Abstract—
The genes encoding carbonic anhydrase (CA) were found in all anoxygenic purple bacteria. The genes of α- and β-CA were found in purple nonsulfur bacteria of the class Alphaproteobacteria:Rhodospirillum rubrum, Rhodospirillum fulvum, Rhodoblastus acidophilus, and Rhodopseudomonas palustris. The alphaproteobacteria Rhodomicrobium vannielii, Blastochlorisviridis, Rhodobacter sphaeroides, Rhodobacter capsulatus, Rhodobacter veldkampii, Rhodovulumeuryhalinum, and Rhodovulum sulfidophilum possessed only the β-CA genes. Both nonsulfur purple bacteria of the class Betaproteobacteria (Rubrivivax gelatinosus) and purple sulfur bacteria (class Gammaproteobacteria) contained the α- and β-CA. No CA genes were found in green sulfur bacteria Chlorobaculum limnaeum and Chlorobaculum parvum, as well as in filamentous green nonsulfur bacteria Chloroflexus aurantiacus. However, the β-CA gene was revealed in Oscillochloris trichoides, which belonged to the latter taxonomic group. No γ-CA genes were detected in the genomes of the phototrophic bacteria studied in the present work. Although CA genes were present in all purple bacteria, the α- and β-CA activity was observed only in four species of purple nonsulfur Alphaproteobacteria: Rhodospirillum rubrum, Rhodopseudomonas palustris, Rhodoblastusacidophilus, and Rhodospirillum fulvum. These bacteria are able to synthesize CA under both photoautotrophic and photoheterotrophic conditions in the media with acetate, malate, or fructose. These bacteria (except for Rhodospirillum fulvum, which is unable to grow under aerobic conditions), also exhibit CA activity when grown under aerobic conditions in the dark.
Similar content being viewed by others
REFERENCES
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J., Basic local alignment search tool, J Mol. Biol., 1990, vol. 215, pp. 403–410.
Badger, M.R. and Bek, E.J., Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle, J. Exp. Bot., 2008, vol. 59, pp. 1525–1541.
Burnap, R.L., Hagemann, M., and Kaplan, A., Regulation of CO2 concentrating mechanism in cyanobacteria, Life (Basel), 2015, vol. 5, pp. 348–371.
Capasso, C. and Supuran, C.T., An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria?, J. Enzyme Inhib. Med. Chem., 2015, vol. 30, pp. 325–332.
Castenholz, R.W. and Pierson, B.K., Isolation of members of the family Chloroflexaceae, in The Procaryotes, Staarr, M.P., Truper, H.G., Ballows, A., and Schlegel, H.G., Eds., Berlin: Springer, 1981, vol. 1, pp. 290–298.
Dahl, C., Sulfur metabolism in phototrophic bacteria, in Modern Topics in the Phototrophic Prokaryotes. Metabolism, Bioenergetics and Omics, Hallenbeck, P., Ed., Springer, 2017, pp. 27–66.
Davis, R.P., The kinetics of the reaction of human erythrocyte carbonic anhydrase. II. The effect of sulfanilamide, sodium sulfide and various chelating agents, J. Amer. Chem. Soc., 1959, vol. 81, pp. 5674–5678.
DiMario, R.J., Machingura, M.C., Waldrop, G.L., and Moroney, J.V., The many types of carbonic anhydrases in photosynthetic organisms., Plant Sci., 2018, vol. 268, pp. 11–17.
Frigaard, N.U. and Dahl, C., Sulfur metabolism in phototrophic sulfur bacteria, Adv. Microb. Physiol., 2009, vol. 54, pp. 103–200.
Furdui, C. and Ragsdale, S.W., The role of pyruvate ferredoxin oxidoreductase in pyruvate synthesis during autotrophic growth by the Wood-Ljungdahl pathway, J. Biol. Chem., 2000, vol. 275, pp. 28494–28499.
Gai, C.S., Lu, J., Brigham, C.J., Bernardi, A.C., and Sinskey, A.J., Insights into bacterial CO2 metabolism revealed by the characterization of four carbonic anhydrases in Ralstonia eutropha H16, AMB Express, 2014, vol. 4, article 2. https://doi.org/10.1186/2191-0855-4-2
Gill, S.R., Fedorka-Cray, P.J., Tweten, R.K., and Sleeper, B.P., Purification and properties of the carbonic anhydrase of Rhodospirillum rubrum,Arch. Microbiol., 1984, vol. 138, pp. 113–118.
Imhoff, J.F., Transfer of Rhodopseudomonas acidophila to the new genus Rhodoblastus as Rhodoblastus acidophilus gen. nov., comb. nov., Int. J. Syst. Evol. Microbiol., 2001, vol. 51, pp. 1863–1866.
Kanehisa, M., Sato, Y., and Morishima, K., BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences, J. Mol. Biol., 2016, vol. 428, pp. 726–731.
Katoh, K., Misawa, K., Kuma, K., and Miyata, T., MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucl. Acids Res., 2002, vol. 30, pp. 3059–3066.
Kumar, S., Stecher, G., and Tamura K., MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets, Mol. Biol. Evol., 2016, vol. 33, pp. 1870–1874.
Larsen, H., On the culture and general physiology of the green sulfur bacteria, J. Bacteriol., 1952, vol. 64, pp. 187–196.
Leustek, T., Hartwig, R., Weissbach, H., and Brot, N., Regulation of ribulose bisphosphate carboxylase expression in Rhodospirillum rubrum: characteristics of mRNA synthesized in vivo and in vitro, J. Bacteriol., 1988, vol. 170, pp. 4065–4071.
Ormerod, J.G., Ormerod, K.S., and Gest, H., Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism, Arch. Biochem. Biophys., 1961, vol. 94, pp. 449–463.
Price, G.D., Badger, M.R., Woodger, F.J., and Long, B.M., Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants, J. Exp. Bot., 2008, vol. 59, pp. 1441–1461.
Puskas, L.G., Inui, M., Zahn, K., and Yukawa, H., A periplasmic, alpha-type carbonic anhydrase from Rhodopseudomonas palustris is essential for bicarbonate uptake, Microbiology (SGM), 2000, vol. 146, pp. 2957–2966.
Rae, B.D., Long, B.M., Badger, M.R., and Price, G.D., Functions, compositions, and evolution of the two types of carboxysomes: polyhedral microcompartments that facilitate CO2 fixation in Cyanobacteria and some Proteobacteria,Microbiol. Mol. Biol. Rev., 2013, vol. 77, pp. 357–379.
Romagnoli, S. and Tabita, F.R., Carbon dioxide metabolism and its regulation in nonsulfur purple photosynthetic bacteria, in The Purple Phototrophic Bacteria. Advances in Photosynthesis and Respiration, Hunter, C.N., Daldal, F., Thurnauer, M.C., and Beatty, J.T., Eds., Dordrecht: Springer, 2009, vol. 28, pp. 563–576.
Sarles, L.S. and Tabita, F.R., Derepression of the synthesis of D-ribulose 1,5-bisphosphate carboxylase/oxygenase from Rhodospirillum rubrum,J. Bacteriol., 1983, vol. 153, pp. 458–464.
Sawaya, M.R., Cannon, G.C., Heinhorst, S., Tanaka, S., Williams, E.B., Yeates, T.O., and Kerfeld, C.A., The structure of beta-carbonic anhydrase from the carboxysomal shell reveals a distinct subclass with one active site for the price of two, J. Biol. Chem., 2006, vol. 281, pp. 7546–7555.
Schlegel, H.G. and Pfennig, N., Enriched culture for various purple sulfur bacteria, Arch. Mikrobiol., 1961, vol. 38, pp. 1–39.
Supuran, C.T. and Capasso, C., An overview of the bacterial carbonic anhydrases, Metabolites, 2017, vol. 7. pii: E56. https://doi.org/10.3390/metabo7040056
Ueda, K., Nishida, H., and Beppu, T., Dispensabilities of carbonic anhydrase in proteobacteria, Int. J. Evol. Biol., 2012, vol. 2012, article 324549. https://doi.org/10.1155/2012/324549
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Additional information
Translated by E. Babchenko
Rights and permissions
About this article
Cite this article
Ivanovsky, R.N., Keppen, O.I., Lebedeva, N.V. et al. Carbonic Anhydrase in Anoxygenic Phototrophic Bacteria. Microbiology 89, 266–272 (2020). https://doi.org/10.1134/S0026261720020058
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0026261720020058