Selenium controls transcription of paralogous formate dehydrogenase genes in the termite gut acetogen, Treponema primitia

Environmental Microbiology

Volumn 12, Issue 8, 2010, Pages 2245-2258

  Matson, Eric G ^a   Zhang, Xinning ^a   Leadbetter, Jared R ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; CARBON DIOXIDE; FORMATE DEHYDROGENASE; SELENIUM; SELENOCYSTEINE; TETRAHYDROFOLIC ACID DERIVATIVE;

ANIMAL; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; CONFORMATION; DNA SEQUENCE; ENZYMOLOGY; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOPTERA; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SYMBIOSIS; TREPONEMA;

ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; CARBON DIOXIDE; DNA, BACTERIAL; FORMATE DEHYDROGENASES; GASTROINTESTINAL TRACT; GENES, BACTERIAL; GENOME, BACTERIAL; ISOPTERA; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; SELENIUM; SELENOCYSTEINE; SEQUENCE ANALYSIS, DNA; SYMBIOSIS; TETRAHYDROFOLATES; TREPONEMA;

ISOPTERA; MOORELLA THERMOACETICA; SPIROCHAETALES; TREPONEMA; TREPONEMA PRIMITIA;

EID: 77955244141     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02188.x     Document Type: Article

References (80)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
2. Andrews SC, Berks BC, McClay J, Ambler A, Quail MA, Golby P, Guest JR. A 12-cistron Escherichia coli operon (hyf) encoding a putative proton-translocating formate hydrogenlyase system. Microbiology 1997, 143:3633-3647.
3. Axley MJ, Böck A, Stadtman TC. Catalytic properties of an Escherichia coli formate dehydrogenase mutant in which sulfur replaces selenium. Proc Natl Acad Sci USA 1991, 88:8450-8454.
4. Berghöfer Y, Agha-Amiri K, Klein A. Selenium is involved in the negative regulation of the expression of selenium-free [NiFe] hydrogenases in Methanococcus voltae. Mol Gen Genet 1994, 242:369-373.
5. Berry MJ, Maia AL, Kieffer JD, Harney JW, Larsen PR. Substitution of cysteine for selenocysteine in type I iodothyronine deiodinase reduces the catalytic efficiency of the protein but enhances its translation. Endocrinology 1992, 131:1848-1852.
6. Bignell DE. Introduction to symbiosis. Termites: Evolution, Sociality, Symboses, Ecology 2000, 189-208. Abe TBignell DEHigashi M., Dordrecht, the Netherlands, Kluwer Academic Publishers
7. Brauman A, Kane MD, Labat M, Breznak JA. Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 1992, 257:1384-1387.
8. Breznak J. Biology of nonpathogenic, host-associated spirochetes. CRC Crit Rev Microbiol 1973, 2:457-489.
9. Breznak JA. Intestinal microbiota of termites and other xylophagous insects. Annu Rev Microbiol 1982, 36:323-343.
10. Breznak JA, Switzer JM. Acetate synthesis from H2 plus CO2 by termite gut microbes. Appl Environ Microbiol 1986, 52:623-630.
11. Drake HL, Daniel SL. Physiology of the thermophilic acetogen Moorella thermoacetica. Res Microbiol 2004, 155:869-883.
12. Ebert A, Brune A. Hydrogen concentration profiles at the oxic-anoxic interface: a microsensor study of the hindgut of the wood-feeding lower termite Reticulitermes flavipes (Kollar). Appl Environ Microbiol 1997, 63:4039-4046.
13. Edgar RC. muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
14. Ferry JG. Formate dehydrogenase: microbiology, biochemistry and genetics. Autotrophic Microbiology and One-Carbon Metabolism 1990a, 117-141. Codd GDijkhuizen LTabita FR., Dordrecht, the Netherlands, Kluwer Academic
15. Ferry JG. Formate dehydrogenase. FEMS Microbiol Rev 1990b, 7:377-382.
16. Fourmy D, Guittet E, Yoshizawa S. Structure of prokaryotic SECIS mRNA hairpin and its interaction with elongation factor SelB. J Mol Biol 2002, 324:137-150.
17. Fraser CM, Norris SJ, Weinstock GM, White O, Sutton GG, Dodson R. Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 1998, 281:375-388.
18. Frey M. Hydrogenases: hydrogen-activating enzymes. Chembiochem 2002, 3:153-160.
19. Fuchs G. CO2 fixation in acetogenic bacteria: variations on a theme. FEMS Microbiol Rev 1986, 39:181-213.
20. Gladyshev VN, Boyington JC, Khangulov SV, Grahame DA, Stadtman TC, Sun PD. Characterization of crystalline formate dehydrogenase H from Escherichia coli. Stabilization, EPR spectroscopy, and preliminary crystallographic analysis. J Biol Chem 1996, 271:8095-8100.
21. Graber JR, Breznak JA. Physiology and nutrition of Treponema primitia, an H2/CO2-acetogenic spirochete from termite hindguts. Appl Environ Microbiol 2004, 70:1307-1314.
22. Graber JR, Breznak JA. Folate cross-feeding supports symbiotic homoacetogenic spirochetes. Appl Environ Microbiol 2005, 71:1883-1889.
23. Graber JR, Leadbetter JR, Breznak JA. Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the first spirochetes isolated from termite guts. Appl Environ Microbiol 2004, 70:1315-1320.
24. Gromer S, Johansson L, Bauer H, Arscott LD, Rauch S, Ballou DP. Active sites of thioredoxin reductases: why selenoproteins? Proc Natl Acad Sci USA 2003, 100:12618-12623.
25. Hakobyan M, Sargsyan H, Bagramyan K. Proton translocation coupled to formate oxidation in anaerobically grown fermenting Escherichia coli. Biophys Chem 2005, 115:55-61.
26. Halboth S, Klein A. Methanococcus voltae harbors four gene clusters potentially encoding two [NiFe] and two [NiFeSe] hydrogenases, each of the cofactor F420-reducing or F420-non-reducing types. Mol Gen Genet 1992, 233:217-224.
27. Hazebrouck S, Camoin L, Faltin Z, Strosberg AD, Eshdat Y. Substituting selenocysteine for catalytic cysteine 41 enhances enzymatic activity of plant phospholipid hydroperoxide glutathione peroxidase expressed in Escherichia coli. J Biol Chem 2000, 275:28715-28721.
28. Heider J, Böck A. Targeted insertion of selenocysteine into the alpha subunit of formate dehydrogenase from Methanobacterium formicicum. J Bacteriol 1992, 174:659-663.
29. Hespell RB, Canale-Parola E. Carbohydrate metabolism in Spirochaeta stenostrepta. J Bacteriol 1970, 103:216-226.
30. Hoehler TM, Bebout BM, Des Marais DJ. The role of microbial mats in the production of reduced gases on the early Earth. Nature 2001, 412:324-327.
31. Jones JB, Stadtman TC. Selenium-dependent and selenium-independent formate dehydrogenases of Methanococcus vannielii. Separation of the two forms and characterization of the purified selenium-independent form. J Biol Chem 1981, 256:656-663.
32. Kim HY, Fomenko DE, Yoon YE, Gladyshev VN. Catalytic advantages provided by selenocysteine in methionine-S-sulfoxide reductases. Biochemistry 2006, 45:13697-13704.
33. Krol A. Evolutionarily different RNA motifs and RNA-protein complexes to achieve selenoprotein synthesis. Biochimie 2002, 84:765-774.
34. Lacourciere GM, Mihara H, Kurihara T, Esaki N, Stadtman TC. Escherichia coli NifS-like proteins provide selenium in the pathway for the biosynthesis of selenophosphate. J Biol Chem 2000, 275:23769-23773.
35. Leadbetter JR, Schmidt TM, Graber JR, Breznak JA. Acetogenesis from H2 plus CO2 by spirochetes from termite guts. Science 1999, 283:686-689.
36. Lee SR, Bar-Noy S, Kwon J, Levine RL, Stadtman TC, Rhee SG. Mammalian thioredoxin reductase: oxidation of the C-terminal cysteine/selenocysteine active site forms a thioselenide, and replacement of selenium with sulfur markedly reduces catalytic activity. Proc Natl Acad Sci USA 2000, 97:2521-2526.
37. Li LF, Ljungdahl L, Wood HG. Properties of nicotinamide adenine dinucleotide phosphate-dependent formate dehydrogenase from Clostridium thermoaceticum. J Bacteriol 1966, 92:405-412.
38. Lilburn TG, Schmidt TM, Breznak JA. Phylogenetic diversity of termite gut spirochaetes. Environ Microbiol 1999, 1:331-345.
39. Liu Z, Reches M, Groisman I, Engelberg-Kulka H. The nature of the minimal 'selenocysteine insertion sequence' (SECIS) in Escherichia coli. Nucleic Acids Res 1998, 26:896-902.
40. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964.
41. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar. ARB: a software environment for sequence data. Nucleic Acids Res 2004, 32:1363-1371.
42. McHardy AC, Martin HG, Tsirigos A, Hugenholtz P, Rigoutsos I. Accurate phylogenetic classification of variable-length DNA fragments. Nat Methods 2007, 4:63-72.
43. Metanis N, Keinan E, Dawson PE. Synthetic seleno-glutaredoxin 3 analogues are highly reducing oxidoreductases with enhanced catalytic efficiency. J Am Chem Soc 2006, 128:16684-16691.
44. Mikx F. Environmental effects on the growth and proteolysis of Treponema denticola ATCC 33520. Oral Microbiol Immunol 1997, 12:249-253.
45. Miozzari G, Niederberger P, Hütter R. Tryptophan biosynthesis in Saccharomyces cerevisiae: control of the flux through the pathway. J Bacteriol 1978, 134:48-59.
46. Noll I, Müller S, Klein A. Transcriptional regulation of genes encoding the selenium-free [NiFe]-hydrogenases in the archaeon Methanococcus voltae involves positive and negative control elements. Genetics 1999, 152:1335-1341.
47. Ochman H, Medhora MM, Garza D, Hartl DL. Amplification of flanking sequences by inverse PCR. PCR Protocols: A Guide to Methods and Applications 1990, 219-227. Innis MA, Gelfand DH, Sninsky JJ, White TJ., San Diego, CA, USA, Academic Press
48. Odelson DA, Breznak JA. Volatile fatty acid production by the hindgut microbiota of xylophagous termites. Appl Environ Microbiol 1983, 45:1602-1613.
49. Odelson DA, Breznak JA. Cellulase and other polymer-hydrolyzing activities of Trichomitopsis termopsidis, a symbiotic protozoan from termites. Appl Environ Microbiol 1985a, 49:622-626.
50. Odelson DA, Breznak JA. Nutrition and growth-characteristics of Trichomitopsis termopsidis, a cellulolytic protozoan from termites. Appl Environ Microbiol 1985b, 49:614-621.
51. Ottesen EA, Hong JW, Quake SR, Leadbetter JR. Microfluidic digital PCR enables multigene analysis of individual environmental bacteria. Science 2006, 314:1464-1467.
52. Paster BJ, Dewhirst FE. Phylogenetic foundation of spirochetes. J Mol Microbiol Biotechnol 2000, 2:341-344.
53. Paster BJ, Dewhirst FE, Cooke SM, Fussing V, Poulsen LK, Breznak JA. Phylogeny of not-yet-cultured spirochetes from termite guts. Appl Environ Microbiol 1996, 62:347-352.
54. Pester M, Brune A. Expression profiles of fhs (FTHFS) genes support the hypothesis that spirochaetes dominate reductive acetogenesis in the hindgut of lower termites. Environ Microbiol 2006, 8:1261-1270.
55. Pester M, Brune A. Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts. ISME J 2007, 1:551-565.
56. Pierce E, Xie G, Barabote RD, Saunders E, Han CS, Detter JC. The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum). Environ Microbiol 2008, 10:2550-2573.
57. Pöhlschroeder M, Leschine SB, Canale-Parola E. Spirochaeta caldaria sp. nov., a thermophilic bacterium that enhances cellulose degradation by Clostridium thermocellum. Arch Microbiol 1994, 161:17-24.
58. Ragsdale SW, Pierce E. Acetogenesis and the Wood-Ljungdahl pathway of CO(2) fixation. Biochim Biophys Acta 2008, 1784:1873-1898.
59. Rother M, Böck A, Wyss C. Selenium-dependent growth of Treponema denticola: evidence for a clostridial-type glycine reductase. Arch Microbiol 2001, 177:113-116.
60. Rozen S, Skaletsky HJ. Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols: Methods in Molecular Biology 2000, 365-386. Krawetz S, Misener S., Totowa, NJ, USA, Humana Press
61. Salmassi TM, Leadbetter JR. Analysis of genes of tetrahydrofolate-dependent metabolism from cultivated spirochaetes and the gut community of the termite Zootermopsis angusticollis. Microbiology 2003, 149:2529-2537.
62. Schauer NL, Ferry JG. Properties of formate dehydrogenase in Methanobacterium formicicum. J Bacteriol 1982, 150:1-7.
63. Schink B, Lupton FS, Zeikus JG. Radioassay for hydrogenase activity in viable cells and documentation of aerobic hydrogen-consuming bacteria living in extreme environments. Appl Environ Microbiol 1983, 45:1491-1500.
64. Seshadri R, Myers GS, Tettelin H, Eisen JA, Heidelberg JF, Dodson RJ. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci USA 2004, 101:5646-5651.
65. Sonnhammer EL, Koonin EV. Orthology, paralogy and proposed classification for paralog subtypes. Trends Genet 2002, 18:619-620.
66. Sun J, Klein A. A lysR-type regulator is involved in the negative regulation of genes encoding selenium-free hydrogenases in the archaeon Methanococcus voltae. Mol Microbiol 2004, 52:563-571.
67. Thanbichler M, Böck A. The function of SECIS RNA in translational control of gene expression in Escherichia coli. EMBO J 2002, 21:6925-6934.
68. Thauer RK. CO(2)-reduction to formate by NADPH. The initial step in the total synthesis of acetate from CO(2) in Clostridium thermoaceticum. FEBS Lett 1972, 27:111-115.
69. Thauer RK, Jungermann K, Decker K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 1977, 41:100-180.
70. Tholen A, Brune A. Localization and in situ activities of homoacetogenic bacteria in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp.). Appl Environ Microbiol 1999, 65:4497-4505.
71. Tholen A, Brune A. Impact of oxygen on metabolic fluxes and in situ rates of reductive acetogenesis in the hindgut of the wood-feeding termite Reticulitermes flavipes. Environ Microbiol 2000, 2:436-449.
72. Valente FM, Almeida CC, Pacheco I, Carita J, Saraiva LM, Pereira IA. Selenium is involved in regulation of periplasmic hydrogenase gene expression in Desulfovibrio vulgaris Hildenborough. J Bacteriol 2006, 188:3228-3235.
73. Veres Z, Kim IY, Scholz TD, Stadtman TC. Selenophosphate synthetase. Enzyme properties and catalytic reaction. J Biol Chem 1994, 269:10597-10603.
74. Vorholt JA, Vaupel M, Thauer RK. A selenium-dependent and a selenium-independent formylmethanofuran dehydrogenase and their transcriptional regulation in the hyperthermophilic Methanopyrus kandleri. Mol Microbiol 1997, 23:1033-1042.
75. Warnecke F, Lüginbuhl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 2007, 450:560-565.
76. Yamin MA. Cellulose metabolism by the flagellate Trichonympha from a termite is independent of endosymbiotic bacteria. Science 1981, 211:58-59.
77. Yoshizawa S, Rasubala L, Ose T, Kohda D, Fourmy D, Maenaka K. Structural basis for mRNA recognition by elongation factor SelB. Nat Struct Mol Biol 2005, 12:198-203.
78. Zhang Y, Gladyshev VN. An algorithm for identification of bacterial selenocysteine insertion sequence elements and selenoprotein genes. Bioinformatics 2005, 21:2580-2589.
79. Zinoni F, Birkmann A, Stadtman TC, Böck A. Nucleotide sequence and expression of the selenocysteine-containing polypeptide of formate dehydrogenase (formate-hydrogen-lyase-linked) from Escherichia coli. Proc Natl Acad Sci USA 1986, 83:4650-4654.
80. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31:3406-3415.