1887

Abstract

Two new autotrophic carbon fixation cycles have been recently described in Crenarchaeota. The 3-hydroxypropionate/4-hydroxybutyrate cycle using acetyl-coenzyme A (CoA)/propionyl-CoA carboxylase as the carboxylating enzyme has been identified for (micro)aerobic members of the Sulfolobales. The dicarboxylate/4-hydroxybutyrate cycle using oxygen-sensitive pyruvate synthase and phosphoenolpyruvate carboxylase as carboxylating enzymes has been found in members of the anaerobic Desulfurococcales and Thermoproteales. However, Sulfolobales include anaerobic and Desulfurococcales aerobic autotrophic representatives, raising the question of which of the two cycles they use. We studied the mechanisms of autotrophic CO fixation in the strictly anaerobic (Sulfolobales) and in the facultatively aerobic (Desulfurococcales). The activities of all enzymes of the 3-hydroxypropionate/4-hydroxybutyrate cycle were found in the anaerobic . In contrast, the aerobic or denitrifying possesses all enzyme activities of the dicarboxylate/4-hydroxybutyrate cycle. We conclude that autotrophic Crenarchaeota use one of the two cycles, and that their distribution correlates with the 16S rRNA-based phylogeny of this group, rather than with the aerobic or anaerobic lifestyle.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.034298-0
2010-01-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/1/256.html?itemId=/content/journal/micro/10.1099/mic.0.034298-0&mimeType=html&fmt=ahah

References

  1. Alber, B., Olinger, M., Rieder, A., Kockelkorn, D., Jobst, B., Hügler, M. & Fuchs, G. ( 2006; ). Malonyl-coenzyme A reductase in the modified 3-hydroxypropionate cycle for autotrophic carbon fixation in archaeal Metallosphaera and Sulfolobus spp. J Bacteriol 188, 8551–8559.[CrossRef]
    [Google Scholar]
  2. Allen, M. B. ( 1959; ). Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Mikrobiol 32, 270–277.[CrossRef]
    [Google Scholar]
  3. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. ( 1990; ). Basic local alignment search tool. J Mol Biol 215, 403–410.[CrossRef]
    [Google Scholar]
  4. Anderson, I. J., Dharmarajan, L., Rodriguez, J., Hooper, S., Porat, I., Ulrich, L. E., Elkins, J. G., Mavromatis, K., Sun, H. & other authors ( 2009; ). The complete genome sequence of Staphylothermus marinus reveals differences in sulfur metabolism among heterotrophic Crenarchaeota. BMC Genomics 10, 145 [CrossRef]
    [Google Scholar]
  5. Aoshima, M. ( 2007; ). Novel enzyme reactions related to the tricarboxylic acid cycle: phylogenetic/functional implications and biotechnological applications. Appl Microbiol Biotechnol 75, 249–255.[CrossRef]
    [Google Scholar]
  6. Ashida, H., Saito, Y., Nakano, T., Tandeau de Marsac, N., Sekowska, A., Danchin, A. & Yokota, A. ( 2008; ). RuBisCO-like proteins as the enolase enzyme in the methionine salvage pathway: functional and evolutionary relationships between RuBisCO-like proteins and photosynthetic RuBisCO. J Exp Bot 59, 1543–1554.
    [Google Scholar]
  7. Auernik, K. S., Maezato, Y., Blum, P. H. & Kelly, R. M. ( 2008; ). The genome sequence of the metal-mobilizing, extremely thermoacidophilic archaeon Metallosphaera sedula provides insights into bioleaching-associated metabolism. Appl Environ Microbiol 74, 682–692.[CrossRef]
    [Google Scholar]
  8. Balch, W. E., Fox, G. E., Magrum, L. J., Woese, C. R. & Wolfe, R. S. ( 1979; ). Methanogens: reevaluation of a unique biological group. Microbiol Rev 43, 260–296.
    [Google Scholar]
  9. Batista, A. P., Kletzin, A. & Pereira, M. M. ( 2008; ). The dihydrolipoamide dehydrogenase from the crenarchaeon Acidianus ambivalens. FEMS Microbiol Lett 281, 147–154.[CrossRef]
    [Google Scholar]
  10. Baumann, C., Judex, M., Huber, H. & Wirth, R. ( 1998; ). Estimation of genome sizes of hyperthermophiles. Extremophiles 2, 101–108.[CrossRef]
    [Google Scholar]
  11. Beh, M., Strauss, G., Huber, R., Stetter, K. O. & Fuchs, G. ( 1993; ). Enzymes of the reductive citric acid cycle in the autotrophic eubacterium Aquifex pyrophilus and in the archebacterium Thermoproteus neutrophilus. Arch Microbiol 160, 306–311.[CrossRef]
    [Google Scholar]
  12. Berg, I. A., Kockelkorn, D., Buckel, W. & Fuchs, G. ( 2007; ). A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318, 1782–1786.[CrossRef]
    [Google Scholar]
  13. Bergmeyer, H. U. ( 1975; ). Neue Werte für die molaren Extinktions-Koeffizienten von NADH und NADPH zum Gebrauch im Routine-Laboratorium. Z Klin Chem Klin Biochem 13, 507–508 (in German).
    [Google Scholar]
  14. Blöchl, E., Rachel, R., Burggraf, S., Hafenbradl, D., Jannasch, H. W. & Stetter, K. O. ( 1997; ). Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113 degrees C. Extremophiles 1, 14–21.[CrossRef]
    [Google Scholar]
  15. Bradford, M. M. ( 1976; ). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248–254.[CrossRef]
    [Google Scholar]
  16. Brochier-Armanet, C., Boussau, B., Gribaldo, S. & Forterre, P. ( 2008; ). Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6, 245–252.[CrossRef]
    [Google Scholar]
  17. Brügger, K., Chen, L., Stark, M., Zibat, A., Redder, P., Ruepp, A., Awayez, M., She, Q., Garrett, R. A. & Klenk, H. P. ( 2007; ). The genome of Hyperthermus butylicus: a sulfur-reducing, peptide fermenting, neutrophilic Crenarchaeote growing up to 10 °C. Archaea 2, 127–135.[CrossRef]
    [Google Scholar]
  18. Buckel, W. & Golding, G. T. ( 2006; ). Radical enzymes in anaerobes. Annu Rev Microbiol 60, 27–49.[CrossRef]
    [Google Scholar]
  19. Burton, N. P., Williams, T. D. & Norris, P. R. ( 1999; ). Carboxylase genes in Sulfolobus metallicus. Arch Microbiol 172, 349–353.[CrossRef]
    [Google Scholar]
  20. Chen, L., Brügger, K., Skovgaard, M., Redder, P., She, Q., Torarinsson, E., Greve, B., Awayez, M., Zibat, A. & other authors ( 2005; ). The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. J Bacteriol 187, 4992–4999.[CrossRef]
    [Google Scholar]
  21. Chuakrut, S., Arai, H., Ishii, M. & Igarashi, Y. ( 2003; ). Characterization of a bifunctional archaeal acyl coenzyme A carboxylase. J Bacteriol 185, 938–947.[CrossRef]
    [Google Scholar]
  22. Cole, J. R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., Kulam-Syed-Mohideen, A. S., McGarrell, D. M., Marsh, T. & other authors ( 2009; ). The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37, (database issue), D141–D145.[CrossRef]
    [Google Scholar]
  23. de la Torre, J. R., Walker, C. B., Ingalls, A. E., Könneke, M. & Stahl, D. A. ( 2008; ). Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10, 810–818.[CrossRef]
    [Google Scholar]
  24. Erb, T. J., Berg, I. A., Brecht, V., Müller, M., Fuchs, G. & Alber, B. E. ( 2007; ). Synthesis of C5-dicarboxylic acids from C2-units involving crotonyl-CoA carboxylase/reductase: the ethylmalonyl-CoA pathway. Proc Natl Acad Sci U S A 104, 10631–10636.[CrossRef]
    [Google Scholar]
  25. Erb, T. J., Rétey, J., Fuchs, G. & Alber, B. ( 2008; ). Ethylmalonyl-CoA mutase from Rhodobacter sphaeroides defines a new subclade of coenzyme B12-dependent acyl-CoA mutases. J Biol Chem 283, 32283–32293.[CrossRef]
    [Google Scholar]
  26. Fuchs, T., Huber, H., Burggraf, S. & Stetter, K. O. ( 1996; ). 16S rDNA-based phylogeny of the archaeal order Sulfolobales and reclassification of Desulfurolobus ambivalens as Acidianus ambivalens comb. nov. Syst Appl Microbiol 19, 56–60.[CrossRef]
    [Google Scholar]
  27. Garrity, G. M. & Holtб, J. G. ( 2001; ). Phylum AI. Crenarchaeota phy. nov. In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 1, pp. 169–210. Edited by D. R. Boone, R. W. Castenholz & G. M. Garrity. New York: Springer.
  28. Garrity, G. M., Bell, J. A. & Lilburn, T. ( 2005; ). The revised road map to the Manual. In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 2A, pp. 159–187. Edited by D. J. Brenner, N. R. Krieg & J. T. Staley. New York: Springer.
  29. Hatzenpichler, R., Lebedeva, E. V., Spieck, E., Stoecker, K., Richter, A., Daims, H. & Wagner, M. ( 2008; ). A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci U S A 105, 2134–2139.[CrossRef]
    [Google Scholar]
  30. Huber, H. & Prangishvili, D. ( 2006; ). Sulfolobales. In The Prokaryotes: an Evolving Electronic Resource for the Microbiological Community, vol. 3, pp. 23–51. Edited by M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Stackebrandt. New York: Springer.
  31. Huber, H. & Stetter, K. O. ( 2001; ). Genus II. Acidianus Segerer, Neuner, Kristjansson and Stetter 1986, 561VP. In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 1, pp. 202–204. Edited by D. R. Boone, R. W. Castenholz & G. M. Garrity. New York: Springer.
  32. Huber, H. & Stetter, K. O. ( 2006; ). Desulfurococcales. In The Prokaryotes: an Evolving Electronic Resource for the Microbiological Community, vol. 3, pp. 52–68. Edited by M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Stackebrandt. New York: Springer.
  33. Huber, G., Spinnler, C., Gambacorta, A. & Stetter, K. O. ( 1989; ). Metallosphaera sedula, gen. and sp. nov. represents a new genus of aerobic, metal-mobilizing, thermoacidophilic archaebacteria. Syst Appl Microbiol 12, 38–47.[CrossRef]
    [Google Scholar]
  34. Huber, H., Gallenberger, M., Jahn, U., Eylert, E., Berg, I. A., Kockelkorn, D., Eisenreich, W. & Fuchs, G. ( 2008; ). A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic archaeum Ignicoccus hospitalis. Proc Natl Acad Sci U S A 105, 7851–7856.[CrossRef]
    [Google Scholar]
  35. Hügler, M., Huber, H., Stetter, K. O. & Fuchs, G. ( 2003a; ). Autotrophic CO2 fixation pathways in archaea (Crenarchaea). Arch Microbiol 179, 160–173.
    [Google Scholar]
  36. Hügler, M., Krieger, R. S., Jahn, M. & Fuchs, G. ( 2003b; ). Characterization of acetyl-CoA/propionyl-CoA carboxylase in Metallosphaera sedula. Carboxylating enzyme in the 3-hydroxypropionate cycle for autotrophic carbon fixation. Eur J Biochem 270, 736–744.[CrossRef]
    [Google Scholar]
  37. Hügler, M., Huber, H., Molyneaux, S. J., Vetriani, C. & Sievert, S. M. ( 2007; ). Autotrophic CO2 fixation via the reductive tricarboxylic acid cycle in different lineages within the phylum Aquificae: evidence for two ways of citrate cleavage. Environ Microbiol 9, 81–92.[CrossRef]
    [Google Scholar]
  38. Ikeda, T., Ochiai, T., Morita, S., Nishiyama, A., Yamada, E., Arai, H., Ishii, M. & Igarashi, Y. ( 2006; ). Anabolic five subunit-type pyruvate : ferredoxin oxidoreductase from Hydrogenobacter thermophilus TK-6. Biochem Biophys Res Commun 340, 76–82.[CrossRef]
    [Google Scholar]
  39. Ishii, M., Miyake, T., Satoh, T., Sugiyama, H., Oshima, Y., Kodama, T. & Igarashi, Y. ( 1996; ). Autotrophic carbon dioxide fixation in Acidianus brierleyi. Arch Microbiol 166, 368–371.[CrossRef]
    [Google Scholar]
  40. Jahn, U., Huber, H., Eisenreich, W., Hügler, M. & Fuchs, G. ( 2007; ). Insights into the autotrophic CO2 fixation pathway of the archaeon Ignicoccus hospitalis: comprehensive analysis of the central carbon metabolism. J Bacteriol 189, 4108–4119.[CrossRef]
    [Google Scholar]
  41. Karner, M. B., DeLong, E. F. & Karl, D. M. ( 2001; ). Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510.[CrossRef]
    [Google Scholar]
  42. Kawarabayasi, Y., Hino, Y., Horikawa, H., Yamazaki, S., Haikawa, Y., Jin-no, K., Takahashi, M., Sekine, M., Baba, S. & other authors ( 1999; ). Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res 6, 83–101, 145–152.[CrossRef]
    [Google Scholar]
  43. Kawarabayasi, Y., Hino, Y., Horikawa, H., Jin-no, K., Takahashi, M., Sekine, M., Baba, S., Ankai, A., Kosugi, H. & other authors ( 2001; ). Complete genome sequence of an aerobic thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain7. DNA Res 8, 123–140.[CrossRef]
    [Google Scholar]
  44. Könneke, M., Bernhard, A. E., de la Torre, J. R., Walker, C. B., Waterbury, J. B. & Stahl, D. A. ( 2005; ). Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546.[CrossRef]
    [Google Scholar]
  45. Martins, B. M., Dobbek, H., Cinkaya, I., Buckel, W. & Messerschmidt, A. ( 2004; ). Crystal structure of 4-hydroxybutyryl-CoA dehydratase: radical catalysis involving a [4Fe–4S] cluster and flavin. Proc Natl Acad Sci U S A 101, 15645–15649.[CrossRef]
    [Google Scholar]
  46. Menendez, C., Bauer, Z., Huber, H., Gad'on, N., Stetter, K.-O. & Fuchs, G. ( 1999; ). Presence of acetyl coenzyme A (CoA) carboxylase and propionyl-CoA carboxylase in autotrophic Crenarchaeota and indication for operation of a 3-hydroxypropionate cycle in autotrophic carbon fixation. J Bacteriol 181, 1088–1098.
    [Google Scholar]
  47. Norris, P., Nixon, A. & Hart, A. ( 1989; ). Acidophilic, mineral-oxidizing bacteria: the utilization of carbon dioxide with particular reference to autotrophy in Sulfolobus. In Microbiology of Extreme Environments and its Potential for Biotechnology, pp. 24–43. Edited by M. S. Da Costa, J. C. Duarte & R. A. D. Williams. London: Elsevier.
  48. O'Hare, M. C. & Doonan, S. ( 1985; ). Purification and structural comparison of the cytosolic and mitochondrial isoenzymes of fumarase from pig liver. Biochim Biophys Acta 827, 127–134.[CrossRef]
    [Google Scholar]
  49. Podar, M., Anderson, I., Makarova, K. S., Elkins, J. G., Ivanova, N., Wall, M. A., Lykidis, A., Mavromatis, K., Sun, H. & other authors ( 2008; ). A genomic analysis of the archaeal system Ignicoccus hospitalis–Nanoarchaeum equitans. Genome Biol 9, R158 [CrossRef]
    [Google Scholar]
  50. Preston, C. M., Wu, K. Y., Molinski, T. F. & DeLong, E. F. ( 1996; ). A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci U S A 93, 6241–6246.[CrossRef]
    [Google Scholar]
  51. Ramos-Vera, W. H., Berg, I. A. & Fuchs, G. ( 2009; ). Autotrophic carbon dioxide assimilation in Thermoproteales revisited. J Bacteriol 191, 4286–4297.[CrossRef]
    [Google Scholar]
  52. Ravin, N. V., Mardanov, A. V., Beletsky, A. V., Kublanov, I. V., Kolganova, T. V., Lebedinsky, A. V., Chernyh, N. A., Bonch-Osmolovskaya, E. A. & Skryabin, K. G. ( 2009; ). Complete genome sequence of the anaerobic, protein-degrading hyperthermophilic crenarchaeon Desulfurococcus kamchatkensis. J Bacteriol 191, 2371–2379.[CrossRef]
    [Google Scholar]
  53. Redder, P. & Garrett, R. A. ( 2006; ). Mutations and rearrangements in the genome of Sulfolobus solfataricus P2. J Bacteriol 188, 4198–4206.[CrossRef]
    [Google Scholar]
  54. Reno, M. L., Held, N. L., Fields, C. J., Burke, P. V. & Whitaker, R. J. ( 2009; ). Biogeography of the Sulfolobus islandicus pan-genome. Proc Natl Acad Sci U S A 106, 8605–8610.[CrossRef]
    [Google Scholar]
  55. Riddles, P. W., Blakeley, R. L. & Zerner, B. ( 1983; ). Reassessment of Ellman's reagent. Methods Enzymol 91, 49–60.
    [Google Scholar]
  56. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  57. Sato, T., Atomi, H. & Imanaka, T. ( 2007; ). Archaeal type III RuBisCOs function in a pathway for AMP metabolism. Science 315, 1003–1006.[CrossRef]
    [Google Scholar]
  58. Schauder, R., Widdel, F. & Fuchs, G. ( 1987; ). Carbon assimilation pathways in sulfate-reducing bacteria. II. Enzymes of a reductive citric acid cycle in the autotrophic Desulfobacter hydrogenophilus. Arch Microbiol 148, 218–225.[CrossRef]
    [Google Scholar]
  59. Scherf, U., Söhling, B., Gottschalk, G., Linder, D. & Buckel, W. ( 1994; ). Succinate-ethanol fermentation in Clostridium kluyveri: purification and characterisation of 4-hydroxybutyryl-CoA dehydratase/vinylacetyl-CoA Δ32-isomerase. Arch Microbiol 161, 239–245.[CrossRef]
    [Google Scholar]
  60. Segerer, A. H., Stetter, K. O. & Klink, F. ( 1985; ). Two contrary modes of chemolithotrophy in the same archaebacterium. Nature 313, 787–789.[CrossRef]
    [Google Scholar]
  61. Segerer, A. H., Neuner, A., Kristjansson, J. K. & Stetter, K. O. ( 1986; ). Acidianus infernus gen. nov., sp. nov., and Acidianus brierleyi comb. nov.: facultatively aerobic, extremely acidophilic thermophilic sulfur-metabolizing archaebacteria. Int J Syst Bacteriol 36, 559–564.[CrossRef]
    [Google Scholar]
  62. Segerer, A. H., Trincone, A., Gahrtz, M. & Stetter, K. O. ( 1991; ). Stygiolobus azoricus gen. nov., sp. nov. represents a novel genus of anaerobic, extremely thermoacidophilic archaebacteria of the order Sulfolobales. Int J Syst Bacteriol 41, 495–501.[CrossRef]
    [Google Scholar]
  63. She, Q., Singh, R. K., Confalonieri, F., Zivanovic, Y., Allard, G., Awayez, M. J., Chan-Weiher, C. C., Clausen, I. G., Curtis, B. A. & other authors ( 2001; ). The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci U S A 98, 7835–7840.[CrossRef]
    [Google Scholar]
  64. Shiba, H., Kawasumi, T., Igarashi, Y., Kodama, T. & Minoda, Y. ( 1985; ). The CO2 assimilation via the reductive tricarboxylic acid cycle in an obligatory autotrophic, aerobic hydrogen-oxidizing bacterium, Hydrogenobacter thermophilus. Arch Microbiol 141, 198–203.[CrossRef]
    [Google Scholar]
  65. Simon, E. J. & Shemin, D. ( 1953; ). The preparation of S-succinyl coenzyme-A. J Am Chem Soc 75, 2520
    [Google Scholar]
  66. Suzuki, S., Osumi, T. & Katsuki, H. ( 1977; ). Properties and metabolic role of mesaconate hydratase of an aerobic bacterium. J Biochem 81, 1917–1925.
    [Google Scholar]
  67. Tabita, F. R., Hanson, T. E., Li, H., Satagopan, S., Singh, J. & Chan, S. ( 2007; ). Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol Mol Biol Rev 71, 576–599.[CrossRef]
    [Google Scholar]
  68. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
  69. Trudinger, P. A. ( 1970; ). On the absorbancy of reduced methyl viologen. Anal Biochem 36, 222–225.[CrossRef]
    [Google Scholar]
  70. Van de Peer, Y. & De Wachter, R. ( 1994; ). treecon for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10, 569–570.
    [Google Scholar]
  71. Yamamoto, M., Arai, H., Ishii, M. & Igarashi, Y. ( 2006; ). Role of two 2-oxoglutarate : ferredoxin oxidoreductases in Hydrogenobacter thermophilus under aerobic and anaerobic conditions. FEMS Microbiol Lett 263, 189–193.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.034298-0
Loading
/content/journal/micro/10.1099/mic.0.034298-0
Loading

Data & Media loading...

Supplementary material 

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error