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CO2-concentrating mechanism and its traits in haloalkaliphilic cyanobacteria

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Abstract

Cyanobacteria are a group of oxygenic phototrophs that have existed for at least 3.5 Ga. Photosynthetic CO2 assimilation by cyanobacteria occurs via the Calvin cycle, with RuBisCO, its key enzyme, having very low affinity to CO2. This is due to the fact that atmospheric CO2 concentration in Archaean, when the photosynthetic apparatus evolved, was several orders higher than now. Later, in the epoch of Precambrian microbial communities, CO2 content in the atmosphere decreased drastically. Thus, present-day phototrophs, including cyanobacteria, require adaptive mechanisms for efficient photosynthesis. In cyanobacterial cells, this function is performed by the CO2-concentrating mechanism (CCM), which creates elevated CO2 concentrations in the vicinity of RuBisCO active centers, thus significantly increasing the rate of CO2 fixation in the Calvin cycle. CCM has been previously studied only for freshwater and marine cyanobacteria. We were the first to investigate CCM in haloalkaliphilic cyanobacteria from soda lakes. Extremophilic haloalkaliphilic cyanobacteria were shown to possess a well-developed CCM with the structure and functional principles similar to those of freshwater and marine strains. Analysis of available data suggests that regulation of the amount of inorganic carbon transported into the cell is probably the general CCM function under these conditions.

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References

  1. Raven, J.A., Cockell, C.S., and De La Rocha, C.L., The evolution of inorganic carbon concentrating mechanisms in photosynthesis, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 2008, vol. 363, pp. 2641–2650.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Price, G.D., Badger, M.R., Wodger, 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.

    Article  CAS  PubMed  Google Scholar 

  3. Price, G.D., Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism, Photosynth. Res., 2011, vol. 109, pp. 47–57.

    Article  CAS  PubMed  Google Scholar 

  4. Kupriyanova, E.V., Sinetova, M.A., Cho, S.M., Park, Y.-I., Los, D.A., and Pronina N.A., CO2-concentrating mechanism in cyanobacterial photosynthesis: organization, physiological role and evolutionary origin, Photosynth. Res., 2013, vol. 117, pp. 133–146.

    Article  CAS  PubMed  Google Scholar 

  5. Moroney, J.V., Jungnick, N., DiMario, R.J., and Longstreth, D.J., Photorespiration and carbon concentrating mechanisms: two adaptations to high O2, low CO2 conditions, Photosynth. Res., 2013, vol. 117, pp. 121–131.

    Article  CAS  PubMed  Google Scholar 

  6. DeRuyter, Y.S. and Fromme, P., Molecular structure of the photosynthetic apparatus, in The Cyanobacteria: Molecular Biology, Genetics and Evolution, Herrero, A. and Flores, E., Eds., Norfolk: Caister, 2008, pp. 217–270.

    Google Scholar 

  7. Jordan, D.B. and Ogren, W.L., Species variation in the specificity of ribulose biphosphate carboxylase/oxygenase, Nature, 1981, vol. 291, pp. 513–515.

    Article  CAS  Google Scholar 

  8. Tabita, F.R., Satagopan, S., Hanson, T.E., Kreel, N.E., and Scott, S.S., Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships, J. Exp. Bot., 2008, pp. 1515–1524.

    Google Scholar 

  9. Badger, M.R. and Spalding, M.H., CO2 acquisition, concentration and fixation in cyanobacteria and algae, in Photosynthesis: Physiology and Metabolism, Leegood, R.C., Sharkey, T.D., and von Caemmerer, S., Eds., Dordrecht: Kluwer, 2000, pp. 369–397.

    Chapter  Google Scholar 

  10. Delwiche, C.F., Tracing the thread of plastid diversity through the tapestry of life, Am. Nat., 1999, vol. 154, pp. 164–177.

    Article  Google Scholar 

  11. Badger, M.R., Hanson, D., and Price, G.D., Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria, Funct. Plant Biol., 2002, vol. 29, no. 2, pp. 161–173.

    Article  CAS  Google Scholar 

  12. Espie, G.S. and Kimber, M.S., Carboxysomes: cyanobacterial RubisCO comes in small packages, Photosynth. Res., 2011, vol. 109, pp. 7–20.

    Article  CAS  PubMed  Google Scholar 

  13. Cannon, G.C., Heinhorst, S., and Kerfeld, C.A., Carboxysomal carbonic anhydrases: structure and role in microbial CO2 fixation, Biochim. Biophys. Acta, 2010, vol. 1804, pp. 382–392.

    Article  CAS  PubMed  Google Scholar 

  14. Rae, B.D., Long, B.M., Badger, M.R., and Price, G.D., Functions, compositions, and evolution of the two types of carboxysomes: polyhedral micro-compartments that facilitate CO2 fixation in cyanobacteria and some proteobacteria, Microbiol. Mol. Biol. Rev., 2013, vol. 77, pp. 357–379.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Whitehead, L., Long, B.M., Price, G.D., and Badger, M.R., Comparing the in vivo function of α-carboxysomes and β-carboxysomes in two model cyanobacteria, Plant Physiol., 2014, vol. 165, pp. 398–411.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Kasting, J.F., Theoretical constraints on oxygen and carbon dioxide concentrations in the Precambrian atmosphere, Precambrian Res., 1987, vol. 34, pp. 205–229.

    Article  CAS  PubMed  Google Scholar 

  17. Zavarzin, G.A., Microbial biosphere, in Biosphere Origin and Evolution, Dobretsov, N.L., Kolchanov, N.A., Rosanov, A.Y., and Zavarzin, G.A., Eds., New York: Springer Science + Business Media, LLC, 2008, pp. 25–42.

    Chapter  Google Scholar 

  18. Tcherkez, G.G., Farquhar, G.D., and Andrews, T.J., Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 7246–7251.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Whitney, S.M., Houtz, R.L., and Alonso, H., Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme Rubisco, Plant Physiol., 2011, vol. 155, pp. 27–35.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Galmés, J., Kapralov, M.V., Andralojc, P.J., Conesa, M.A., Keys, A.J., Parry, M.A., and Flexas, J., Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends, Plant Cell Environ., 2014, vol. 37, pp. 1989–2001.

    Article  PubMed  Google Scholar 

  21. Jungnick, N., Ma, Y., Mukherjee, B., Cronan, J.C., Speed, D.J., Laborde, S.M., Longstreth, D.J., and Moroney, J.V., The carbon concentrating mechanism in Chlamydomonas reinhardtii: finding the missing pieces, Photosynth. Res., 2014, vol. 121, pp. 159–173.

    Article  CAS  PubMed  Google Scholar 

  22. Field, C.B., Behrenfeld, M.J., Randerson, J.T., and Falkowski, P., Primary production of the biosphere: integrating terrestrial and oceanic components, Science, 1998, vol. 281, pp. 237–240.

    Article  CAS  PubMed  Google Scholar 

  23. Cameron, J.C., Wilson, S.C., Bernstein, S.L., and Kerfeld, C.A., Biogenesis of a bacterial organelle: the carboxysome assembly pathway, Cell, 2013, vol. 155, pp. 1131–1140.

    Article  CAS  PubMed  Google Scholar 

  24. Kinney, J.N., Axen, S.D., and Kerfeld, C.A., Comparative analysis of carboxysome shell proteins, Photosynth. Res., 2011, vol. 109, pp. 21–32.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Sonnenfeld, P., Brines and Evaporites, Orlando: Academic, 1984.

    Google Scholar 

  26. Marcus, Y., Distribution of inorganic carbon among its component species in cyanobacteria: do cyanobacteria in fact actively accumulate inorganic carbon?, J. Theor. Biol., 1997, vol. 187, pp. 31–45.

    Article  Google Scholar 

  27. Kaplan, A. and Reinhold, L., CO2 concentrating mechanisms in photosynthetic microorganisms, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1999, vol. 50, pp. 539–570.

    Article  CAS  PubMed  Google Scholar 

  28. Pronina, N.A., The organization and physiological role of the CO2-CM in microalgal photosynthesis, Russ. J. Plant Physiol., 2000, vol. 47, no. 5, pp. 706–714.

    CAS  Google Scholar 

  29. Omata, T., Price, G.D., Badger, M.R., Okamura, M., Gohta, S., and Ogawa, T., Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC7942, Proc. Natl. Acad. Sci. U. S. A., 1999, vol. 96, pp. 13571–13576.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Shibata, M., Katoh, H., Sonoda, M., Ohkawa, H., Shimoyama, M., Fukuzawa, H., Kaplan, A., and Ogawa, T., Genes essential to sodium-dependent bicarbonate transport in cyanobacteria. Function and phylogenetic analysis, J. Biol. Chem., 2002, vol. 277, pp. 18658–18664.

    Article  CAS  PubMed  Google Scholar 

  31. Zhang, P.P., Battchikova, N., Jansen, T., Appel, J., Ogawa, T., and Aro, E.M., Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp. PCC 6803, Plant Cell, 2004, vol. 16, pp. 3326–3340.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Price, G.D., Woodger, F.J., Badger, M.R., Howitt, S.M., and Tucker, L., Identification of a SulP-type bicarbonate transporter in marine cyanobacteria, Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, pp. 18228–18233.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Shibata, M., Ohkawa, H., Kaneko, T., Fukuzawa, H., Tabata, S., Kaplan, A., and Ogawa, T., Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms, Proc. Natl. Acad. Sci. U. S. A., 2001, vol. 98, pp. 11789–11794.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Maeda, S., Badger, M.R., and Price, G.D., Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942, Mol. Microbiol., 2002, vol. 43, pp. 425–435.

    Article  CAS  PubMed  Google Scholar 

  35. Badger, M.R., Price, G.D., Long, B.M., and Woodger, F.J., The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism, J. Exp. Bot., 2006, vol. 57, no. 2, pp. 249–265.

    Article  CAS  PubMed  Google Scholar 

  36. Badger, M.R. and Price, G.D., CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution, J. Exp. Bot., 2003, vol. 54, no. 383, pp. 609–622.

    Article  CAS  PubMed  Google Scholar 

  37. Carbonic Anhydrase: Mechanism, Regulation, Links to Disease, and Industrial Applications. Subcellular Biochemistry 75, Frost, S.C. and McKenna, R., Eds., Dordrecht: Springer Science+Business Media, 2014.

    Google Scholar 

  38. Cot, S.S., So, A.K., and Espie, G.S., A multiprotein bicarbonate dehydration complex essential to carboxysome function in cyanobacteria, J. Bacteriol., 2008, vol. 190, pp. 936–945.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Penã, K.L., Castel, S.E., de Araujo, C., Espie, G.S., and Kimber, M.S., Structural basis of the oxidative activation of the carboxysomal γ-carbonic anhydrase, CcmM, Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, pp. 2455–2460.

    Article  PubMed Central  PubMed  Google Scholar 

  40. Rae, B.D., Long, B.M., Whitehead, L.F., Förster B., Badger, M.R., and Price, G.D., Cyanobacterial carboxysomes: microcompartments that facilitate CO2 fixation, J. Mol. Microbiol. Biotechnol., 2013, vol. 23, pp. 300–307.

    Article  CAS  PubMed  Google Scholar 

  41. Cannon, G.C., Bradburne, C.E., Aldrich, H.C., Baker, S.H., Heinhorst, S., and Shively, J.M., Microcompartments in prokaryotes: carboxysomes and related polyhedra, Appl. Environ. Microbiol., 2001, vol. 67, pp. 5351–5361.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Zavarzin, G.A., Epicontinental soda lakes as presumable relic biotopes of formation of terrestrial biota, Mikrobiologiya, 1993, vol. 62, pp. 477–479.

    Google Scholar 

  43. Dubinin, A.V., Gerasimenko, L.M., and Zavarzin, G.A., Ecophysiology and species diversity of cyanobacteria in Lake Magadi, Microbiology (Moscow), 1995, vol. 64, pp. 717–721.

    Google Scholar 

  44. Mikhodyuk, O.S., Gerasimenko, L.M., Akimov, V.N., Ivanovsky, R.N., and Zavarzin, G.A., Ecophysiology and polymorphism of the unicellular extremely natronophilic cyanobacterium Euhalothece sp. Z-M001 from Lake Magadi, Microbiology (Moscow), 2008, vol. 77, no. 6, pp. 717–725.

    Article  CAS  Google Scholar 

  45. Gerasimenko, L.M., Mityushina, L.L., and Namsaraev, B.B., Microcoleus mats from alkaliphilic and halophilic communities, Microbiology (Moscow), 2003, vol. 72, pp. 71–79.

    Article  CAS  Google Scholar 

  46. Namsaraev, Z.B., Gorlenko, V.M., Buryukhaev, S.P., Barkhutova, D.D., Dambaev, V.B., Dulov, L.E., Sorokin, D.Yu., and Namsaraev, B.B., Water regime and variations in hydrochemical characteristics of the soda salt Lake Khilganta (Southeastern Transbaikalia), Water Res., 2010, vol. 37, no. 4, pp. 513–519.

    Article  CAS  Google Scholar 

  47. Mikhodyuk, O.S., Zavarzin, G.A., and Ivanovsky, R.N., Transport systems for carbonate in the extremely natronophilic cyanobacterium Euhalothece sp., Microbiology (Moscow), 2008, vol. 77, no. 4, pp. 412–418.

    Article  CAS  Google Scholar 

  48. Samylina, O.S., Carbon-concentrating mechanism as a component of adaptation of an extremely halophilic cyanobacterium ‘Euhalothece natronophila’ to soda lake environment, Extended Abstract Cand. Sci. (Biol.) Dissertation, Moscow, 2008.

    Google Scholar 

  49. Samylina, O.S. and Ivanovsky, R.N., CO2-concentrating mechanism of cyanobacteria, Trudy Instituta mikrobiologii imeni S.N. Vinogradskogo (Proc. Winogradsky Inst. Microbiol.), vol. 15. Photosynthetic Bacteria, Gal’chenko, V.F., Ed., Moscow: MAKS, 2010, pp. 86–117.

    Google Scholar 

  50. Kupriyanova, E., Villarejo, A., Markelova, A., Gerasimenko, L., Zavarzin, G., Samuelsson, G., Los, D.A., and Pronina, N., Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes, Microbiology (UK), 2007, vol. 153, pp. 1149–1156.

    Article  CAS  Google Scholar 

  51. Kupriyanova, E.V., Sinetova, M.A., Markelova, A.G., Allakhverdiev, S.I., Los, D.A., and Pronina, N.A., Extracellular β-class carbonic anhydrase of the alkaliphilic cyanobacterium Microcoleus chthonoplastes, J. Photochem. Photobiol., 2011, vol. 103, pp. 78–86.

    Article  CAS  Google Scholar 

  52. Dudoladova, M.V., Kupriyanova, E.V., Markelova, A.G., Sinetova, M.P., Allakhverdiev, S.I., and Pronina, N.A., The thylakoid carbonic anhydrase associated with photosystem II is the component of inorganic carbon accumulating system in cells of halo- and alkaliphilic cyanobacterium Rhabdoderma lineare, Biochimica et Biophysica Acta-Bioenergetics, 2007, vol. 1767, pp. 616–623.

    Article  CAS  Google Scholar 

  53. Kupriyanova, E.V., Lebedeva, N.V., Dudoladova, M.V., Gerasimenko, L.M., Alekseeva, S.G., Pronina, N.A., and Zavarzin, G.A., Carbonic anhydrase activity of alkalophilic cyanobacteria from soda lakes, Russ. J. Plant Physiol., 2003, vol. 50, pp. 532–539.

    Article  CAS  Google Scholar 

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Correspondence to O. S. Samylina.

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Original Russian Text © E.V. Kupriyanova, O.S. Samylina, 2015, published in Mikrobiologiya, 2015, Vol. 84, No. 2, pp. 144–159.

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Kupriyanova, E.V., Samylina, O.S. CO2-concentrating mechanism and its traits in haloalkaliphilic cyanobacteria. Microbiology 84, 112–124 (2015). https://doi.org/10.1134/S0026261715010075

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