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Corresponding author: Jörg Soppa, J. W. Goethe-Universität, Biozentrum Niederursel, Institut für Mikrobiologie, Marie-Curie-Str. 9, D-60439 Frankfurt, Germany., soppa{at}em.uni-frankfurt.de (E-mail)
Communicating editor: F. PFEIFER
 | ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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More than 40 nitrate respiration-deficient mutants of Haloferax volcanii belonging to three different phenotypic classes were isolated. All 15 mutants of the null phenotype were complemented with a genomic library of the wild type. Wild-type copies of mutated genes were recovered from complemented mutants using two different approaches. The DNA sequences of 13 isolated fragments were determined. Five fragments were found to overlap; therefore nine different genomic regions containing genes essential for nitrate respiration could be identified. Three genomic regions containing genes coding for subunits of ABC transporters were further characterized. In two cases, genes coding for an ATP-binding subunit and a permease subunit were clustered and overlapped by four nucleotides. The third gene for a permease subunit had no additional ABC transporter gene in proximity. One ABC transporter was found to be glucose specific. The mutant reveals that the ABC transporter solely mediates anaerobic glucose transport. Based on sequence similarity, the second ABC transporter is proposed to be molybdate specific, explaining its essential role in nitrate respiration. The third ABC transporter is proposed to be anion specific. Genome sequencing has shown that ABC transporters are widespread in Archaea. Nevertheless, this study represents only the second example of a functional characterization.
ARCHAEA form a third monophyletic domain of living organisms apart from Bacteria and Eukarya (
In contrast to the increasing knowledge about basal transcription, only a little information about regulation of transcription is available. As many components of the archaeal central metabolism are more closely related to bacterial than to eukaryal enzymes, it seems interesting to study how "Bacteria-like" genes are regulated in organisms with a "Eukarya-like" transcription apparatus. A variety of model systems that will allow study of transcriptional regulation in Archaea emerge (e.g.,
ABC transporters couple the hydrolysis of ATP to solute transport across biological membranes (for reviews see
ABC transporters are typically composed of two membrane subunits and two ATP-binding subunits, both of which can be either homodimeric or heterodimeric. In addition, the genes for two or more subunits can be fused, and the functions are then fulfilled by protein domains of fusion proteins instead of different polypeptides.
The ATP-binding subunit is typically characterized by several well-conserved sequence motifs: a Walker site A (GXXGXGKS/T; X represents any amino acid), a helical domain, a linker peptide (LSGGQQ/R/KQR), a Walker site B (hhhhD; h represents a hydrophobic amino acid), and a switch region with a conserved histidine. Membrane subunits typically contain five to six membrane-spanning helices and a so-called EAA-loop ~100 amino acids from the C terminus (EAAXXLGX11LP). Many bacterial ABC transporters contain, in addition, periplasmic solute-binding proteins, which carry the substrate to the transport complex. Binding proteins from gram-negative bacteria are soluble in the periplasm, whereas binding proteins from gram-positive bacteria are bound to the cytoplasmic membrane by a lipid anchor or by electrostatic forces.
| MATERIALS AND METHODS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Organisms:
H. volcanii WR340 was obtained from Moshe Mevarech (Tel Aviv University, Tel Aviv, Israel). Escherichia coli XL-1 Blue MRF' and E. coli SCS110 were obtained from Stratagene (Heidelberg, Germany).
Media and growth conditions:
H. volcanii WR340 was grown at 42° either in complex medium as described by
Molecular biological methods:
General molecular biological methods were performed according to
Construction of a genomic library and complementation of nitrate respiration-deficient mutants:
Genomic DNA from wild-type H. volcanii was isolated as described previously (
H. volcanii has a restriction system that recognizes GATC-methylated DNA, and consequently the transformation frequency using unmethylated DNA is 1000-fold higher than that using dam-methylated DNA (
Reisolation of wild-type copies after complementation:
Two strategies were used to reisolate wild-type copies of the genes defective in the nitrate respiration-deficient mutants (see RESULTS). In both cases, genomic DNA of the complemented mutants was isolated and cleaved with restriction endonucleases at a DNA concentration of 50 ng/µl. After endonuclease inactivation, the DNA fragments were religated at a DNA concentration of 5 ng/µl, resulting in intramolecular circularization. The fragment mixture was used to transform E. coli. Only religated fragments containing the vector pBN1 and haloarchaeal genomic DNA flanking the integration site were able to yield stable ampicillin-resistant transformants. Plasmids were isolated from several independent clones and characterized by mapping with restriction endonucleases. Complementation of the respective nitrate respiration-deficient H. volcanii mutants allowed us to identify plasmids with haloarchaeal genomic fragments including wild-type copies of the mutated genes. After this functional test, the inserts of selected plasmids were sequenced on both strands by primer walking.
Northern blot analysis:
For Northern blot analysis, total RNA was isolated from wild-type cells according to
Databases, computer programs, and internet sites:
The EMBL nucleotide sequence database (
Nucleotide sequence accession numbers:
The nucleotide sequences have been deposited in the EMBL database under the accession nos. AJ238879 (glucose-specific ABC transporter), AJ238878 (presumed molybdate transporter), and AJ238877 (presumed anion transporter).
| RESULTS AND DISCUSSION |
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| TOPABSTRACTMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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Characterization of nitrate respiration-deficient mutants:
Nitrate respiration-deficient mutants were isolated using an optimized 5-bromo-2'-deoxyuridine selection procedure as previously described (
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Construction of a genomic library of H. volcanii:
The restriction endonuclease HpaII was chosen for library construction. It has the recognition sequence G'CGC and upon total digestion cleaves the GC-rich genome of H. volcanii into fragments of an average size below 0.5 kbp. For a statistical representation of the haloarchaeal genome, the conditions for partial cleavage were optimized and a fragment mixture with a size distribution of 3–5 kbp was isolated. It was cloned into the suicide vector pBN1 (
Complementation of mutants:
The genomic library was passed through the E. coli strain SCS110 to circumvent the restriction system of H. volcanii (see MATERIALS AND METHODS). Subsequently it was used for transformation of H. volcanii mutants. For stable transformation, plasmids have to integrate into the genome via homologous recombination at the site of the cloned genomic fragment (see Figure 2). Two consecutive aerobic cultures of the cell mixtures in novobiocin-containing medium were used to select for stable transformants. By plating of aliquots the average combined frequency of transformation and recombination was determined to be 2 x 104 per microgram of DNA. Anaerobic cultures in nitrate-containing liquid media were used to select for mutants complemented with wild-type copies of the inactivated genes. The resulting mixtures of complemented cells were plated on solid media, and the nitrate respiration-positive phenotype of randomly chosen clones was checked. In this study, 15 mutants of the null phenotype were chosen for complementation, and the isolation of complemented clones was successful in all cases.
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Isolation of wild-type copies of mutated genes:
In the genome of complemented mutants the integrated vector pBN1 is bordered by a wild-type copy and a mutated copy of a gene essential for nitrate respiration (see Figure 2). Two strategies were used to reisolate wild-type copies. The first approach made use of restriction enzymes, which cut at a single site at the border of the integrated pBN1 and at an unknown site within the genome (sites A or B in Figure 2). Genomic DNA of complemented mutants was cleaved with these enzymes in separate reactions, religated in dilute solutions, and the resulting fragment mixture was used to transform E. coli. This approach yielded pairs of plasmids for each mutant, one containing genomic DNA left of the integration site, the other containing genomic DNA right of the integration site. The plasmids were used to retransform the respective H. volcanii mutants. Complementation to the nitrate respiration-positive phenotype allowed the identification of plasmids with wild-type copies of essential genes defective in the mutants. This approach was successful in 6 out of the 15 cases. The approach will fail if the restriction sites A or B are very close to the integration site, allowing the cloning of only very small genomic fragments without enough wild-type information, or if the restriction sites are very far from the integration site, inhibiting cloning in E. coli.
In the remaining nine cases an alternative strategy was chosen. Genomic DNA of complemented mutants was cleaved with enzymes that do not cut within pBN1 (enzymes C in Figure 2). Emphasis was put on enzymes with AT-rich recognition sequences with a low average cutting frequency in the GC-rich genome. After religation in dilute solution, the fragment mixtures were used to transform E. coli. This approach leads to plasmids that contain genomic DNA flanking the integrated vector on both sides. After isolation from E. coli, plasmid sizes were checked, and plasmids of 8–10 kbp were chosen for retransformation of the respective H. volcanii mutants. Again, complementation of mutants to a nitrate respiration-positive phenotype revealed cloning of wild-type copies of the mutated genes. This approach was successful in the remaining nine cases.
Characterization of isolated genomic regions:
For each mutant 1 plasmid was chosen for sequence determination of the cloned genomic fragment. Before sequencing it was confirmed that the plasmid can complement the respective mutant. Until now the genomic fragments from 13 different plasmids were sequenced. Comparison of the sequences showed that 5 plasmids carried overlapping fragments from the same genomic region, whereas the remaining plasmids were from different parts of the genome. Therefore, in total, fragments from nine genomic regions carrying essential genes for nitrate respiration have been cloned. Here we present the data on three genomic regions that include genes for ATP binding cassette transporters (ABC transporters). The characterization of the six additional genomic regions is presented elsewhere. Mutants, plasmids, and relevant genes discussed below are summarized in Table 1.
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A glucose-specific ABC transporter:
Plasmid pCW292 was isolated from the complemented mutant 170/5 using the second approach. It contains an insert of ~3.8 kbp. Two partial open reading frames (ORFs) with haloarchaeal codon usage were detected (Figure 3A).
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Partial ORF 1 is similar to ATP-binding subunits of ABC transporters. A total of 313 C-terminal amino acids can be deduced from the partial gene sequence, which is larger than the 250 amino acids of a monomeric ATP-binding protein. The most similar protein is an ATP-binding subunit of an ABC transporter of Archaeoglobus fulgidus with 45% of identical amino acids (AF0887), which is annotated to be ribose specific based on its similarity with the E. coli ribose transporter RsbA. Most proteins in the protein sequence databases with similarity to the haloarchaeal protein are annotated as sugar-specific ABC transporters and they belong to ortholog group 2 (
Directly downstream of ORF1 a second partial ORF was found. Both ORFs overlap by four nucleotides, indicating that they are cotranscribed and that the gene products are involved in the same process. ORF2 codes for a polypeptide of 140 amino acids. The most similar protein is a permease subunit of an ABC transporter of A. fulgidus (52% identity), which is annotated to be ribose specific (AF0888). The ATP-binding subunit (see above) and the permease subunit of the A. fulgidus ribose ABC transporter are encoded by adjacent genes. The majority of database entries with similarity to the haloarchaeal protein deduced from ORF2 are permease subunits of sugar-specific ABC transporters and belong to ortholog group two. A multiple sequence alignment with the most similar database entries is shown in Figure 3C. The amino acid composition of the deduced protein shows the high abundance of alanine, leucine, and valine residues that is typical for haloarchaeal membrane proteins (
The two ORFs cover 1.5 kbp out of the 3.8 kbp of cloned genomic DNA. No further ORF with haloarchaeal codon usage could be detected within the remaining 2.3 kbp. To ascertain that mutant 170/5 has a defect within ORF1 or ORF2, the rest of the cloned genomic region was deleted from plasmid pCW292, yielding plasmid pCW20 (Figure 3A). It could still complement mutant 170/5, proving that the cloned ABC transporter is essential for nitrate respiration.
To elucidate the substrate specificity of this ABC transporter, H. volcanii wild type was grown anaerobically in synthetic medium with nitrate and different sugars as electron donors. It could not grow with ribose and most other sugars tested, but it could grow on glucose/nitrate and pyruvate/nitrate, respectively. Anaerobic growth of mutant 170/5 with pyruvate/nitrate was indistinguishable from the wild type, but it could not use glucose for nitrate respirative growth. However, the mutant can grow aerobically in synthetic medium using glucose as the sole energy source. These data show that (1) H. volcanii can couple glucose oxidation and nitrate reduction for anaerobic growth, (2) glucose is transported into the cell using an ABC transporter composed of at least ORF1 and ORF2, (3) during anaerobic growth no alternative glucose transport system is present, and (4) a different glucose transporter is present under aerobic conditions. This is in accordance with an earlier report that had shown that during aerobic growth glucose import by H. volcanii is catalyzed by a sodium/glucose-symporter (
An ABC transporter with presumed molybdate specificity:
Genomic DNA (3.5 kbp) was recovered from the complemented mutant 168/6. Two genes with haloarchaeal codon usage were detected, coding for the permease subunit of an ABC transporter (ORF1) and a benzaldehyde dehydrogenase (ORF2; Figure 4A). To clarify which of the genes is essential for nitrate respiration, two smaller plasmids containing exclusively the gene for the permease subunit (pCW15) or for the dehydrogenase (pCW10) were constructed. Upon transformation of the mutant, only pCW15 could restore the wild-type phenotype, proving that the ABC transporter is indispensable for nitrate respiration. A 340-bp overlapping part of this gene was sequenced previously by Charlebois and colleagues (R. FARAHANI, J.-C. IMBEAULT, A. ST. JEAN, C. C.-Y. CHAN, G. ALLARD AND R. L. CHARLEBOIS, unpublished data; accession no. U95374) while studying the instability of the megaplasmid pHV3, showing that this essential gene is not encoded on the chromosome.
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The amino acid composition of the permease subunit is typical for haloarchaeal membrane proteins with a high content of alanine, valine, and leucine residues (44.9%). A hydropathic profile allows the prediction of five membrane-spanning helices, which is typical for ABC transporters with an import function (data not shown). The deduced protein contains an EAA-loop that matches the consensus sequence well (Figure 4B).
The most similar database entry is the permease subunit of an ABC transporter from A. fulgidus (41% identity; AF0093), which is annotated to be sulfate specific due to its similarity to other ABC transporters. The highest similarity to a database entry with an experimentally proven function is to ModB of E. coli (
An ABC transporter with presumed anion specificity:
About 2.9 kbp of genomic DNA was recovered from the complemented mutant 167/30 using the first approach (Figure 5A). Three ORFs with haloarchaeal codon usage could be detected: the C-terminal part of an ORF coding for a conserved hypothetical archaeal protein of unknown function (ORF1) and two ORFs with coding capacity for the permease (ORF2) and the ATP-binding subunit (ORF3) of an ABC transporter. To elucidate whether the ABC transporter is essential for nitrate respiration, plasmid pCW30 was constructed. It contains only the ABC transporter genes but lacks the first open reading frame (Figure 5A). Transformation of mutant 167/30 with pCW30 restored the wild-type phenotype, proving that nitrate respiration requires the ABC transporter activity.
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The permease subunit is 232 amino acids long (Figure 5B). The amino acid composition is typical for haloarchaeal membrane proteins; the content of alanine, leucine, and valine residues is 39.2%. A hydropathic profile allows the prediction of five to six membrane-spanning helices (data not shown). The protein sequence contains an EAA-loop that matches the consensus sequence well. The database entry with the highest similarity is the permease subunit of an ABC transporter from Methanobacterium thermoautotrophicum (44% identity; MTH1731), which is proposed to be sulfate specific. Half of the 50 most similar database entries are annotated to be either sulfate or phosphate specific and belong to ortholog group 1-1 or 3-7, respectively.
A 289-amino-acid-long ORF with coding capacity for an ATP-binding subunit was found downstream of the permease gene. The two genes have an overlap of four nucleotides, indicating that they are cotranscribed. Database searches revealed that a high fraction of similar proteins are annotated to be phosphate specific and belong to ortholog group 3-7. A multiple sequence alignment of the ATP-binding subunit with the most similar database entries is shown in Figure 5B. As can be seen, the sequence motifs indicative for ABC transporters are well conserved in the haloarchaeal protein.
The substrate specificity of this ABC transporter is not clear. Primary sequences of both subunits indicate that it is anion specific. It seems possible that phosphate transport is mediated by different transporters aerobically and anaerobically, comparable to glucose transport. Alternatively, nitrate transport would be another essential process for nitrate respiration.
An unusual arginine content of haloarchaeal ATP-binding subunits:
Haloarchaeal soluble proteins have a very specific amino acid distribution as determined by the amino acid analysis of bulk haloarchaeal proteins (
The high arginine content of ~10% seems to be confined to haloarchaeal ATP-binding subunits. It is not found in the homologous ATP-binding proteins from Bacteria and other Archaea; e.g., the average arginine content of the nonhaloarchaeal sequences shown in Figure 3C and Figure 5C is 6%. Nor is it found in other soluble haloarchaeal proteins interacting with integral membrane proteins, i.e., the chemotaxis signal transducers CheA and CheB (
It is tempting to speculate that the high arginine content facilitates interactions with the negatively charged phospholipids and/or with the membrane subunit. In this respect it is noteworthy that in the anion transporter subunit the "haloarchaeal-specific arginines," which do not have counterparts in homologous proteins, are clustered around the helical domain (boxed in Figure 5C). The positive charge density of this region is extremely high: 11 out of 42 residues are arginines. On the basis of the analysis of suppressor mutations it was proposed earlier that this helical domain could be involved in the interaction of the ATP-binding subunits with the membrane subunits (
Transcription of ABC transporter genes:
To investigate transcription of the ABC transporter genes, Northern blot analyses were performed using RNA isolated from aerobically and anaerobically grown cultures. No transcripts could be detected. Therefore, unlabeled PCR fragments generated from the respective genes were used as internal standards to determine the sensitivity of detection, and transcription from the gene for the cell surface glycoprotein (
ABC transporters in Archaea:
The first archaeal ABC transporters were discovered in 1996 (
Conclusions:
Complementation of H. volcanii mutants with a genomic library of the wild type turned out to be a very effective method for identification of essential genes for nitrate respiration. In total, nine genomic regions have been detected until now, at least one of which resides on a megaplasmid. As will be presented elsewhere, highly expressed genes that are either constitutively transcribed or upregulated during nitrate respiration, as well as genes encoding regulatory proteins, were found. Here we show that also poorly expressed genes could be detected, coding for three different ABC transporters involved in substrate and cofactor import. The glucose-specific ABC transporter is essential solely under anaerobic conditions. This is in accordance with an earlier study, which showed that under aerobic conditions glucose is imported via a sodium:glucose-symporter.
| ACKNOWLEDGMENTS |
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This work was supported by the Deutsche Forschungsgemeinschaft (DFG) through grant So264/3. J.S. is supported by the DFG through a "Heisenbergstipendium" (grant So264/4).
Manuscript received March 22, 1999; Accepted for publication May 13, 1999.
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