Occurrence of hydrogenases in cyanobacteria and anoxygenic photosynthetic bacteria: Implications for the phylogenetic origin of cyanobacterial and algal hydrogenases

Journal of Molecular Evolution

Volumn 63, Issue 6, 2006, Pages 758-768

  Ludwig, Marcus ^a,b   Schulz Friedrich, Rüdiger ^a   Appel, Jens ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Chloroflexus; Heliobacteria; Oxygenic photosynthesis; Photosynthetic proteobacteria

Indexed keywords

HYDROGENASE; IRON; SULFUR;

ANIMAL CELL; ARTICLE; CHLOROBI; CHLOROFLEXUS; CYANOBACTERIUM; ENZYME ACTIVITY; HORIZONTAL GENE TRANSFER; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; PHYLOGENY; UNINDEXED SEQUENCE;

ALGAE; BACTERIAL PROTEINS; CYANOBACTERIA; HYDROGEN; HYDROGENASE; PHOTOSYNTHESIS; PHYLOGENY;

ALGAE; ARCHAEA; BACTERIA (MICROORGANISMS); CHLOROBI; CHLOROFLEXI; CHLOROFLEXUS; CHLOROFLEXUS AURANTIACUS; CYANOBACTERIA; PHOTOBACTERIA; PROKARYOTA; PROTEOBACTERIA; SYNECHOCOCCUS;

EID: 33845369271     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-006-0001-6     Document Type: Article

References (58)

1. Adams MWW (1990) The structure and mechanism of iron-hydrogenases. Biochim Biophys Acta 1020:115-145
2. Albracht SP, Hedderich R (2000) Learning from hydrogenases: location of a proton pump and of a second FMN in bovine NADH-ubiquinone oxidoreductase (Complex I). FEBS Lett 485:1-6
3. Anderson SGE, Kurland CG (1999) Origins of mitochondria and hydrogenosomes. Curr Opin Microbiol 2:535-541
4. Appel J, Schulz R (1996) Sequence analysis of an operon of a NAD(P)-reducing nickel hydrogenase from the cyanobacterium Synechocystis sp. PCC 6803 gives additional evidence for direct coupling of the enzyme to NAD(P)H-dehydrogenase (complex I). Biochim Biophys Acta 1298:141-147
5. Appel J, Schulz R (1998) Hydrogen metabolism in organisms with oxygenic photosynthesis: Hydrogenase as important regulatory devices for a proper redox poising? J Photochem Photobiol B Biol 47:1-11
6. Appel J, Phunpruch S, Steinmüller K, Schulz R (2000) The bidirectional hydrogenase of Synechocystis sp. PCC 6803 works as an electron valve during photosynthesis. Arch Microbiol 173:333-338
7. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306: 79-86
8. Belkin S, Padan E (1978) Sulfide-dependent hydrogen evolution in the cyanobacterium Oscillatoria limnetica. FEBS Lett 94:291-293
9. Blokesch M, Paschos A, Theodoratou E, Bauer A, Hube M, Huth S, Böck A (2002) Metal insertion into NiFe-hyrogenases. Biochem Soc Trans 30:674-680
10. Boucher Y, Douady CJ, Papke RT, Walsh DA, Boudreau MER, Nesbo CL, Case RJ, Doolittle WF (2003) Lateral gene transfer and the origins of prokaryotic groups. Annu Rev Genet 37:283-328
11. Calteau A, Gouy M, Perriere G (2005) Horizontal transfer of two operons coding for hydrogenases between bacteria and archaea. J Mol Evol 60:557-565
12. Carrasco CD, Buettner JA, Golden JW (1995) Programmed DNA rearrangement of a cyanobacterial hupL gene in heterocysts. Proc Natl Acad Sci USA 92:791-795
13. Cobley JG, Clark AC, Weerasurya S, Queseda FA, Xiao JY, Bandrapali N, D'Silva I, Thounaojam M, Oda JF, Sumiyoshi T, Chu MH (2002) CpeR is an activator required for expression of the phycoerythrin operon (cpeBA) in the cyanobacterium Fremyella diplosiphon and is encoded in the phycoerythrin linker-polypeptide operon (cpeCDESTR). Mol Microbiol 44:1517-1531
14. Cournac L, Mus F, Bernard L, Guedeney G, Vignais P, Peltier G (2002) Limiting steps of hydrogen production in Chlamydomonas rheinhardtii and Synechocystis PCC 6803 as analysed by light-induced gas exchange transients. Int J Hydr Energ 27:1229-1237
15. Cournac L, Guedeney G, Peltier G, Vignais PM (2004) Sustained photoevolution of molecular hydrogen in a mutant of Synechocystis sp. Strain PCC 6803 deficient in the type I NADPH-dehydrogenase complex. J Bacteriol 186:1737-1746
16. Delwiche CF, Palmer JD (1997) The origin of plastids and their spread via secondary symbiosis. In: Bhattacharya D (ed) The origin of algae and their plastids. Springer Verlag, Heidelberg, pp 53-86
17. Dupuis A, Prieur I, Lunardi J (2001) Toward a characterization of the connecting module of complex I. J Bioenerg Biomembr 33:159-168
18. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package), version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle
19. Figge RM, Cassier-Chauvat C, Chauvat F, Cerff R (2000) The carbon metabolism-controlled Synechocystis gap2 gene harbours a conserved enhancer element and a gram-positive-like - 16 promotor box retained in some chloroplast genes. Mol Microbiol 36:44-54
20. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279-284
21. Florin L, Tsokoglou A, Happe T (2001) A novel type of iron hydrogenase in the green alga Scenedesmus obliquus is linked to the photosynthetic electron transport chain. J Biol Chem 276:6125-6132
22. Gaffron H, Rubin J (1942) Fermentative and photochemical production of hydrogen in algae. J Gen Physiol 26:219-240
23. Gupta RS (1998) Protein phylogenies and signature sequences: A reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62:1435-1491
24. Gupta RS (2003) Evolutionary relationship among photosynthetic bacteria. Photosynth Res 76:173-183
25. Gupta RS, Mukhtar T, Singh B (1999) Evolutionary relationships among photosynthetic prokaryotes (Heliobacterium chlorum, Chloroflexus aurantiacus, cyanobacteria, Chlorobium tepidum and proteobacteria): implications regarding the origin of photosynthesis. Mol Microbiol 32:893-906
26. Gutekunst K, Phunpruch S, Schwarz C, Schuchardt S, Schulz-Friedrich R, Appel J (2005) LexA regulates the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 as a transcription activator. Mol Microbiol 58:810-823
27. Horner DS, Foster PG, Embley TM (2000) Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol Biol Evol 17:1695-1709
28. Horner DS, Heil B, Happe T, Embley TM (2002) Iron hydrogenases - ancient enzymes in modern eukaryotes. Trends Biochem Sci 27:148-153
29. Houchins JP (1984) The physiology and biochemistry of hydrogen metabolism in cyanobacteria. Biochim Biophys Acta 768:227-255
30. Jones RF, Speer HL, Kury W (1963) Studies on the growth of the red alga Porphyridium cruentum. Phys Plant 16:636-643
31. Kovacs KL, Kovacs AT, Maroti G, Meszaros LS, Balogh J, Latinovics D, Fulop A, David R, Doroghazi E, Rakhely G (2005) The hydrogenases of Thiocapsa roseopersicina. Biochem Soc Trans 33:61-63
32. Liebl U, Mockensturm-Wilson M, Trost JT, Brune DC, Blankenship RE, Vermaas W (1993) Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis: structural implications and relations to other photosystems. Proc Natl Acad Sci USA 90:7124-7128
33. 2 by wildtype Anabaena sp. PCC 7120 and a hydrogen uptake deficient mutant: from laboratory experiments to outdoor culture. Int J Hydr Energ 27:1271-1281
34. Martin W, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37-41
35. Mazon G, Lucena JM, Campoy S, de Fernandez Henestrosa AR, Candau P, Barbe J (2004) LexA-binding sequences in gram-positive and cyanobacteria are closely related. Mol Gen Genomics 271:40-49
36. 2 photoproduction activities under nongrowing conditions in an aerobic nitrogen-fixing unicellular cyanobacterium Synechococcus sp. Curr Microbiol 30:1-6
37. Moreira D, Lopez-Garcia P (1998) Symbiosis between methanogenic archaea and δ-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J Mol Evol 47:517-530
38. Notredame C, Higgins D, Heringa J (2000) T-Coffee: a novel method for multiple sequence alignments. J Mol Biol 302:205-217
39. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299-304
40. Olsen JM, Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosynth Res 80:373-386
41. Oren A, Padan E (1978) Induction of anaerobic, photoautotrophic growth in the cyanobacterium Oscillatoria limnetica. J Bacteriol 133:558-563
42. Padan E (1979) Facultative anoxygenic photosynthesis in cyanobacteria. Annu Rev Plant Physiol 30:27-40
43. Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63:106-127
44. Pierson BK, Olson JM (1987) Photosynthetic bacteria. In: Amesz J (ed) New comprehensive biochemistry-photosynthesis, Vol 15. Amsterdam, pp 21-42
45. Posewitz MC, King PW, Smolinski SL, Zhang L, Seibert M, Ghirardi ML (2004) Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J Biol Chem 279:25711-25720
46. Raymond J, Zhaxybayeva O, Gogarten JP, Gerdes SY, Blankenship RE (2002) Whole genome analysis of photosynthetic prokaryotes. Science 298:1616-1620
47. Raymond J, Zhaxybayeva O, Gogarten JP, Blankenship RE (2003) Evolution of photosynthetic prokaryotes: a maximum-likelihood mapping approach. Phil Trans R Soc Lond B 358:223-230
48. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1-61
49. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
50. Shima S, Lyon EJ, Sordel-Klippert M, Kauss M, Kahnt J, Thauer RK, Steinbach K, Xie X, Verdier L, Griesinger C (2004) The cofactor of the iron-sulfur cluster free hydrogenase hmd: structure of the light-inactivation product. Angew Chem Int Ed Engl 43:2547-2551
51. Stal LJ, Moezelaar R (1997) Fermentation in cyanobacteria. FEMS Microbiol Rev 21:179-211
52. 2 photoproduction capability in a synchronously grown aerobic nitrogen-fixing cyanobacterium Synechococcus sp. Miami BG 045311. Arch Microbiol 158:1-4
53. Tamagnini P, Troshina O, Oxelfelt F, Salema R, Lindblad P (1997) Hydrogenases in Nostoc sp. strain PCC 73102, a strain lacking a bidirectional enzyme. Appl Environ Microbiol 63:1801-1807
54. Tamagnini P, Costa JL, Almeida L, Oliveira MJ, Salema R, Lindblad P (2000) Diversity of cyanobacterial hydrogenases, a molecular approach. Curr Microbiol 40:356-361
55. Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wünschiers R, Lindblad P (2002) Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev 66:1-20
56. Thompson JD, Higgins DG, Gibson TJ (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
57. van der Oost J, Cox RP (1987) Hydrogenase activtiy in nitrate grown cells of the unicellular cyanobacterium Cyanothece PCC 7822. Arch Microbiol 151:40-43
58. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455-501