1932
0

Annual Review of Microbiology

Volume 63, 2009

A Life with Acetogens, Thermophiles, and Cellulolytic Anaerobes

Abstract

Frankly, I was surprised to receive an invitation to write a prefatory chapter for the . I have read several such chapters written by outstanding researchers, many of whom I know and admire. I did not think I belonged to such a preeminent group. In my view, my contributions to the physiology and biochemistry of anaerobic thermophilic bacteria and, more lately, to anaerobic fungi are modest compared to the contribution made by other authors of prefatory chapters. I am honored to write about my life and my work, and I hope that those who read this chapter will sense how exciting and rewarding they have been.

Keyword(s): acetyl-CoA pathway, anaerobic fungi, Autobiography, cellulosomes, clostridia, CO2 fixation, corrinoids, tetrahydrofolates
Loading

Article metrics loading...

/content/journals/10.1146/annurev.micro.091208.073617
2009-10-13
2025-06-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/63/1/annurev.micro.091208.073617.html?itemId=/content/journals/10.1146/annurev.micro.091208.073617&mimeType=html&fmt=ahah

Literature Cited

  1. Allen MB. 1.  1953. The thermophilic aerobic sporeforming bacteria. Bacteriol. Rev. 17:125–73 [Google Scholar]
  2. Andreesen JR, Gottschalk G, Schlegel HG. 2.  1970. Clostridium formicoaceticum nov. spec. isolation, description and distinction from C. aceticum and C. thermoaceticum. Arch. Mikrobiol. 72:154–74 [Google Scholar]
  3. Andreesen JR, Makdessi K. 3.  2008. Tungsten, the surprisingly positively acting heavy metal element for prokaryotes. Ann. N. Y. Acad. Sci. 1125:215–29 [Google Scholar]
  4. Andreesen JR, Schaupp A, Neurauter C, Brown A, Ljungdahl LG. 4.  1973. Fermentation of glucose, fructose, and xylose by Clostridium thermoaceticum: effect of metals on growth yield, enzymes, and the synthesis of acetate from CO2. J. Bacteriol. 114:743–51 [Google Scholar]
  5. Barker HA, Kamen MD. 5.  1945. Carbon dioxide utilization in the synthesis of acetic acid by Clostridium thermoaceticum. Proc. Natl. Acad. Sci. USA 31:219–25 [Google Scholar]
  6. Bayer EA, Belaich JP, Shoham Y, Lamed R. 6.  2004. The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu. Rev. Microbiol. 58:521–54 [Google Scholar]
  7. Bayer EA, Morag E, Lamed R. 7.  1994. The cellulosome—a treasure-trove for biotechnology. Trends Biotechnol. 12:379–86 [Google Scholar]
  8. Borneman WS, Akin DE, Ljungdahl LG. 8.  1989. Fermentation products and plant cell wall-degrading enzymes produced by monocentric and polycentric anaerobic ruminal fungi. Appl. Environ. Microbiol. 55:1066–73 [Google Scholar]
  9. Brock TD, Freeze H. 9.  1969. Thermus aquaticus gen. n. and sp. n., a nonsporulating extreme thermophile. J. Bacteriol. 98:289–97 [Google Scholar]
  10. Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J. 10.  et al. 1994. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int. J. Syst. Bacteriol. 44:812–26 [Google Scholar]
  11. Consden R, Gordon AH, Martin AJ. 11.  1944. Qualitative analysis of proteins: a partition chromatographic method using paper. Biochem. J. 38:224–32 [Google Scholar]
  12. Cormier MJ. 12.  2007. My Journey Into, Through and Beyond the Ivory Tower Chandler, AZ: OPA Publ99 pp. [Google Scholar]
  13. Das A, Fu ZQ, Tempel W, Liu ZJ, Chang J. 13.  et al. 2007. Characterization of a corrinoid protein involved in the C1 metabolism of strict anaerobic bacterium Moorella thermoacetica. Proteins 67:167–76 [Google Scholar]
  14. Das A, Silaghi-Dumitrescu R, Ljungdahl LG, Kurtz DM Jr. 14.  2005. Cytochrome bd oxidase, oxidative stress, and dioxygen tolerance of the strictly anaerobic bacterium Moorella thermoacetica. J. Bacteriol. 187:2020–29 [Google Scholar]
  15. Demain AL, Newcomb M, Wu JHD. 15.  2005. Cellulose, clostridia, and ethanol. Microbiol. Mol. Biol. Rev. 69:124–54 [Google Scholar]
  16. Diekert GB, Thauer RK. 16.  1978. Carbon monoxide oxidation by Clostridium thermoaceticum and Clostridium formicoaceticum. J. Bacteriol. 136:597–606 [Google Scholar]
  17. Drake HL. 17.  1982. Demonstration of hydrogenase in extracts of the homoacetate-fermenting bacterium Clostridium thermoaceticum. J. Bacteriol. 150:702–9 [Google Scholar]
  18. Drake HL, Gössner AS, Daniel SL. 18.  2008. Old acetogens, new light. Ann. N. Y. Acad. Sci. 1125:100–28 [Google Scholar]
  19. Drake HL, Hu SI, Wood HG. 19.  1981. Purification of five components from Clostridium thermoaceticum which catalyze synthesis of acetate from pyruvate and methyltetrahydrofolate. Properties of phosphotransacetylase. J. Biol. Chem. 256:11137–44 [Google Scholar]
  20. Dürre P, Andreesen JR. 20.  1983. Purine and glycine metabolism by purinolytic clostridia. J. Bacteriol. 154:192–99 [Google Scholar]
  21. Edman P. 21.  1945. On the purification and chemical composition of hypertensin (angiotonin). Arkiv. Kem. Mineral. Geol. 22A:1–52 [Google Scholar]
  22. Edman P. 22.  1949. A method for the determination of amino acid sequence in peptides. Arch. Biochem. 22:475 [Google Scholar]
  23. El-Ghazzawi E. 23.  1967. New isolation of Clostridium aceticum Wieringa and studies on the metabolic physiology. Arch. Mikrobiol. 57:1–19 [Google Scholar]
  24. Elsden SR. 24.  1962. Photosynthesis and lithotophic carbon dioxide fixation. The Bacteria IC Gunsalus, RY Stainer 1–40 New York: Academic [Google Scholar]
  25. Enebo L. 25.  1943. Om termofil cellulosajäsning I. Svensk Kem. Tidskrift 5:144–51 [Google Scholar]
  26. Enebo L. 26.  1951. On three bacteria connected with thermophilic cellulose fermentation. Physiol. Plant. 4:652–66 [Google Scholar]
  27. Enebo L, Sandegren E, Ljungdahl LG. 27.  1953. Cell wall decomposing enzymes of barley and malt. II. Cellulase increase during germination and influence of sugars on cellulase activity. J. Inst. Brew. 59:205–11 [Google Scholar]
  28. Fontaine FE, Peterson WH, McCoy E, Johnson MJ, Ritter GJ. 28.  1942. A new type of glucose fermentation by Clostridium thermoaceticum. J. Bacteriol. 43:701–15 [Google Scholar]
  29. Friedrich W, Bernhauer K. 29.  1956. Chemistry and biochemistry of cobalamines. 1. Alkylation of vitamin B12-factor III and vitamin B12. Chem. Ber. 89:2030–44 [Google Scholar]
  30. Gottwald M, Andreesen JR, LeGall J, Ljungdahl LG. 30.  1975. Presence of cytochrome and menaquinone in Clostridium formicoaceticum and Clostridium thermoaceticum. J. Bacteriol. 122:325–28 [Google Scholar]
  31. Guest JR, Friedman S, Woods DD, Smith EL. 31.  1962. A methyl analogue of cobamide coenzyme in relation to methionine synthesis by bacteria. Nature 195:340–42 [Google Scholar]
  32. Hugenholtz J, Ljungdahl LG. 32.  1990. Metabolism and energy generation in homoacetogenic clostridia. FEMS Microbiol. Rev. 7:383–89 [Google Scholar]
  33. Irion E, Ljungdahl L. 33.  1965. Isolation of factor 3m coenzyme and cobyric acid coenzyme plus other B12 factors from Clostridium thermoaceticum. Biochemistry 4:2780–90 [Google Scholar]
  34. Kataeva IA, Uversky VN, Brewer JM, Schubot F, Rose JP. 34.  et al. 2004. Interactions between immunoglobulin-like and catalytic modules in Clostridium thermocellum cellulosomal cellobiohydrolase CbhA. Protein Eng. Des. Select. 17:759–69 [Google Scholar]
  35. Kerby R, Zeikus JG. 35.  1983. Growth of Clostridium thermoaceticum on H2/CO2 or CO as energy source. Curr. Microbiol. 8:27–30 [Google Scholar]
  36. Lamed R, Setter E, Bayer EA. 36.  1983. Characterization of a cellulose-binding, cellulase-containing complex in Clostridium thermocellum. J. Bacteriol. 156:828–36 [Google Scholar]
  37. Lentz K, Wood HG. 37.  1955. Synthesis of acetate from formate and carbon dioxide by Clostridium thermoaceticum. J. Biol. Chem. 215:645–54 [Google Scholar]
  38. Ljungdahl L. 38.  1981. Trace elements and the synthesis of acetate by Clostridium thermoaceticum. Science and Scientists: Essays by Biochemists, Biologists and Chemists M Kageyama, K Nakamura, T Oshima, T Uchida 89–96 Tokyo: Jpn. Sci. Soc. Press [Google Scholar]
  39. Ljungdahl L, Irion E, Wood HG. 39.  1965. Total synthesis of acetate from CO2. I. Co-methylcobyric acid and CO-(methyl)-5-methoxybenzimidazolylcobamide as intermediates with Clostridium thermoaceticum. Biochemistry 4:2771–80 [Google Scholar]
  40. Ljungdahl L, Irion E, Wood HG. 40.  1966. Role of corrinoids in the total synthesis of acetate from CO2 by Clostridium thermoaceticum. Fed. Proc. 25:1642–48 [Google Scholar]
  41. Ljungdahl L, Sandegren E. 41.  1950. Free amino acid in brewing materials. Acta Chem. Scand. 4:1150 [Google Scholar]
  42. Ljungdahl L, Wood HG. 42.  1963. Two thermophilic exchange reactions between pyruvate-CO2 and formate-CO2 in Clostridium thermoaceticum. Bact. Proc.109 [Google Scholar]
  43. Ljungdahl L, Wood HG, Racker E, Couri D. 43.  1961. Formation of unequally labeled fructose 6-phosphate by an exchange reaction catalyzed by transaldolase. J. Biol. Chem. 236:1622–25 [Google Scholar]
  44. Ljungdahl LG. 44.  1979. Physiology of thermophilic bacteria. Adv. Microb. Physiol. 19:149–243 [Google Scholar]
  45. Ljungdahl LG. 45.  1986. The autotrophic pathway of acetate synthesis in acetogenic bacteria. Annu. Rev. Microbiol. 40:415–50 [Google Scholar]
  46. Ljungdahl LG. 46.  2008. The cellulase/hemicellulase system of the anaerobic fungus Orpinomyces PC-2 and aspects of its applied use. Ann. N. Y. Acad. Sci. 1125:308–21 [Google Scholar]
  47. Ljungdahl LG, Andreesen JR. 47.  1976. Reduction of CO2 to acetate in homo acetate fermenting clostridia and the involvement of tungsten in formate dehydrogenase. Microbial Production and Utilization of Gases HG Schlegel, G Gottschalk, N Pfennig 163–72 Göttingen: E. Goltze KG [Google Scholar]
  48. Ljungdahl LG, Bryant F, Carreira L, Saiki T, Wiegel J. 48.  1981. Some aspects of thermophilic and extreme thermophilic anaerobic microorganisms. Basic Life Sci. 18:397–419 [Google Scholar]
  49. Ljungdahl LG, Eriksson K-E. 49.  1985. Ecology of microbial cellulose degradation. Adv. Microb. Ecol. 8:237–99 [Google Scholar]
  50. Ljungdahl LG, Op den Camp HJM, Gilbert HJ, Harhangi HR, Steenbakkers PJM, Li X-L. 50.  2006. Cellulosomes of anaerobic fungi. Cellulosome V Uversky, IA Kataeva 271–303 New York: Novo Sci. Publ. [Google Scholar]
  51. Ljungdahl LG, Sherod D. 51.  1974. Proteins from thermophilic microorganisms. Extreme Environments. Mechanisms of Microbial Adaptation MR Heinrich 147–87 New York: Academic [Google Scholar]
  52. Ljungdahl LG, Wood HG. 52.  1969. Total synthesis of acetate from CO2 by heterotrophic bacteria. Annu. Rev. Microbiol. 23:515–38 [Google Scholar]
  53. Martin W, Russell MJ. 53.  2007. On the origin of biochemistry at an alkaline hydrothermal vent. Philos. Trans. R. Soc. London B Biol. Sci. 362:1887–925 [Google Scholar]
  54. Mayer F, Coughlan MP, Mori Y, Ljungdahl LG. 54.  1987. Macromolecular organization of the cellulolytic enzyme complex of Clostridium thermocellum as revealed by electron microscopy. Appl. Environ. Microbiol. 53:2785–92 [Google Scholar]
  55. Morton TA, Runquist JA, Ragsdale SW, Shanmugasundaram T, Wood HG, Ljungdahl LG. 55.  1991. The primary structure of the subunits of carbon monoxide dehydrogenase/acetyl-CoA synthase from Clostridium thermoaceticum. J. Biol. Chem. 266:23824–28 [Google Scholar]
  56. Noble EP, Stjernohlm R, Ljungdahl L. 56.  1961. Carbohydrate metabolism in leucocytes. III. Carbon dioxide incorporation in the rabbit polymorphonuclear leukocyte. Biochim. Biophys. Acta 49:593–95 [Google Scholar]
  57. O'Brien WE, Ljungdahl LG. 57.  1972. Fermentation of fructose and synthesis of acetate from carbon dioxide by Clostridium formicoaceticum. J. Bacteriol. 109:626–32 [Google Scholar]
  58. Orpin CG. 58.  1975. Studies on the rumen flagellate Neocallimastix frontalis. J. Gen. Microbiol. 91:249–62 [Google Scholar]
  59. Partridge SM, Blombäck B. 59.  1979. Pehr Victor Edman, 14 April 1916–19 March 1977. Biogr. Mem. Fellows R. Soc. 25:241–65 [Google Scholar]
  60. Payne WJ. 60.  1970. Energy yields and growth of heterotrophs. Annu. Rev. Microbiol. 24:17–52 [Google Scholar]
  61. Pierce E, Xie G, Barabote RD, Saunders E, Han CS. 61.  et al. 2008. The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum). Environ. Microbiol. 10:2550–73 [Google Scholar]
  62. Pinsent J. 62.  1954. The need for selenite and molybdate in the formation of formic dehydrogenase by members of the coli-aerogenes group of bacteria. Biochem. J. 57:10–16 [Google Scholar]
  63. Poston JM, Kuratomi K, Stadtman ER. 63.  1964. Methyl-vitamin B12 as a source of methyl groups for the synthesis of acetate by cell-free extracts of Clostridium thermoaceticum. Ann. N. Y. Acad. Sci. 112:804–6 [Google Scholar]
  64. Ragsdale SW. 64.  2007. Nickel and the carbon cycle. J. Inorg. Biochem. 101:1657–66 [Google Scholar]
  65. Ragsdale SW, Clark JE, Ljungdahl LG, Lundie LL, Drake HL. 65.  1983. Properties of purified carbon monoxide dehydrogenase from Clostridium thermoaceticum, a nickel, iron-sulfur protein. J. Biol. Chem. 258:2364–69 [Google Scholar]
  66. Ragsdale SW, Ljungdahl LG, DerVartanian DV. 66.  1983. 13C and 61Ni isotope substitutions confirm the presence of a nickel (III)-carbon species in acetogenic CO dehydrogenases. Biochem. Biophys. Res. Commun. 115:658–65 [Google Scholar]
  67. Ragsdale SW, Wood HG. 67.  1985. Acetate biosynthesis by acetogenic bacteria. Evidence that carbon monoxide dehydrogenase is the condensing enzyme that catalyzes the final steps of the synthesis. J. Biol. Chem. 260:3970–77 [Google Scholar]
  68. Russell MJ, Martin W. 68.  2004. The rocky roots of the acetyl-CoA pathway. Trends Biochem. Sci. 29:358–63 [Google Scholar]
  69. Schulman M, Parker D, Ljungdahl LG, Wood HG. 69.  1972. Total synthesis of acetate from CO2. V. Determination by mass analysis of the different types of acetate formed from 13CO2 by heterotrophic bacteria. J. Bacteriol. 109:633–44 [Google Scholar]
  70. Shannon KW, Rabinowitz JC. 70.  1988. Isolation and characterization of the Saccharomyces cerevisiae MIS1 gene encoding mitochondrial C1-tetrahydrofolate synthase. J. Biol. Chem. 263:7717–25 [Google Scholar]
  71. Steenbakkers PJ, Li XL, Ximenes EA, Arts JG, Chen H. 71.  et al. 2001. Noncatalytic docking domains of cellulosomes of anaerobic fungi. J. Bacteriol. 183:5325–33 [Google Scholar]
  72. Thauer RK. 72.  2007. Microbiology. A fifth pathway of carbon fixation. Science 318:1732–33 [Google Scholar]
  73. Uversky V, Kataeva IA. 73.  2006. Cellulosome New York: Nova Sci. Publ.317 pp. [Google Scholar]
  74. Whitman WB, Coleman DC, Wiebe WJ. 74.  1998. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95:6578–83 [Google Scholar]
  75. Wiegel J, Braun M, Gottschalk G. 75.  1981. Clostridium thermoautotrophicum species novum, a thermophile producing acetate from molecular hydrogen and carbon dioxide. Curr. Microbiol. 5:255–60 [Google Scholar]
  76. Wiegel J, Dykstra M. 76.  1984. Clostridium thermocellum: adhesion and sporulation while adhered to cellulose and hemicellulose. Appl. Microbiol. Biotechnol. 20:59–65 [Google Scholar]
  77. Wiegel J, Ljungdahl LG. 77.  1981. Thermoanaerobacter ethanolicus gen. nov., spec. nov., a new, extreme thermophilic, anaerobic bacterium. Arch. Microbiol. 128:343–48 [Google Scholar]
  78. Wiegel J, Ljungdahl LG, Rawson JR. 78.  1979. Isolation from soil and properties of the extreme thermophile Clostridium thermohydrosulfuricum. J. Bacteriol. 139:800–10 [Google Scholar]
  79. Wiegel J, Maier RJ, Adams MWW. 79.  2008. Incredible Anaerobes: From Physiology to Genomics to Fuels 1125 Boston: Blackwell Publ./NY Acad. Sci.373 pp. [Google Scholar]
  80. Wieringa KT. 80.  1936. Over het verdwijnen van waterstof en koolzuur onder anaerobe voorwaarden. Antonie Leeuwenhoek 3:263–73 [Google Scholar]
  81. Woese CR, Kandler O, Wheelis ML. 81.  1990. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. USA 87:4576–79 [Google Scholar]
  82. Wood HG. 82.  1952. A study of carbon dioxide fixation by mass determination of the types of C13-acetate. J. Biol. Chem. 194:905–31 [Google Scholar]
  83. Wood HG. 83.  1952. Fermentation of 3, 4–14C-and 1–14C-labeled glucose by Clostridium thermoaceticum. J. Biol. Chem. 199:579–83 [Google Scholar]
  84. Wood HG, Katz J. 84.  1958. The distribution of 14C in the hexose phosphates and the effect of recycling in the pentose cycle. J. Biol. Chem. 233:1279–82 [Google Scholar]
  85. Wood HG, Ljungdahl LG. 85.  1991. Autotrophic character of the acetogenic bacteria. Variations in Autotrophic Life JM Shively, LL Barton 201–50 San Diego: Academic [Google Scholar]
  86. Wood HG, Stjernholm R. 86.  1962. Assimilation of carbon dioxide by heterotrophic organisms. The Bacteria IC Gunsalus, RY Stainer 41–117 New York: Academic [Google Scholar]
  87. Yamamoto I, Saiki T, Liu SM, Ljungdahl LG. 87.  1983. Purification and properties of NADP-dependent formate dehydrogenase from Clostridium thermoaceticum, a tungsten-selenium-iron protein. J. Biol. Chem. 258:1826–32 [Google Scholar]
  88. Zverlov VV, Velikodvorskaya GV, Schwarz WH, Bronnenmeier K, Kellermann J, Staudenbauer WL. 88.  1998. Multidomain structure and cellulosomal localization of the Clostridium thermocellum cellobiohydrolase CbhA. J. Bacteriol. 180:3091–99 [Google Scholar]
  89. Ljungdahl L, Wood HG. 89.  1965. Incorporation of C14 from carbon dioxide into sugar phosphates, carboxylic acids, and amino acids by Clostridium thermoaceticum. J. Bacteriol 89:1055–64 [Google Scholar]
  90. Kataeva IA, Blum DL, Li XL, Ljungdahl LG. 90.  2001. Do domain interactions of glycosyl hydrolases from Clostridium thermocellum contribute to protein stability?. Protein Eng. 14:167–72 [Google Scholar]
/content/journals/10.1146/annurev.micro.091208.073617
Loading
A Life with Acetogens, Thermophiles, and Cellulolytic Anaerobes
Annual Review of Microbiology 63, 1 (2009); https://doi.org/10.1146/annurev.micro.091208.073617
/content/journals/10.1146/annurev.micro.091208.073617
/content/journals/10.1146/annurev.micro.091208.073617
Loading

Data & Media loading...

Most Cited Most Cited RSS feed

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