CO2-responsive Expression and Gene Organization of Three Ribulose-1,5-bisphosphate Carboxylase/oxygenase Enzymes and Carboxysomes in Hydrogenovibrio Marinus Strain MH-110

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 2004 Aug 20

PMID 15317772

Citations 29

Authors

Yoichi Yoshizawa

Koichi Toyoda

Hiroyuki Arai

Masaharu Ishii

Yasuo Igarashi

Affiliations

Soon will be listed here.

Abstract

Hydrogenovibrio marinus strain MH-110, an obligately lithoautotrophic hydrogen-oxidizing bacterium, fixes CO2 by the Calvin-Benson-Bassham cycle. Strain MH-110 possesses three different sets of genes for ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO): CbbLS-1 and CbbLS-2, which belong to form I (L8S8), and CbbM, which belongs to form II (Lx). In this paper, we report that the genes for CbbLS-1 (cbbLS-1) and CbbM (cbbM) are both followed by the cbbQO genes and preceded by the cbbR genes encoding LysR-type regulators. In contrast, the gene for CbbLS-2 (cbbLS-2) is followed by genes encoding carboxysome shell peptides. We also characterized the three RubisCOs in vivo by examining their expression profiles in environments with different CO2 availabilities. Immunoblot analyses revealed that when strain MH-110 was cultivated in 15% CO2, only the form II RubisCO, CbbM, was expressed. When strain MH-110 was cultivated in 2% CO2, CbbLS-1 was expressed in addition to CbbM. In the 0.15% CO2 culture, the expression of CbbM decreased and that of CbbLS-1 disappeared, and CbbLS-2 was expressed. In the atmospheric CO2 concentration of approximately 0.03%, all three RubisCOs were expressed. Transcriptional analyses of mRNA by reverse transcription-PCR showed that the regulation was at the transcriptional level. Electron microscopic observation of MH-110 cells revealed the formation of carboxysomes in the 0.15% CO2 concentration. The results obtained here indicate that strain MH-110 adapts well to various CO2 concentrations by using different types of RubisCO enzymes.

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References

Baker S, Jin S, Aldrich H, Howard G, Shively J . Insertion mutation of the form I cbbL gene encoding ribulose bisphosphate carboxylase/oxygenase (RuBisCO) in Thiobacillus neapolitanus results in expression of form II RuBisCO, loss of carboxysomes, and an increased CO2 requirement for growth. J Bacteriol. 1998; 180(16):4133-9. PMC: 107408. DOI: 10.1128/JB.180.16.4133-4139.1998. View

Nishihara H, Yaguchi T, Chung S, Suzuki K, Yanagi M, Yamasato K . Phylogenetic position of an obligately chemoautotrophic, marine hydrogen-oxidizing bacterium, Hydrogenovibrio marinus, on the basis of 16S rRNA gene sequences and two form I RuBisCO gene sequences. Arch Microbiol. 1998; 169(4):364-8. DOI: 10.1007/s002030050584. View

Hayashi N, Arai H, Kodama T, Igarashi Y . The nirQ gene, which is required for denitrification of Pseudomonas aeruginosa, can activate the RubisCO from Pseudomonas hydrogenothermophila. Biochim Biophys Acta. 1998; 1381(3):347-50. DOI: 10.1016/s0304-4165(98)00045-2. View

Tabita F, McFadden B . D-ribulose 1,5-diphosphate carboxylase from Rhodospirillum rubrum. II. Quaternary structure, composition, catalytic, and immunological properties. J Biol Chem. 1974; 249(11):3459-64. View

Hayashi N, Arai H, Kodama T, Igarashi Y . The novel genes, cbbQ and cbbO, located downstream from the RubisCO genes of Pseudomonas hydrogenothermophila, affect the conformational states and activity of RubisCO. Biochem Biophys Res Commun. 1998; 241(2):565-9. DOI: 10.1006/bbrc.1997.7853. View

Kusian B, Bednarski R, Husemann M, Bowien B . Characterization of the duplicate ribulose-1,5-bisphosphate carboxylase genes and cbb promoters of Alcaligenes eutrophus. J Bacteriol. 1995; 177(15):4442-50. PMC: 177195. DOI: 10.1128/jb.177.15.4442-4450.1995. View

van Keulen G, Girbal L, van den Bergh E, Dijkhuizen L, Meijer W . The LysR-type transcriptional regulator CbbR controlling autotrophic CO2 fixation by Xanthobacter flavus is an NADPH sensor. J Bacteriol. 1998; 180(6):1411-7. PMC: 107038. DOI: 10.1128/JB.180.6.1411-1417.1998. View

Hayashi N, Arai H, Kodama T, Igarashi Y . The cbbQ genes, located downstream of the form I and form II RubisCO genes, affect the activity of both RubisCOs. Biochem Biophys Res Commun. 1999; 265(1):177-83. DOI: 10.1006/bbrc.1999.1103. View

Heinhorst S, Baker S, Johnson D, Davies P, Cannon G, Shively J . Two Copies of form I RuBisCO genes in Acidithiobacillus ferrooxidans ATCC 23270. Curr Microbiol. 2002; 45(2):115-7. DOI: 10.1007/s00284-001-0094-5. View

10.

Watson G, Yu J, Tabita F . Unusual ribulose 1,5-bisphosphate carboxylase/oxygenase of anoxic Archaea. J Bacteriol. 1999; 181(5):1569-75. PMC: 93548. DOI: 10.1128/JB.181.5.1569-1575.1999. View

11.

Laing W . Regulation of Soybean Net Photosynthetic CO(2) Fixation by the Interaction of CO(2), O(2), and Ribulose 1,5-Diphosphate Carboxylase. Plant Physiol. 1974; 54(5):678-85. PMC: 366581. DOI: 10.1104/pp.54.5.678. View

12.

Grzeszik C, Jeffke T, Schaferjohann J, Kusian B, Bowien B . Phosphoenolpyruvate is a signal metabolite in transcriptional control of the cbb CO2 fixation operons in Ralstonia eutropha. J Mol Microbiol Biotechnol. 2000; 2(3):311-20. View

13.

Cannon G, Baker S, Soyer F, Johnson D, Bradburne C, Mehlman J . Organization of carboxysome genes in the thiobacilli. Curr Microbiol. 2003; 46(2):115-9. DOI: 10.1007/s00284-002-3825-3. View

14.

Viale A, Kobayashi H, Akazawa T . Expressed genes for plant-type ribulose 1,5-bisphosphate carboxylase/oxygenase in the photosynthetic bacterium Chromatium vinosum, which possesses two complete sets of the genes. J Bacteriol. 1989; 171(5):2391-400. PMC: 209913. DOI: 10.1128/jb.171.5.2391-2400.1989. View

15.

Baker S, Williams D, Aldrich H, Gambrell A, Shively J . Identification and localization of the carboxysome peptide Csos3 and its corresponding gene in Thiobacillus neapolitanus. Arch Microbiol. 2000; 173(4):278-83. DOI: 10.1007/s002030000141. View

16.

Hayashi N, Terazono K, Kodama T, Igarashi Y . Structure of ribulose 1,5-bisphosphate carboxylase/oxygenase gene cluster from a thermophilic hydrogen-oxidizing bacterium, Hydrogenophilus thermoluteolus, and phylogeny of the fructose 1,6-bisphosphate aldolase encoded by cbbA in the cluster. Biosci Biotechnol Biochem. 2000; 64(1):61-71. DOI: 10.1271/bbb.64.61. View

17.

Hanson T, Tabita F . A ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc Natl Acad Sci U S A. 2001; 98(8):4397-402. PMC: 31846. DOI: 10.1073/pnas.081610398. View

18.

Kusian B, Bowien B . Organization and regulation of cbb CO2 assimilation genes in autotrophic bacteria. FEMS Microbiol Rev. 1997; 21(2):135-55. DOI: 10.1111/j.1574-6976.1997.tb00348.x. View

19.

de Boer A, van der Oost J, Reijnders W, Westerhoff H, Stouthamer A, Van Spanning R . Mutational analysis of the nor gene cluster which encodes nitric-oxide reductase from Paracoccus denitrificans. Eur J Biochem. 1996; 242(3):592-600. DOI: 10.1111/j.1432-1033.1996.0592r.x. View

20.

Yokoyama K, Hayashi N, Arai H, Chung S, Igarashi Y, Kodama T . Genes encoding RubisCO in Pseudomonas hydrogenothermophila are followed by a novel cbbQ gene similar to nirQ of the denitrification gene cluster from Pseudomonas species. Gene. 1995; 153(1):75-9. DOI: 10.1016/0378-1119(94)00808-6. View