THE JOURNAL OF BIOLOC~CAL CHEMISTRY Vol. 265, No. 35, Issue of December 15, pp. 21509-21513,199O 0 1990 by The American Society for Biochemistry and Molecular Biology, Inc. Printed in U.S.A.

Structure of an ATPase Operon of an Acidothermophilic Archaebacterium, Sulfolobus acidocaldarius*

(Received for publication, June 18, 1990)

Kimitoshi Denda, Jin Konishi, Kyoko Hajiro, Tairo Oshima, Takayasu Date+, and Masasuke Yoshida$ From the Department of Life Science, Tokyo Institute of Technology, Nagatsuta, Yokohama 227 and the *Department of Biochemistry, Kanazawa Medical University, Uchinada, Kawakita-gun, Zshikawa 920-02, Japan

The nucleotide sequence of the operon of the ATPase complex of an acidothermophilic archaehacterium, Sulfolobus acidocaldarius, has been determined. In ad- dition to the three previously reported genes for the a, (B, and c (proteolipid) subunits of the ATPase complex (Denda, K., Konishi, J., Oshima, T., Date, T., and Yoshida, M. (1989) J. Biol. Chem. 264, 7119-7121), the operon contained three other genes encoding hy- drophilic proteins with molecular masses 25, 13, and 7 kDa. The 25-kDa protein is the third largest subunit (y), the 13-kDa protein is most likely the fourth subunit (6), and the 7-kDa protein may correspond to an un- known subunit of the ATPase, tentatively named as t subunit. They do not have significant sequence simi- larity to subunits in FOF,-ATPases and eukaryotic V- type ATPases, whereas the other three subunits, CX, 8, and c, have homologous counterparts in FoF1- and V- type ATPases. The order of the genes in the operon was &Y&C. The S. acidocaldarius ATPase operon dif- fered from the eucabacterial FOF1-ATPase operon in that the former contains only one gene for a hydropho- bic subunit at the most downstream part of the operon whereas the latter has three hydrophobic F. genes preceding five hydrophilic F1 genes.

FOF1-ATPase in membranes of mitochondria, chloroplasts, and bacteria, synthesizes ATP coupled with an electrochem- ical gradient of protons generated by the electron transfer chain (l-3). It consists of two sectors: the water-soluble F,’ which retains ATP hydrolytic activity and the membranous F. which mediates proton transport across membranes. F1 and F. are comprised of five (cu, fi, y, 6, and t) and at least three (a, b, and c) kinds of subunits, respectively. These subunits are encoded in the same operon in genomes of Escherichia coli (4, 5) and the thermophilic bacterium PS3 (6). The order of the genes in their operons is I:a:c:b:8:oc:y:@:~ where I is a 14-kDa polypeptide whose exact role is still unknown.

It had been long believed that FOF1-ATPase is the only

* This work was partially supported by a Grant-in-Aid for Scien- tific Research (to M. Y.) from the Ministry of Education, Science and Culture of Japan. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked “aduertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EMBL Data Bank with accession number(s) JO5671.

I To whom correspondence should be addressed. ’ The abbreviations used are: F,, a water-soluble sector of F,F,-

ATPase; TFI, F, from a thermophilic bacterium PS3.

operational proton flow-driven ATP synthase, H’-ATP syn- thase, in all kinds of cells. However, novel ATPases, most likely a water-soluble part of membranous ATPase complexes which act as H’-ATP synthases in the cells, have been re- cently purified from the membranes of archaebacteria, such as Sulfolobus acidocaldarius (7,8), Methanosarcina barkeri (9), Halobacterium halobium (lo), and Halobacterium sacchurouo- rum (11, la), and their enzymatic properties are significantly different from those of F1. Genes of their major subunits, the cy and p subunits, have been cloned and sequenced. Compar- ison of their amino acid sequences with those of other ATPases revealed that archaebacterial ATPases are related more closely to V-type ATPases than FoF1-ATPases (13-22). V-type ATPase is a class of H’-ATPase found in eukaryotic endomembrane systems, such as chromaffin granules, Golgi apparatus, lysosomes, and plant vacuoles (23-36). However, it was recently found that the c (proteolipid)’ subunit of membranous sector of the S. acidocaldarius ATPase complex is more similar to that of F,,F1-ATPase than that of V-type ATPase (37,38). The implication of these relationships in the evolution of H+-ATPase/synthase, as well as in the origin of eukaryotic cells, has been lately discussed (37, 39, 40).

Here, we report the structure and sequence of the S. aci- docaldarius ATPase operon and compare them with those of other ATPases. The arrangement of genes and deduced amino acid sequences of the newly found genes in the S. acidocaldar- ius ATPase operon are totally different from those of FoF,- ATPase.

MATERIALS AND METHODS

Sequencing and Sequence Analysis of the ATPose Operon-The DNA fragment which we cloned for the first time contained the full- length operon (13). We have determined the nucleotide sequence of the atp operon by both strands. The method of sequencing and computer analysis of the gene have been described in our previous papers (13, 14,37,41).

Peptide Sequencing-The soluble S. acidocalderius ATPase was purified as described in our previous paper (7). Purified soluble S. &idocaldarius ATPase (250 $) was dissolved in a solution containing 4% sodium dodecvl sulfate, 12% crlvcerol (w/v). 50 mM Tris-Cl. aH 6.8, 2% mercaptoethanol (v/v), 661% bromphenol blue, heated at 100 “C for 3 min, and subjected to 13% polyacrylamide gel electro- phoresis in the presence of sodium dodecyl sulfate. Subunit bands of the S. acidocaldarius ATPase in an electrophoresed gel were electro- blotted using a transfer apparatus (ATTO, Tokyo). The transfer buffer contained 40 mM Tris, 240 mM glycine, 0.02% sodium dodecyl sulfate, and 20% (v/v) ethanol. Electroblotting onto polyvinylidene difluoride membrane (Immoblin, Millipore Inc., MA) was performed at 25 “C for 60 min. Blotted membrane was washed with distilled

’ The most hydrophobic subunit of F,FI-ATPase is called the 12 proteolipid subunit or c subunit. A homologous protein was isolated from S. acidocaldarius and we called it proteolipid subunit (37). However, we call it c subunit in this paper for convenience.

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Archaebacterial ATPase Operon

342 1779 1396 651 160 306

no 1 0 -4 -17 17

(6) a P y (e) c

FIG. 1. Arrangements of genes in the atp operon encoding ATPase subunits in S. acidocaldarius. The letters N, (3, y, and c indicate subunits of ATPase encoded in the genes A, B, G, and P, and the letters 6 and c show putative ATPase subunits encoded in the genes a&D and E.

water and stained with 0.5% Coomassie Brilliant Blue. Stained bands of the y and 6 subunits were cut out separately and applied directly on a gas-phase peptide sequencer (Applied Biosystems 470A). How- ever, the samples did not give readable sequence. In order to determine the internal peptide sequence, the subunit bands blotted on the membrane were cut out without staining and subjected to CNBr treatment (42). The pieces of membranes were placed in a 1.5-m] Eppendorf tube and 150 11 of 0.15 M CNBr in 70% formic acid (v/v) was added. The tube was incubated overnight in the dark at room temperature. The membrane pieces were separated from the solution and the solution was concentrated to 20 ~1. Both membrane pieces were separated from the solution and the solution was concentrated to 20 ~1. Both membrane pieces and the solutions were analyzed separately by a gas-phase peptide sequencer and only the solution obtained from the y subunit gave a readable sequence.

RESULTS AND DISCUSSION

Structure and Sequence of the Operon-The operon con- tained six genes, designated as atpD, A, B, G, E, and P, as shown in Fig. 1. There is no potential open reading frame which is immediately upstream of the 5’ end of atpD or downstream of the 3’ end of atpP. Consistently, preliminary results of Northern blot hybridization showed the presence of a 5-kilobase transcript which can cover the whole operon.” Fig. 2 shows nucleotide sequence of the operon and the deduced amino acid sequences. The molecular weights and amino acid compositions of the six encoded polypeptides are shown in Table I. Gene products of atpA, atpB, and atpP have been already identified as the cy, p, and c subunits of the S. acidocaldarius ATPase complex, respectively (13, 14,37), and their sequences are omitted from the figure. Gene products of atpD, atpG, and atpE, as well as those of atpA and atpB, are hydrophilic polypeptides as shown in Table I. Gene products of atpG and atpE are basic proteins and a product of atpG is a neutral one.

Soluble ATPase of S. acidocaldarius was at first reported to have three kinds of subunits, LY, & and y (7), but later the fourth subunit was found by Liibben et al. (8). We alsc found the fourth subunit, the 6 subunit, in our preparation.4 The estimated molecular weights of the y and 6 subunits were 28,000 and 12,000, respectively, from the mobility in sodium dodecyl sulfate-polyacrylamide gel electrophoresis (7, 8). These molecular weights are in good agreement with those estimated from the nucleotide sequences of genes atpG and atpD, respectively. The NH2-terminal amino acids of the y and 6 subunits are probably blocked since no significant amount of PTH amino acid was detected when they were analyzed with Edman degradation in a gas-phase sequencer. CNBr cleavage of the blotted membranes was effective to obtain an internal peptide of the y subunit of which sequence was found in the deduced amino acid sequence of the atpG gene (Fig. 2, underlined sequence). atpG is thus identified as a gene for the y subunit. However, the same procedure was not effective for the 6 subunit and no internal sequence has

” K. Denda and T. Date, unpublished observations. ‘J. Konishi and K. Hajiro, unpublished observations.

FIG. 2. Nucleotide sequence of the S. acidocaldarius atp operon and nearby region. The sequences from R&II to EcoRV restriction sites are shown. The sequences of atpA, R, and P were already shown in the previous reports (13, 14, 37) and omitted from the figure. Potential ribosome-binding sites and initiation codons are both ouer- and underlined. The potential transcriptional termination signal is indicated by dots above and below the nucleotide sequence. The peptide sequence confirmed by a gas-phase peptide sequenator is underlined.

been obtained. Attempts to isolate the 6 subunit using a reverse-phase high performance liquid chromatography were unsuccessful. Therefore, we tentatively assume that atpD is the gene encoding the 6 subunit, but further study is necessary to prove that its product is the 6 subunit. Any candidate of the product of atpE has not been found in our preparation of the purified soluble ATPase. It is possible that this small

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Archaebacterial ATPase Operon 21511

TABLE I Amino acid compositions of proteins encoded by the atp operon

Protein Amino acid

a B 7 6 L c

Hydrophobic residues GUY 44 42 7 5 1 15 Ala 40 34 9 2 0 17 Val 60 27 16 7 1 7 Leu 52 46 27 6 9 14 Ile 41 38 19 17 6 10 Met 13 14 4 1 2 4 Phe 17 18 4 4 0 8 Trp 10 1 0 1 0 1 Pro 39 24 8 2 0 3

Neutral residues Ser 33 30 19 12 4 2 Thr 24 25 10 3 2 5 Asn 17 21 9 4 4 1 Gln 16 11 7 3 3 2 GYS 1 1 0 2 0 0

Hydrophilic residues Asp 38 24 7 11 4 2 Glu 44 37 20 8 7 3 LYS 40 23 18 17 13 3 His 5 4 0 0 0 0 Arg 36 28 20 2 1 2 Tyr 21 17 12 6 2 2

No. of residues 591 465 216 113 59 101

M* 66,009 51,246 25,104 13,006 7,038 10,362

(a) S. acidocaldarius :

(b) E. co/i :

(c) Synechococcus :

(d) Chloroplasts :

(4 Rsp. rubrum :

6 a B 7

FIG. 3. Arrangements of genes encoding ATP synthase/ATPase subunits in S. acidocaldarius (a), E. coli (b), Synechococcus 6301 (c), spinach chloroplast (d), and Rhodospirirum rubrum (e). The letters a, b, c, 01, p, y, 6 and 6 represent subunits encoded in the gene. The genes encoding hydrophobic subunits are .&o&d. Chloroplast b contains an intron (57). The dashed line signifies that the genes are at least 15 kilobases apart and are separately transcribed.

polypeptide is a subunit of the soluble ATPase, tentatively named as the t subunit, which is easily dissociated from the soluble ATPase during purification. Similar subunit loss dur- ing purification has been observed for some of Fis (43-45). If the product of a&E is, in fact, a subunit of the soluble ATPase, then, the intact soluble ATPase of S. acidocaldariu.s is com- prised of five kinds of subunits, the (Y, 0, y, 6, and c subunits, similar to F1.

It was already shown that the major two subunits, the (Y and fl subunits, of the S. ucidoculdurius ATPase are homo-

logues of the 70- and 60-kDa subunits of the V-type ATPase, respectively, and that the c subunit of the S. ucidoculdurius ATPase complex is a homologue of the c subunit of FoFI- ATPase and a 16-kDa hydrophobic subunit of the V-type ATPase (37,38). However, the amino acid sequences of the y subunit and two other putative subunits of S. ucidoculdurius ATPase deduced from the nucleotide sequence of utpG, D, and E genes do not have significant sequence similarity to any of subunits of V-type ATPases and FoF1-ATPases (46, 47). Their hydropathy profiles do not show apparent similar-

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21512 Archaebacterial ATPase Operon

ity to those of any subunits of V-type ATPases and FoFI- ATPases, either (data not shown). Furthermore, a search through the NBRF database did not detect any significantly similar sequences.

Putative Initiation, Termination, and Ribosome Binding Sequences-AT-rich consensus base sequences of promoter regions have been speculated for archaebacterial genes (48- 50). However, since sequence conservation at speculated pro- moter regions is not always strict and only a few protein- coding S. acidocaldarius genes have been identified, it seems premature to speculate about the location of the promoter region of this operon (51-55). Complementary sequences (GAGGTGAT) to the 3’ termini of 16 S rRNA from the same genus S. solfataricus or its similar sequences are found at several nucleotides upstream of initiation ATG of each gene of the operon as indicated by the over- and underlined se- quences in Fig. 2. They might be the ribosome-binding sites. The intercistronic non-coding regions in S. acidocaldarius atp operon are extremely short and even gene overlappings are observed between genes P/-r and y/c. The intergenic region between atpE and atpP (17 base pairs) is the longest. A comparison of transcription termination sites so far deter- mined for archaebacterial operons reveals a common, readily distinguishable archaebacterial signal, which is a T-rich se- quence (56). A similar sequence, hence a candidate for tran- scription termination site of atp operon, was found at the 14 base pair downstream of the stop codon of the c subunit gene. In preliminary experiments, a new 2-kilobase transcript was detected when a DNA fragment corresponding to the down- stream region of the c subunit gene was used as a probe for Northern blot hybridization.3 This indicates that atp operon ends after the c subunit gene and then another operon starts.

Comparison of the Structure of the Operon with Fzl-ATP- ase Operons-Since the S. acidocaldarius ATPase operon is the first example of an archaebacterial ATPase in which the whole sequence has been determined, it is interesting to compare the arrangement of the genes in the operon with that of FOF1-ATPase operon. One of the characteristics of the arrangement of genes in the F,,F,-ATPase operon is that genes for hydrophobic F0 subunits precede genes for hydrophilic F1 subunits (Fig. 3). This feature of gene arrangement in the FOF,-ATPase operon has been typically observed in FoF1- ATPase operons of E. coli and a thermophilic bacterium PS3. F,,F1-ATPase operons of two cyanobacteria, Synechococcus 6301 and Synechococcus 6716, and spinach chloroplast also retain this feature even though some of subunits are encoded in a second operon (57, 58). On the other hand, five genes, atpD, A, B, G, and E, encoding hydrophilic polypeptides in the ATPase operon of S. acidocaldarius precede a gene, atpP, encoding a very hydrophobic c subunit. Thus, the order of genes encoding hydrophobic and hydrophilic polypeptides in the operon of S. acidocaldarius ATPase is the reverse of that in the FOF,-ATPase operon.

Another feature of the operon of S. acklocaldarius ATPase is that there is only one gene which encodes a hydrophobic polypeptide, the c subunit. Here, two possibilities may be pointed out. The first possibility is that the operon contains all of the genes of the whole ATPase complex and the c subunit alone constitutes a H+ channeling membrane sector. The second possibility is that the genes related to a H’ channeling membrane sector are split into two (or more) independent operons and some hydrophobic subunits other than c are encoded in other operon(s) as observed for a purple non-sulfur photobacterium Rhodospirirum rubrum in which the F. and F1 subunits are encoded by two separately tran- scribed gene clusters (59, 60). Since attempts to isolate whole

ATPase complex consisting of a membrane sector and a soluble ATPase from S. acidocaldarius membranes with good yield have been unsuccessful and the precise subunit organi- zation of the ATPase has not been known, judgment of the above two possibilities should await further study.

Acknowledgmenrs-We thank M. Sumi and Dr. M. Ishida for preparation of figures. We are also grateful to Dr. T. Tanaka and M. Kawata, Mitsubishi Kasei Institute of Life Science. and Drs. Y. Shoii- Kobayashi and N. Enomoto, Kanazawa Medical University, for their helpful discussions. We also thank our colleague, Dr. F. Arisaka, for a critical review of the manuscript.

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K Denda, J Konishi, K Hajiro, T Oshima, T Date and M YoshidaSulfolobus acidocaldarius.

Structure of an ATPase operon of an acidothermophilic archaebacterium,

1990, 265:21509-21513.J. Biol. Chem. 

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