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PMID: 10611359 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Carbonic anhydrase is an ancient enzyme widespread in prokaryotes.

Smith KS, Jakubzick C, Whittam TS, Ferry JG

Abstract

Carbonic anhydrases catalyze the reversible hydration of CO(2) and are ubiquitous in highly evolved eukaryotes. The recent identification of a third class of carbonic anhydrase (gamma class) in a methanoarchaeon and our present finding that the beta class also extends into thermophilic species from the Archaea domain led us to initiate a systematic search for these enzymes in metabolically and phylogenetically diverse prokaryotes. Here we show that carbonic anhydrase is widespread in the Archaea and Bacteria domains, and is an ancient enzyme. The occurrence in chemolithoautotrophic species occupying deep branches of the universal phylogenetic tree suggests a role for this enzyme in the proposed autotrophic origin of life. The presence of the beta and gamma classes in metabolically diverse species spanning the Archaea and Bacteria domains demonstrates that carbonic anhydrases have a far more extensive and fundamental role in prokaryotic biology than previously recognized.

MeSH Terms
Archaea/classification,enzymology,genetics Bacteria/classification,enzymology,genetics Carbonic Anhydrases/classification,genetics Evolution, Molecular Phylogeny Prokaryotic Cells/enzymology
Chemicals
Carbonic Anhydrases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Smith K S
Department of Biochemistry, The Pennsylvania State University, University Park, PA 16802, USA.
Jakubzick C
Whittam T S
Ferry J G
References (35)
35 references, click to expand
  1. Carbonic anhydrase in Escherichia coli. A product of the cyn operon.
    J Biol Chem. 1992 Feb 25;267(6):3731-4 PMID: 1740425
  2. Kinetic and structural characterization of spinach carbonic anhydrase.
    Biochemistry. 1994 Nov 29;33(47):13967-76 PMID: 7947805
  3. A physiological role for cyanate-induced carbonic anhydrase in Escherichia coli.
    J Bacteriol. 1993 Mar;175(5):1443-51 PMID: 8444806
  4. CO2 CONCENTRATING MECHANISMS IN PHOTOSYNTHETIC MICROORGANISMS.
    Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:539-570 PMID: 15012219
  5. A plant-type (beta-class) carbonic anhydrase in the thermophilic methanoarchaeon Methanobacterium thermoautotrophicum.
    J Bacteriol. 1999 Oct;181(20):6247-53 PMID: 10515911
  6. A carbonic anhydrase from the archaeon Methanosarcina thermophila.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6909-13 PMID: 8041719
  7. Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene families.
    Mol Phylogenet Evol. 1996 Feb;5(1):50-77 PMID: 8673298
  8. Carbonic anhydrase in bacteria.
    Nature. 1963 Jan 5;197:76-7 PMID: 13996562
  9. Estimation of the number of amino acid substitutions per site when the substitution rate varies among sites.
    J Mol Evol. 1995 Nov;41(5):675-9 PMID: 18345592
  10. Phylogenetic test of the molecular clock and linearized trees.
    Mol Biol Evol. 1995 Sep;12(5):823-33 PMID: 7476128
  11. cDNA cloning, sequence, and expression of carbonic anhydrase in Chlamydomonas reinhardtii: regulation by environmental CO2 concentration.
    Proc Natl Acad Sci U S A. 1990 Jun;87(11):4383-7 PMID: 2112252
  12. MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers.
    Comput Appl Biosci. 1994 Apr;10(2):189-91 PMID: 8019868
  13. Carbonic anhydrase from Neisseria sicca, strain 6021. I. Bacterial growth and purification of the enzyme.
    Biochim Biophys Acta. 1972 Sep 19;284(1):298-310 PMID: 4627452
  14. Carbonic anhydrase. Its preparation and properties.
    J Physiol. 1933 Dec 5;80(2):113-42 PMID: 16994489
  15. Fluorescence-based isolation of bacterial genes expressed within host cells.
    Science. 1997 Sep 26;277(5334):2007-11 PMID: 9302299
  16. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  17. Electrometric and colorimetric determination of carbonic anhydrase.
    J Biol Chem. 1948 Oct;176(1):147-54 PMID: 18886152
  18. Identification and characterization of a gene encoding a vertebrate-type carbonic anhydrase in cyanobacteria.
    J Bacteriol. 1997 Feb;179(3):769-74 PMID: 9006032
  19. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  20. Characterization of heterologously produced carbonic anhydrase from Methanosarcina thermophila.
    J Bacteriol. 1996 Jun;178(11):3270-4 PMID: 8655508
  21. Isolation and characterization of CA XIV, a novel membrane-bound carbonic anhydrase from mouse kidney.
    J Biol Chem. 1999 May 28;274(22):15701-5 PMID: 10336468
  22. Evolutionarily conserved, "acatalytic" carbonic anhydrase-related protein XI contains a sequence motif present in the neuropeptide sauvagine: the human CA-RP XI gene (CA11) is embedded between the secretor gene cluster and the DBP gene at 19q13.3.
    Genomics. 1998 Dec 15;54(3):484-93 PMID: 9878252
  23. Carbonic anhydrase in Acetobacterium woodii and other acetogenic bacteria.
    J Bacteriol. 1997 Nov;179(22):7197-200 PMID: 9371472
  24. Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC7942 involved in carboxysome assembly and function.
    J Bacteriol. 1993 May;175(10):2871-9 PMID: 8491708
  25. A general method applicable to the search for similarities in the amino acid sequence of two proteins.
    J Mol Biol. 1970 Mar;48(3):443-53 PMID: 5420325
  26. The catalytic properties of murine carbonic anhydrase VII.
    Biochemistry. 1998 Jul 28;37(30):10837-45 PMID: 9692974
  27. A left-hand beta-helix revealed by the crystal structure of a carbonic anhydrase from the archaeon Methanosarcina thermophila.
    EMBO J. 1996 May 15;15(10):2323-30 PMID: 8665839
  28. Spinach carbonic anhydrase: investigation of the zinc-binding ligands by site-directed mutagenesis, elemental analysis, and EXAFS.
    Biochemistry. 1994 Nov 8;33(44):13126-31 PMID: 7947718
  29. Determining divergence times with a protein clock: update and reevaluation.
    Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):13028-33 PMID: 9371794
  30. Organization and growth phase-dependent transcription of methane genes in two regions of the Methanobacterium thermoautotrophicum genome.
    J Bacteriol. 1995 May;177(9):2460-8 PMID: 7730278
  31. Nucleotide sequences of two genes CAH1 and CAH2 which encode carbonic anhydrase polypeptides in Chlamydomonas reinhardtii.
    Nucleic Acids Res. 1990 Nov 11;18(21):6441-2 PMID: 2243800
  32. Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics.
    J Bacteriol. 1997 Nov;179(22):7135-55 PMID: 9371463
  33. Multiple roles of carbonic anhydrase in cellular transport and metabolism.
    Annu Rev Physiol. 1996;58:523-38 PMID: 8815807
  34. Structure, function and regulation of pyruvate carboxylase.
    Biochem J. 1999 May 15;340 ( Pt 1):1-16 PMID: 10229653
  35. The complete sequence, expression in Escherichia coli, purification and some properties of carbonic anhydrase from Neisseria gonorrhoeae.
    Eur J Biochem. 1997 Mar 15;244(3):755-60 PMID: 9108244
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1999-12-21
Pages
15184-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC24794
Subset
IM
Grants
NIGMS NIH HHS · R01 GM044661 · United States
NIAID NIH HHS · AI/GM42391 · United States
NIGMS NIH HHS · GM44661 · United States
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