©1995 by The American Society for Biochemistry and Molecular Biology, Inc.
Thermophilic Bacilli Have Split Cytochrome b Genes for Cytochrome b and Subunit IV
FIRST CLONING OF CYTOCHROME b FROM A GRAM-POSITIVE BACTERIUM ( BACILLUS STEAROTHERMOPHILUS) (*)

Nobuhito Sone (§) , Go Sawa , Takefumi Sone (¶) , Shunsuke Noguchi

From the (1) Department of Biochemical Engineering and Science, Kyushu Institute of Technology, Iizuka, Fukuoka-ken 820, Japan

ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS AND DISCUSSION
FOOTNOTES
ACKNOWLEDGEMENTS
REFERENCES

ABSTRACT

The genes of Bacillus stearothermophilus K1041 encoding cytochrome b( Bacillus cytochrome b is referred to as cytochrome bfor its resemblance to plastid b) and subunit IV of the quinol:cytochrome c oxidoreductase ( bc complex) were cloned and sequenced. For preparation of the probe for cloning, polymerase chain reaction was carried out using oligonucleotide mixtures targeting for N-terminal regions of cytochrome bc and subunit IV of the thermophilic Bacillus PS3. The deduced amino acid sequences contained 224 residues of 25,425 daltons for cytochrome band 173 residues of 19,371 daltons for subunit IV, and both open reading frames were separated by 67 base pairs. Cytochrome b and subunit IV contained 4 and 3 hydrophobic transmembrane segments, respectively, indicating that the fourth segment of subunit IV (eighth segment of cytochrome b) is lacking. Four histidine residues supposed to ligand two protohemes were conserved, but the two His in the fourth segment were separated by 14 amino acid residues like cytochrome b, not like mitochondrial cytochrome b. The residues that might have conferred the two quinol-binding sites were mostly conserved, but especially the third His residue in the fourth segment of mitochondrial cytochrome b was replaced by Arg in Bacillus cytochrome b as in cytochrome b. These characteristics and quantitative comparison of the protein sequences indicate that this Bacillus sequence is unique and meanwhile rather close to the cyanobacteria-plastids type than the purple bacteria-mitochondria type.


INTRODUCTION

Cytochrome b is the central catalytic subunit of ubiquinol:cytochrome c oxidoreductase (or bc complex) in the respiratory chain of mitochondria and aerobic bacteria (1, 2, 3) . A similar cytochrome named cytochrome b is known to be present in the homologous b f complex of the photosynthetic electron transfer chain of cyanobacteria and chloroplasts (3, 4, 5) . The cytochromes b/ b are transmembrane proteins containing two protohemes responsible for vectorial electron transfer. The molecular mass of cyanobacterial and chloroplast cytochrome b determined by SDS-PAGE() (20-22 kDa) was much smaller than the mitochondrial and purple bacterial ones (34-40 kDa) (3, 4) , but this is due to the fact that the C-terminal half of the cytochrome b is translated separately in chloroplast and cyanobacteria (6) , which is named subunit IV (3) . The gene for cytochrome b ( petB) is terminated at the downstream of the fourth transmembrane segment (between helix D and E, in cytochrome b), and the gene for subunit IV ( petD) composed of three helices (equivalent for E, F, and G of cytochrome b) sits downstream of the gene for cytochrome b, indicating that cytochrome b plus subunit IV is equivalent to mitochondrial cytochrome b(2, 3, 4) .

In contrast to the respiratory chain of Gram-negative bacteria, little is known about that of Gram-positive bacteria. 1) Thermophilic Bacillus PS3 contains both four-subunit cytochrome c oxidase and four-subunit bc complex forming a menaquinol-oxidizing respiratory chain (8, 9, 10) . 2) Bacillus subtilis(11, 12, 13) and Bacillus cereus(14) grown under regular conditions use quinol oxidases containing cytochrome aa-600 and Cu instead of cytochrome c oxidase, while any cytochrome bc- b f complex has not been reported (13) . The thermophilic Bacillus bc complex is composed of 29-kDa cytochrome c 23-kDa Rieske iron-sulfur protein, 21-kDa cytochrome b, and 14-kDa subunit IV (9) . The absorption spectrum of PS3 ferrocytochrome c has a shoulder at 548 nm in addition to the peak at 553 nm like cytochrome f, and two protohemes in 21-kDa cytochrome bshows very similar absorption maxima, not like mitochondrial cytochromes b-562 and b-566 (9) . These characteristics suggest that quinol:cytochrome c oxidoreductase of Gram-positive bacteria is rather similar to cytochrome b f complex. The history of a living creature and protein molecule may be written in DNA, and the gene for quinol reductase of a thermophilic Bacillus may contribute elucidation of the role of quinol reductase in mesophilic Bacillus having quinol oxidase (cytochrome aa-600).

We succeeded to clone the genes for cytochrome band subunit IV of Bacillusstearothermophilus K1041 using PCR. This is the first report of the gene structure and the deduced protein sequence of the genes for the cytochrome b of Gram-positive bacteria. Comparison of the protein sequence indicates closer similarity to cyanobacterial and plastid cytochrome brather than to those of purple bacteria and mitochondria, as well as several unique characteristics.


EXPERIMENTAL PROCEDURES

Materials

T4-DNA ligase, Klenow fragment, DNA polymerase of Thermusaquaticus ( Taq polymerase), restriction enzymes, plasmid vectors pUC18 and pUC19, and M13 bacteriophages mp18 and mp19 were obtained from Takara Shuzo Co. (Kyoto, Japan). [-P]dCTP and Hybond N (nylon membranes for DNA blotting) were purchased from Amersham Corp. Butyl-toyopearl (butylfractogel) was a product of Tosoh Co. (Tokyo). Cytochrome bc complex from the thermophilic Bacillus PS3 was prepared as previously described (9) . Separation of each subunit of the complex was carried out by SDS-PAGE (15) .

Molecular Cloning

The methods used for molecular cloning were based on those of Maniatis et al.(16) . Purified genomic DNA of B. stearothermophilus K1041 was partially digested with Sau3AI, fractionated by gradient centrifugation, and ligated to the BamHI site of the vector EMBL-3. This library was screened using the probe containing the gene for cytochrome b of Bacillus PS3 under the hybridization condition at 55 °C in 5 SSC. This PS3 gene was prepared by cloning the PCR product synthesized with the sense [5`-TGGCG(A/C/G/T)GA(C/T)AT(A/C/T)GC(A/G/C/T)GA] and antisense oligonucleotides [5`-CA(A/G)TT(C/T)TC(A/G)AA(C/T)TTCAT] as the primers (Fig. 1) and PS3 DNA as the template. These primers are targeted against N-terminal peptides of PS3 cytoochrome band subunit IV, respectively, although these oligonucleotides are not completely redundant (see for the codon usage). The PCR was performed according to the manufacturer's protocol in a thermal cycler (Perkin-Elmer Corp.) with PS3 DNA (1 ng). A combination of 94, 45, and 72 °C (2 min each) was repeated 25 times. The PCR product was centrifuged in a cup of a Centricon (Amicon, Beverly, MA) to remove primers and mononucleotides, dephosphorylated by calf intestine alkaline phosphatase (2 µg), and ligated to the M13 mp19 vector cleaved with SmaI. One clone in M13 ( bc15) contained the sense primer site but no antisense primer site, and the deduced amino acid sequence showed that the cloned gene really encoded the cytochrome bprotein composed of 230 amino acid residues, including four conserved histidines as ligands for the hemes.


Figure 1: Sequence strategy and a map of B. stearothermophilus chromosome in the region encoding cytochrome b and subunit IV. The area subcloned, from SalI (the 5`-end of the EMBL3) to EcoRI and its vicinity, is shown.



Sequencing of DNA and Peptide

Nucleotide sequencing was carried out by the chain termination method (17) using [-P]dCTP. Peptide sequences were determined by the Edman degradation method using an Applied Biosystems model 473A gas-phase sequencer with specimen transferred to polyvinylidene fluoride membrane after SDS-PAGE. The sequence data were analyzed with a software program (GENETYX 2.0.0).


RESULTS AND DISCUSSION

Cloning of B. stearothermophilus Genes Encoding Cytochrome b + Subunit IV

The N-terminal protein sequences of cytochrome b and subunit IV of cytochrome bc1 complex from the thermophilic Bacillus PS3 were analyzed to be MLNKLYDWVDERLDITPLWRDIADHE- and MKFENTGL-, respectively. We then prepared oligonucleotides as primers, expecting that the structure gene for subunit IV may sit after the gene for cytochrome bas in the operon of cytochrome b f complexes in chloroplast and cyanobacteria (7) . PCR with the sense and antisense primers in the presence of total PS3 DNA produced a DNA of about 700 base pairs.

Most of this DNA was cloned in M13 phage, and the clone was named bc15. Using this bc15 as the probe, about 10,000 recombinants of the B. stearothermophilus K1041 library in EMBL-3 were screened. Only one plaque was truly positive to hybridize with the probe. The DNA prepared from the phage lysate infected with this plaque and cut by restriction enzymes showed that 4 kilobase pairs ( SalI cut) and 1.6 kilobase pairs ( SalI and EcoRI double cut) fragments hybridized the probe. This 1.6-kilobase pair fragment was subcloned into pUC119 and sequenced. Fig. 1 shows the map of the genes coding for cytochrome band subunit IV of the bc complex and the sequence strategy.

DNA and Amino Acid Sequences

Fig. 2 shows the DNA and deduced amino acid sequences of this SalI- EcoRI fragment from B. stearothermophilus K1041. The open reading frame for cytochrome b consists of 672 bases, and the deduced protein is composed of 224 amino acid residues having 25,425 Da. Likewise, the open reading frame for subunit IV starts at position 934 and terminates with TGA at position 1447, coding 173 amino acid residues of 19,371 Da. These values are higher than the apparent molecular masses of 21 kDa for PS3 cytochrome c and 14 kDa for the subunit IV estimated from SDS-PAGE (8) . However, this kind of discrepancy is often observed for highly hydrophobic membrane proteins as is also observed in subunits of cytochrome c oxidase. The amino acid sequence of the N-terminal region of PS3 cytochrome b coincides with the DNA sequence reading from the initiation codon at position 191, indicating that no processing occurs at the N-terminal region. The N-terminal MKF was shown with peptide sequencing of PS3 subunit IV. The sequences at C-terminal region has not been confirmed. The two structure genes are separated by a relatively long nucleotide sequence composed of 68 bases, although neither terminator nor promotor structure is found, and thus the gene for cytochrome b and subunit IV seems to form an operon. A promotor-like structure ( dotted in Fig. 2) is present in the 5`-upstream region of the gene for cytochrome b, but we have not found a terminator structure in 3`-downstream region of the figure after the stop codon for subunit IV.


Figure 2: DNA and deduced amino acid sequences of B. stearothermophilus b and subunit IV. The putative Shine-Dalgarno sequences are boxed. The nucleotides that may constitute the putative promotor region are dotted.



Structure of Cytochrome b

Fig. 3 shows the hydropathy plots of cytochrome band subunit IV. The hydrophobicity of the segment marked ``IV'' was not so strong in B. stearothermophilus cytochrome b, and this segment might sit on the surface of the lipid bilayer or membrane protein as claimed by Rao and Argos (18) and Croft et al.(19) . On the contrary, the numbers of hydrophobic segments of subunit IV are three as in subunits IV of cyanobacteria and plastids (2, 3, 7) . It is thus likely that total numbers of membrane-spanning hydrophobic segments of cytochrome b+ subunit IV are seven as in the cyanobacteria and plastids and not eight as in cytochromes b of purple bacteria and mitochondria.


Figure 3: Hydropathy profile of cytochrome b and subunit IV of B. stearothermophilus. The procedure of Kyte and Doolittle (41) was used for calculation with a window of 17 residues.



Fig. 4 shows the alignment of B. stearothermophilus sequences of cytochrome band subunit IV with the corresponding sequences of four typical groups, mitochondrial b, purple bacterial b, cyanobacterial b + IV, and chloroplast b + IV. Four heme-binding histidine residues are conserved: two His residues, respectively, in segments B and D in a pairwise fashion. Two His residues in segment D are separated by 14 residues as in cytochrome b instead of 13 in cytochrome b. Cytochrome b ( b + IV) is the catalytic subunit of the bc complex playing central roles for vectorial oxidation of quinol. The Q-cycle mechanism, originally proposed by P. Mitchell (20) , is now crucially supported by several experiments (21, 22) . The mechanism needs for cytochrome b ( b + IV) to possess two hemes and two quinone-binding sites (2, 3, 4, 5) . Four histidine residues are conserved: two each in hydrophobic segments B and D as marked (&cjs1372;). The quinol-oxidizing (Qo) site sits close to outside of the cytoplasmic membrane and is known to be susceptible to myxothiazol and 2-alkyl-4-hydroxyquinoline N-oxide, while the quinone-reducing (Qi) site close to cytoplasm is known to be antimycin A-sensitive and to possess a stabilized semiquinone in the mitochondrial and purple bacterial complexes (2, 23) . The Bacillus enzyme was insensitive to antimycin A as cytochrome b f complexes (9) , indicating that the Qi sites of these complexes are somewhat different from that of the mitochondrial bc complex. In fact, His-202 in the yeast cytochrome b just after the fourth His residue in segment D was replaced by Arg in the thermophilic bacilli as in Nostoc and maiza plastid sequences. An important role of His-217 as a residue conferring Qi site was reported with the Rhodobacter capsulatus enzyme (24) . On the contrary, the Bacillus enzyme is susceptible to 2-alkyl-4-hydroxyquinoline N-oxide and myxothiazol, which is consistent with the present finding that the several residues in the loop cd as well as -PEWY- and -LR- in the loop ef of subunit IV are also conserved in the thermophilic Bacillus as in cytochrome b and subunit IV.


Figure 4: Multiple alignment of cytochrome b/ b + subunit IV. Identical or conserved (L = I = V, K = R, D = E, Q = N) residues among cytochrome b or b + IV are boxed. Identical and conserved residues among all cytochrome b/ b + IV are indicated by asterisks on the top and are also boxed. 1, yeast Saccharomyces cerevisiae cytochrome b (41); 2, Rhodopseudomonas viridis cytochrome b (42); 3, B. stearothermophilus cytochrome b (present work); 4, Nostoc PCC7906 cytochrome b (7); 5, maiza chloroplast cytochrome b (43). The alignment starts at the 1st ( 1), 13th ( 2), and 4th ( 3-5) amino acid residues.



It is also generally confirmed that the amino acid sequences of Bacillus are mostly in common with those of the b group, and only a few are in common with cytochrome b group, as shown in Fig. 4 . gives percentage identities for the cytochrome b sequences. B. stearothermophilus cytochrome bis more similar to Nostoc b and maiza plastid b than the corresponding Rhodopseudomonas viridis and yeast mitochondrial sequences (A). The same tendency was also observed in subunit IV (B), but the similarity of Bacillus subunit IV to cyanobacterial and plastid subunit IV was not so high as the former. Thus, the comparison of the percentage identity shows closeness of the Bacillus cytochrome b to those of cyanobacterial and plastidal counterparts rather than to the mitochondria-purple bacteria group, although it is different from the other four groups.

Characteristics of Bacillus Cytochrome b + IV

Purified cytochrome bc complex from the thermophilic Bacillus PS3 showed that its cytochrome bwas rather small (21 kDa by SDS-PAGE) and contained the fourth subunit (9) . Bacillus cytochrome bcontained two protohemes showing similar values of E and absorption maxima of the band (9) like plastid cytochrome b. The present result of cloning and sequencing of the genes for the thermophilic Bacillus enzyme is in accord with the above protein characterization. 1) The open reading frame for Bacillus cytochrome bencodes 224 residues, and the initiation codon for subunit IV (173 residues) is separated by 67 base pairs. 2) The third hydrophobic segment in subunit IV (segment H) is lacking in Bacillus subunit IV. 3) Two His residues in Bacillus segment D are separated by 14 amino acid residues as in cyanobacterial and plastid enzymes, not 13 residues as in mitochondrial and purple bacterial counterparts. 4) Arg residue is present in the Bacillus enzyme as in cyanobacteria cytochrome b but not His-202 as in yeast cytochrome b, which is supposed to confer inhibitor sensitivity on the Qi site (24) . This difference may explain the inhibitor sensitivity. 5) Lys-228 conserved among antimycin-susceptible cytochrome b is replaced by Asn as in cytochrome b. The K228I mutant of yeast was shown to be antimycin A resistant (7, 25) .

The conclusion that Bacillus cytochrome bc ( b f) complex is not so similar to purple bacterial-mitochondrial enzyme and rather close to cyanobacterial enzyme is in accord with the case of cytochrome c oxidase; the cta operons of Bacillus PS3 (26, 27) , B. subtilis(28) , Bacillus firmus(29) , and Synechococcus vulcanus(30, 31) encode subunit II (2) -I (14) -III (5) , whereas the operons of purple bacteria such as of Paracoccus denitrificans(32) and Rhodopseudomonas sphaeroides(33) encode subunit II (2) -I (12) -III (7) . The numbers in parentheses are the numbers of hydrophobic segments. This difference may be explained by assuming that the places of the stop codon of subunit I are different in the two groups (34) . It is also noteworthy that analyses of 16 S rRNA showed a close relationship between Gram-positive bacteria and cyanobacteria (35) .

Use of B. stearothermophilus K1041

In this work, we used B. stearothermophilus K1041, which was recently isolated from soil and shown to be transformable by electroporation (36, 37) . The bacterium grows up to 65 °C. The doubling time in the complex medium is about 15 min. The thermophilic Bacillus PS3 separated from a hot spring in Japan and able to grow up to 75 °C is also similar to B. stearothermophilus. The present data (Fig. 2) indicate that their differences in DNA and amino acid sequences of cytochrome bare minor; only 62 bases and 8 amino acids are replaced out of 620 bases (corresponding to nucleotides 245-864 in Fig. 2) and 206 amino acids. The amino acid replacements are caused by three single-base changes and five double-base changes, while 49 base changes do not affect the amino acid sequence.

Codon Usage of the Thermophilic Bacilli

gives the codon usage in cytochromes b of B. stearothermophilus and the thermophilic Bacillus PS3. The latter is a partial sequence due to PCR. Its sequence has been previously reported (38) , and the protein sequence has been aligned (4) . The codon usage of both bacteria is very similar. There is a tendency for G or C to be preferentially chosen at the third position of four-codon-using amino acids such as Gly, Ala, Val, Thr, and Pro, as we have observed in the PS3 genes for cytochrome c oxidase (27) and H-ATP synthase (39) . This tendency may be a little milder in K1041 than in PS3; K1041 does not use GGC for Gly so frequently as PS3. Tolner et al. (40) , however, reported a preference for A/T over G/C in the third letter of genes encoding Na/H-coupled L-glutamate symport proteins of B. stearothermophilus ATCC 7954 and Bacillus caldotenax.

Conclusion and Perspectives

This is the first report of the cloning and sequencing of the genes for cytochrome b ( bplus subunit IV) of cytochrome c reductase of Gram-positive bacteria. The structure and sequence homologies of the genes indicate they are similar to those of cyanobacteria rather than to those of purple bacteria and mitochondria. The gene seems useful to clarify the presence and roles of cytochrome b ( bplus subunit IV) in mesophilic Bacilli such as B. subtilis, in which the presence of cytochrome band cytochrome c reductase was postulated (13) , but nothing has been known about it probably because of its rare presence due to the fact that quinol oxidase (cytochrome aa-600) is mainly working in the B. subtilis respiratory chain (11, 12) .

  
Table: Comparative matrices for cytochrome b/b + IV proteins


  
Table: Comparison of codon usage of the cytochrome b gene of B. stearothermophilus K1041 with that of PS3

The PS3 gene lacks 54 base pairs for the N-terminal region (see Fig. 2), and thus total amino acid numbers are 223 in the K1041 gene and 205 in the PS3 gene. The codon usage number is shown as K1041/PS3.



FOOTNOTES

*
This work was supported in part by Grants-in-Aid for Scientific Research 02454546 and 04266217 from the Ministry of Education, Science, and Culture of Japan (to N. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore by hereby marked `` advertisement'' 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 GenBank/EMBL Data Bank with accession number(s) D45410.

§
To whom correspondence should be addressed. Tel.: 81-948-297813; Fax: 81-948-297801.

Present address: Dept. of Agricultural Chemistry, Faculty of Agriculture, Kyoto University, Japan.

The abbreviations used are: PAGE, polyacrylamide gel electrophoresis; PCR, polymerase chain reaction; Qi site, quinone-reducing site.


ACKNOWLEDGEMENTS

We thank Mie Shugyo for skillful technical assistance.


REFERENCES
  1. Trumpower, B. L. (1990) J. Biol. Chem. 265, 11409-11412 [Free Full Text]
  2. Trumpower, B. L. (199O) Microbiol. Rev. 554, 101-129
  3. Hauska, G., Nitschke, W., and Herrmann, R. G. (1988) J. Bioenerg. Biomembr. 20, 211-228 [Medline] [Order article via Infotrieve]
  4. Degli Esposti, M., De Vries, S., Crimi, M., Ghelli, A., Patarnello, T., and Meyer, A. (1993) Biochim. Biophys. Acta 1143, 243-271 [Medline] [Order article via Infotrieve]
  5. Trumpower, B. L., and Gennis, R. B. (1994) Annu. Rev. Biochem. 63, 675-716 [CrossRef][Medline] [Order article via Infotrieve]
  6. Widger, W. R., Cramer, W. A., Herrmann, R. G., and Trebst, A. (1984) Proc. Natl. Acad. Sci. U. S. A. 81, 674-678 [Abstract]
  7. Kallas, T., Spiller, S., and Malkin, R. (1988) J. Biol. Chem. 263, 14334-14342 [Abstract/Free Full Text]
  8. Sone, N., Sekimachi, M., and Kutoh, E. (1987) J. Biol. Chem. 262, 15386-15391 [Abstract/Free Full Text]
  9. Kutoh, E., and Sone, N. (1988) J. Biol. Chem. 263, 9020-9026 [Abstract/Free Full Text]
  10. Sone, N., and Fujiwara, Y. (1991) J. Biochem. 110, 1016-1021 [Abstract]
  11. Lauraeus, M., Haltia, T., Saraste, M., and Wikstrom, M. (1991) Eur. J. Biochem. 197, 699-705 [Abstract]
  12. Santana, M., Kunst, F., Hullo, M. F., Rapoport, G., Danchin, A., and Glaser, P. (1992) J. Biol. Chem. 267, 10225-10231 [Abstract/Free Full Text]
  13. Von Wachenfeldt, C., and Hederstedt, L. (1990) FEMS Microbiol. Lett. 100, 91-100
  14. Garcia-Horsman, J. A., Barquera, B., Gonzalez-Halphen, D., and Escamilla, J. E. (1991) Mol. Microbiol. 5, 197-205 [Medline] [Order article via Infotrieve]
  15. Laemmli, U. K. (1970) Nature 277, 680-685
  16. Maniatis, T., Fritsch, E. F., and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
  17. Sanger, F., Nicklen, S., and Coulson, A. R. (1977) Proc. Natl. Acad. Sci. U. S. A. 74, 5463-5467 [Abstract]
  18. Rao, J. K. M., and Argos, P. (1986) Biochim. Biophys. Acta 869, 197-214 [Medline] [Order article via Infotrieve]
  19. Croft, A., Robinson, H., Andrews, K., Von Doren, S., and Berry, E. (1987) in Cytochrome Systems (Papa, S., Chance, B., and Ernster, L., eds) pp. 617-624, Plenum Press, New York
  20. Mitchell, P. (1975) J. Theor. Biol. 62, 327-367
  21. Croft, A., Meinhardt, S. W., Jones, K. R., and Snozzi, M. (1983) Biochim. Biophys. Acta 723, 202-218
  22. Yang, X., and Trumpower, B. L. (1988) J. Biol. Chem. 12282-12289
  23. Robertson, D. E., Daldal, F., and Dutton, P. L. (1990) Biochemistry 29, 11249-11260 [Medline] [Order article via Infotrieve]
  24. Gray, K. A., Dutton, P. L., and Daldal, F. (1994) Biochemistry 33, 723-733 [Medline] [Order article via Infotrieve]
  25. Howell, N., and Gilbert, K. (1989) J. Mol. Biol. 203, 607-618
  26. Sone, N., Yokoi, F., Fu, T., Ohta, S., Metso, T., Raitio, M., and Ishizuka, M. (1988) J. Biochem. ( Tokyo) 103, 606-610 [Abstract]
  27. Ishizuka, M., Machida, K., Shimada, S., Mogi, A., Tsuchiya, T., Ohmori, T., Souma, Y., Gonda, M., and Sone, N. (1990) J. Biochem. ( Tokyo) 108, 866-873 [Abstract]
  28. Saraste, M., Metso, T., Nakari, T., Jalli, T., Lauraeus, M., and van der Ost, J. (1991) Eur. J. Biochem. 195, 517-525 [Abstract]
  29. Quirk, P. G., Hicks, D. B., and Krulwich, T. A. (1993) J. Biol. Chem. 268, 678-685 [Abstract/Free Full Text]
  30. Tano, H., Ishizuka, M., and Sone, N. (1991) Biochem. Biophys. Res. Commun. 181, 437-442 [Medline] [Order article via Infotrieve]
  31. Sone, N., Tano, H., and Ishizuka, M. (1993) Biochim. Biophys. Acta 1183, 130-138 [Medline] [Order article via Infotrieve]
  32. Raitio, M., Jalli, T., and Saraste, M. (1987) EMBO J. 6, 2825-2833
  33. Cao, J., Hosler, J., Shapleigh, J., Revzin, A., and Ferguson-Miller, S. (1992) J. Biol. Chem. 267, 24273-24278 [Abstract/Free Full Text]
  34. Saraste, M. (1990) Q. Rev. Biophys. 23, 331-366 [Medline] [Order article via Infotrieve]
  35. Woese, C. R. (1987) Microbiol. Rev. 51, 221-271
  36. Narumi, I., Sawakami, K., Nakamoto, S., Nakayama, N., Yanagisawa, T., Takahashi, N., and Kihara, H. (1992) Bio/Technology 6, 83-86
  37. Nakayama, N., Narumi, I., Nakamoto, S., and Kihara, H. (1992) Bio/Technology Lett. 14, 649-652
  38. Sone, N., and Sone, T. (1991) Seikagaku ( Japanese) 63, 873 (abstr.)
  39. Ohta, S., Yohda, M., Ishizuka, M., Hirata, H., Hamamoto, T., Otawara-Hamamoto, Y., Matsuda, K., and Kagawa, Y. (1988) Biochim. Biophys. Acta 933, 141-155 [Medline] [Order article via Infotrieve]
  40. Tolner, B., Poolman, B., and Konings, W. N. (1992) Mol. Microbiol. 6, 2845-2856 [Medline] [Order article via Infotrieve]
  41. Kyte, J., and Doolittle, R. F. (1982) J. Mol. Biol. 151, 389-409
  42. Nobrega, F. G., and Tzagoloff, A. (1980) J. Biol. Chem. 255, 9828-9837 [Abstract/Free Full Text]
  43. Verbis, J., Lang, F., Gabellini, N., and Oesterhelt, D. (1989) Mol. & Gen. Genet. 219, 445-452
  44. Rock, C. D., Barkan, A., and Taylor, W. L. (1987) Curr. Genet. 12, 69-77 [Medline] [Order article via Infotrieve]

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