui possesses three copies that show 5 % divergence (Dennis et al., 1998; Baliga et al., 2004), while two copies in Haloarcula japonica (K. Nakasone, unpublished data) differ by 5.2 %. Two copies in Halosimplex carlsbadense display 6.7 % divergence (Vreeland et al. 2002), and one of the four genes in Natrinema sp. XA3-1 differs by 5 % from the other three copies (Boucher et al., 2004).
Substantial studies on the polymerase of haloarchaea were initiated by the group of Wolfram Zillig (Zillig et al., 1978). In Halobacterium halobium (presently regarded as a synonym of Halobacterium salinarum) and three methanogenic archaea, subunit B was shown to be split into smaller subunits, B' and B'' (Gropp et al., 1986), and complete sequences of the genes of subunits B'', B', A' and A'' (original nomenclature was B'', B', A and C; Leffers et al., 1989) of Hbt. halobium were determined. At present, it is known that the rpoB genes of all haloarchaea and methanogenic archaea whose genomes have been sequenced and that of Archaeoglobus fulgidus are fragmented into rpoB'' (5' side) and rpoB' (3' side). Recently, Walsh et al. (2004) have proposed that rpoB' can be used as an alternative to the 16S rRNA gene in the taxonomic investigation of haloarchaea. They demonstrated that the gene provided a similar degree of phylogenetic resolution to the 16S rRNA gene, yet does not bear the problem of paralogy, by showing that compositional bias of the nucleotides and amino acids of each sequence did not affect their phylogenetic analyses. A disadvantage in using the subunit B' is that the amplification of genes by PCR and subsequent sequencing are relatively difficult. In some strains, primer sets were not able to amplify the rpoB' gene or primers for sequencing the amplified genes did not work (Walsh et al., 2004). This drawback is, however, compensated for by the fact that the sequences are highly conserved in archaea, particularly in members of the Halobacteriaceae. In this study, we ascertained that the complete rpoB' sequences of the following five haloarchaea can be aligned without any gaps or deletions: Hbt. salinarum NRC-1 (1827 bp), Har. marismortui ATCC 43049T (1827 bp), Haloquadratum walsbyi DSM 16790 (1836 bp) (Bolhuis et al., 2006), Natronomonas pharaonis DSM 2160T (1833 bp) (Falb et al., 2005) and Haloferax volcanii DS2 (1830 bp). The first four gene sequences were downloaded from the Kyoto Encyclopedia of Genes and Genomes (KEGG; http://www.genome.jp/kegg/). The sequence of Hfx. volcanii DS2 was taken from the UCSC Archaeal Genome Browser (http://archaea.ucsc.edu/). The three to nine base differences observed amongst the five sequences are found in the 5' termini. Partial sequences of rpoB' determined by Walsh et al. (2004) (GenBank accession numbers AJ809508–AJ809527; 1305 bp, with two exceptions of 1291 and 1299 bp) were also aligned completely with the five sequences without any gaps or deletions. On the other hand, the lengths of rpoB'' of the five haloarchaea mentioned above were 1566–1578 bp. They also aligned quite well, and the 12 base differences were concentrated in 3'-terminal positions, where rpoB was split into rpoB'' and rpoB'.
In the present study, we sequenced PCR-amplified rpoB' subunit genes of 11 alkaliphilic strains of the genera Halobiforma, Halorubrum, Natrialba, Natronococcus, Natronolimnobius and Natronorubrum, as well as six allied neutrophilic strains of the genera Halobiforma, Haloferax and Natrinema. The gene sequences and their deduced amino acid sequences were aligned with the 23 sequences mentioned above. Phylogenetic analysis demonstrated that rpoB'- and RpoB'-based phylogenies are mostly congruent with the 16S rRNA gene-based phylogeny, but some incongruence was also observed. This study may be helpful for the accurate classification of haloalkaliphilic archaea, complementing the 16S rRNA gene-based phylogeny.
The haloarchaeal strains used in this study and accession numbers for their 16S rRNA and rpoB' gene sequences are listed in Table 1. The DNA was extracted using the method of Tamaoka (1994) and a segment of rpoB' (approx. 1300 bp) was amplified by PCR using the following 50 µl mixture: 5 µl 10x ExTaq PCR buffer, 5 µl dNTPs (2.5 mM each), 2.5 µl forward primer, 2.5 µl reverse primer (1.6 µM each), 34 µl distilled water, 0.5 µl Taq DNA polymerase (TaKaRa) and 0.5 µl purified DNA. In some experiments, Platinum Taq DNA polymerase High Fidelity (Invitrogen) was also used. Primers 444F (5'-TCCCGTACCCNGARCAYAAY-3'; Walsh et al., 2004) and 1743R (5'-TTGAAYGCGTAGSWSATCTC-3', designed in this work) were used for the amplification of rpoB' genes from Hbf. nitratireducens JCM 10879T, Hbf. lacisalsi JCM 12983T, Haloferax sp. BV2, Nab. chahannaoensis JCM 10990T, Nab. magadii NCMB 2190T, Nnm. pellirubrum JCM 10476T, Natrinema sp. XA3-1, Ncc. occultus NCMB 2192T, Nln. baerhuensis JCM 12253T, Nlm. innermongolicus JCM 12255T and Nrr. bangense AS 1.1984T. Another primer set, 398F (5'-ACCCGCAGCTCATCTTCGGYAT-3') and 1752R (5'-AGTAGAAGYTTRAANGCRTA-3'; Walsh et al., 2004), was used for Nrr. tibetense AS 1.2123T, while the third primer set 462F (5'-GCCWCSCCCCGNATTACGAT-3') and 1743R was used for Hrr. vacuolatum NCIMB 13189T, Nab. hulunbeirensis JCM 10989T, Nnm. versiforme JCM 10478T and Ncc. amylolyticus JCM 9655T.
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) and vector-specific primers T7 (5'-TAATACGACTCACTATAGGG-3') and U19 (5'-GTTTTCCCAGTCACGACGT-3'). In this study, three additional primers were used in sequencing of the gene in some strains: 841F (5'-CACCTCGACGAGGATGGCCTCGTCAA-3'), 1175R (5'-GTGAASGGCATGTCCTCGTG-3') and 1466R (5'-ACCATGTGGTAGAGCTTSTGGTAGAA-3'). The 16S rRNA gene sequence of Haloferax sp. strain BV2 isolated from Green Bath Lake in Romania was determined as described previously (Enache et al., 2007).
Multiple alignments of the nucleotide and deduced amino acid sequences were generated using CLUSTAL W and phylogenetic trees were reconstructed by the neighbour-joining method (Saitou & Nei, 1987) and evaluated by 1000 bootstrap samplings.
The alignment of 34 rpoB' gene sequences contained 1305 sites, of which 672 (51.5 %) were constant across all taxa. A phylogenetic tree reconstruction (Fig. 1; left side) showed that the species of the genera with multiple sequences individually formed coherent clusters except for Natronorubrum and Haloterrigena/Natrinema. It was noted that the genera Natrialba, Natronococcus, Halobiforma, Natronobacterium, Natronolimnobius, Natronorubrum, Natrinema and Haloterrigena formed a monophyletic group. The same group was also observed in the tree reconstructed from amino acid sequences translated from the corresponding rpoB' gene sequences (Fig. 1; right side). The alignment contained 435 sites, of which 281 (64.5 %) were constant across all taxa. Furthermore, the same group was supported in the tree reconstructed in this study from 16S rRNA gene sequences (Fig. 2). This group observed in the three trees seems equivalent to clade I detected by Walsh et al. (2004), composed of Natrialba, Halobiforma, Natronobacterium, Natronorubrum, Natrinema and Haloterrigena. The presence of this group was also detected in the phylogenetic tree presented by Wright (2006) based on 16S rRNA gene sequences. Taken together, the trees shown in Figs 1 and 2 suggested strongly that the genera Natronococcus and Natronolimnobius are also components of clade I. A separate, rather loose group, clade II, composed of Haloferax, Halogeometricum, Halobaculum and Halorubrum (Walsh et al., 2004), was also observed in the rpoB' gene and protein trees inferred in this study. Clade II, however, was not reproduced in the phylogenetic tree of Wright (2006) or a tree composed of sequences of the type strains of all species of the Halobacteriaceae that have validly published names (M. Kamekura, unpublished data).
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). Nab. asiatica, a neutrophilic species, and three alkaliphilic species, Nab. chahannaoensis, Nab. hulunbeirensis and Nab. magadii, formed a single cluster in the rpoB' gene tree. In the RpoB' protein tree, however, the three alkaliphilic species formed a tight group, and the neutrophilic species Nab. asiatica formed a group with species of Natronorubrum and Natronolimnobius. In order to make this situation clearer, we tried to amplify the gene from a strain of another neutrophilic species, Natrialba aegyptiaca JCM 11194T, but none of the rpoB' gene primers were able to amplify a product. The RpoB' protein tree reminded us of the suggestion that the three alkaliphilic species could be placed in a different genus (Xu et al., 2001). Further investigations of rpoB' gene and protein sequences of many strains that have been suggested to belong to the genus Natrialba should clarify the taxonomy of this genus.
The genus Natronorubrum is composed of three species at the time of writing (Cui et al., 2006). The 16S rRNA gene sequences of two species and isolate Natronorubrum sp. Tenzan-10 formed a tight group in the 16S rRNA gene tree (Fig. 2). In the work of Walsh et al. (2004), only isolate Natronorubrum sp. Tenzan-10 (=JCM 10938) was sequenced as a representative. In this study, we sequenced the rpoB' genes from the type strains of two species and noticed that the three sequences did not form a coherent cluster; two clustered with Natronolimnobius species and one with Haloterrigena and Natrinema species in the gene tree, whereas Nrr. tibetense clustered with Natronolimnobius species and Nab. asiatica in the protein tree (Fig. 1). More study is needed to clarify this situation.
Halorubrum is another genus composed of alkaliphilic and neutrophilic species. Although rpoB' genes have not been sequenced from the recently described alkaliphilic species Hrr. tibetense (Fan et al., 2004) and Hrr. alkaliphilum (Feng et al., 2005), the alkaliphilic species Hrr. vacuolatum clustered with the two neutrophilic species in all trees. Other genera with multiple species, Haloferax, Haloarcula, Halobiforma, Natronococcus and Natronolimnobius, were also supported as individual coherent groups in all trees.
It has been pointed out that the taxonomy of the genera Haloterrigena and Natrinema has problems (Tindall, 2003), and one of the aims of this work was to solve this problem based on rpoB' gene and protein sequences. We determined sequences from Nnm. pellirubrum JCM 10476T, Nnm. versiforme JCM 10478T and Natrinema sp. XA3-1 in this work. Amplification products of the expected size were obtained from Htg. saccharevitans JCM 12889T and Htg. thermotolerans DSM 11552T, but the sequences of five clones were not those of rpoB', suggesting that unrelated portions had been amplified. More effort will be needed for the design of better primers for amplification of rpoB' from these strains. The phylogenetic position of Natrinema sp. XA3-1 inferred from rpoB' gene and protein sequences was similar to that inferred from three of its 16S rRNA genes, SSU-B, -C and -D, rather than SSU-A (Fig. 2) (see also Fig. 5b of Boucher et al., 2004). Although we need more data from Haloterrigena, the available sequences formed coherent groups in the three trees, suggesting that the species of the two genera are very closely related. According to DNA G+C content, however, two lineages can be distinguished. Nnm. pellirubrum, Natrinema sp. XA3-1, Nnm. pallidum and Haloterrigena sp. GSL-11 are characterized by G+C contents greater than 65 mol%. Another lineage consisting of Nnm. versiforme and Htg. turkmenica is characterized by G+C contents lower than 65 mol%.
Despite difficulties in amplification and sequencing encountered by Walsh et al. (2004), Case et al. (2007) and in this study, the most important advantage of the use of the rpoB' gene is that the sequences are highly conserved amongst species of the family Halobacteriaceae. The 16 sequences determined in this study and those determined by Walsh et al. (2004) could be aligned unambiguously without any gaps. Thus, if gaps or insertions are detected in alignment of newly determined sequences, they are likely to come from misreading of sequencing or from PCR mutations. Furthermore, a set of a gap and an insertion in a short stretch of a sequence caused by two mistakes in reading (for example, within 10 to 15 nucleotides), but not apparent in the alignment of the nucleotides, will be detected in the alignment of the translated amino acid sequences (see an alignment of the translated amino acid sequences shown in Supplementary Fig. S1). On the other hand, gaps at 11 positions were required to obtain a reasonable alignment of the five 16S rRNA gene sequences from strains of Hbt. salinarum (1473 bp), Har. marismortui (1472 bp), Hfx. volcanii (1472 bp), Hqr. walsbyi (1472 bp; HQR01) and Nmn. pharaonis (1467 bp). In the alignment used in the reconstruction of Fig. 2, gaps were necessary in 49 positions in the inner part of the alignment and at 19 and 33 positions at the 5' and 3' termini, respectively.
We would like to conclude that, in spite of some incongruities, the rpoB' gene can be used as an excellent alternative molecular marker in phylogenetic analysis of the Halobacteriaceae.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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