On the Origin of Heterotrophy

Trends in Microbiology

Volumn 24, Issue 1, 2016, Pages 12-25

  Schönheit, Peter ^a   Buckel, Wolfgang ^b,c   Martin, William F ^d,e  

^a UNIVERSITY OF KIEL   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Amino acid fermentations; Archaeal type III RubisCO; Autotrophic origins; Hydrothermal vents; Purine fermentations

Indexed keywords

AMINO ACID; HYDROGEN; PURINE; PYRIMIDINE; RIBOSE; ARCHAEAL PROTEIN; BACTERIAL PROTEIN; CARBON;

AMINO ACID METABOLISM; ARCHAEON; BACTERIAL CELL; BIOGENESIS; CARBON METABOLISM; CELL METABOLISM; CHEMOAUTOTROPH; CHEMOHETEROTROPH; CLOSTRIDIA; ENERGY METABOLISM; ESCHERICHIA COLI; FERMENTATION; HETEROTROPHY; NONHUMAN; PRIORITY JOURNAL; REVIEW; THERMODYNAMICS; AUTOTROPHY; BACTERIUM; CHEMISTRY; EVOLUTION; HYDROTHERMAL VENT; METABOLISM;

ARCHAEA; ARCHAEAL PROTEINS; AUTOTROPHIC PROCESSES; BACTERIA; BACTERIAL PROTEINS; BIOLOGICAL EVOLUTION; CARBON; HETEROTROPHIC PROCESSES; HYDROGEN; HYDROTHERMAL VENTS; ORIGIN OF LIFE;

EID: 84955410245     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2015.10.003     Document Type: Review

References (115)

1. Say R.F., Fuchs G. Fructose 1,6-bisphosphate aldolase/phosphatase may be an ancestral gluconeogenic enzyme. Nature 2010, 464:1077-1081.
2. Fuchs G. Alternative pathways of carbon dioxide fixation: insights into the early evolution of life?. Annu. Rev. Microbiol. 2011, 65:631-658.
3. Bada J.L., Lazcano A. Some like it hot, but not the first biomolecules. Science 2002, 296:1982-1983.
4. Orgel L.E. The implausibility of metabolic cycles on the prebiotic earth. PLoS Biol. 2008, 6:e18.
5. Joyce G.F. RNA evolution and the origins of life. Nature 1989, 338:217-224.
6. Saladino R., et al. Formamide and the origin of life. Phys. Life Rev. 2012, 9:84-104.
7. Patel B.H., et al. Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism. Nat. Chem. 2015, 7:301-307.
8. Keller M.A., et al. Non-enzymatic glycolysis and pentose phosphate pathway-like reactions in a plausible Archean ocean. Mol. Syst. Biol. 2014, 10:725.
9. Shapiro R. Prebiotic cytosine synthesis: a critical analysis and implications for the origin of life. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:4396-4401.
10. McCollom T.M. Miller-Urey and beyond: what have we learned about prebiotic organic synthesis reactions in the past 60 years?. Annu. Rev. Earth Planet. Sci. 2013, 41:207-229.
11. Baross J.A., Hoffman S.E. Submarine hydrothermal vents and associated gradient environments as sites for the origin and evolution of life. Orig. Life Evol. Biosph. 1985, 15:327-345.
12. Wächtershäuser G. Groundworks for an evolutionary biochemistry - the iron-sulfur world. Prog. Biophys. Mol. Biol. 1992, 58:85-201.
13. Russel M.J., Hall A.J. The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J. Geol. Soc. London 1997, 154:377-402.
14. Martin W., Russell M.J. On the origin of biochemistry at an alkaline hydrothermal vent. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2007, 367:1887-1925.
15. Ragsdale S.W. Nickel-based enzyme systems. J. Biol. Chem. 2009, 284:18571-18575.
16. Peters J.W., Williams L.D. The origin of life: look up and look down. Astrobiology 2012, 12:1087-1092.
17. Sousa F.L., Martin W.F. Biochemical fossils of the ancient transition from geoenergetics to bioenergetics in prokaryotic one carbon compound metabolism. Biochim. Biophys. Acta 2014, 1837:964-981.
18. McDermott J., et al. Pathways for abiotic organic synthesis at submarine hydrothermal fields. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:7668-7672.
19. Schrenk M.O., et al. Serpentinization, carbon and deep life. Rev. Mineral. Geochem. 2013, 75:575-606.
20. McCollom T.M., Seewald J.S. Serpentinites, hydrogen, and life. Elements 2013, 9:129-134.
21. Amend J.P., McCollom T.M. Energetics of biomolecule synthesis on early Earth. Chemical Evolution II: From the Origins of Life to Modern Society 2009, 63-94. American Chemical Society. L. Zaikowski (Ed.).
22. Chivian D., et al. Environmental genomics reveals a single-species ecosystem deep within Earth. Science 2008, 322:275-278.
23. Chapelle F.H., et al. A hydrogen-based subsurface microbial community dominated by methanogens. Nature 2002, 415:312-315.
24. Lever M.A., et al. Acetogenesis in deep subseafloor sediments of the Juan de Fuca Ridge flank: a synthesis of geochemical, thermodynamic, and gene-based evidence. Geomicrobiol. J. 2010, 27:183-211.
25. Berg I.A., et al. Autotrophic carbon fixation in archaea. Nat. Rev. Microbiol. 2010, 8:447-460.
26. Lang S.Q., et al. Elevated concentrations of formate, acetate and dissolved organic carbon found at the Lost City hydrothermal field. Geochim. Cosmochim. Acta 2010, 74:941-952.
27. Proskurowski G., et al. Abiogenic hydrocarbon production at Lost City Hydrothermal Field. Science 2008, 319:604-607.
28. Lane N., Martin W.F. The origin of membrane bioenergetics. Cell 2012, 151:1406-1416.
29. Westall F., et al. Archean (3.33 Ga) microbe-sediment systems were diverse and flourished in a hydrothermal context. Geology 2015, 43:615-618.
30. Ueno Y., et al. Evidence from fluid inclusions for microbial methanogenesis in the early archaean era. Nature 2006, 440:516-519.
31. Kelly S., et al. Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes. Proc. R. Soc. Lond. B 2011, 278:1009-1018.
32. Raymann K., et al. The two-domain tree of life is linked to a new root for the Archaea. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:6670-6675.
33. 2 conversion by iron sulfide catalysts under sustainable conditions. Chem. Commun. 2015, 51:7501-7504.
34. Herschy B., et al. An origin-of-life reactor to simulate alkaline hydrothermal vents. J. Mol. Evol. 2014, 79:213-227.
35. Chyba C.F., et al. Cometary delivery of organic molecules to the early Earth. Science 1990, 249:366-373.
36. Sephton M.A. Organic compounds in carbonaceous meteorites. Nat. Prod. Rep. 2002, 19:292-311.
37. Fisher A.T. Marine hydrogeology: recent accomplishments and future opportunities. Hydrogeol. J. 2005, 13:69-97.
38. Stouthamer A.H. A theoretical study on the amount of ATP required for synthesis of microbial cell material. Antonie van Leeuwenhoek 1973, 39:545-565.
39. Biology of the Prokaryotes 1999, Thieme, Blackwell Science. J.W. Lengeler (Ed.).
40. Physiology of the Bacterial Cell 1990, Sinauer Associates. F.C. Neidhardt (Ed.).
41. Barker H.A. Fermentation of nitrogenous compounds. The Bacteria. A Treatise on Structure and Function 1961, 151-207. Academic Press. I.C. Gunsalus, R.Y. Stanier (Eds.).
42. Stickland L.H. Studies in the metabolism of the strict anaerobes (genus Clostridium): the chemical reactions by which Cl. sporogenes obtains its energy. Biochem. J. 1934, 28:1746-1759.
43. Andreesen J.R. Glycine metabolism in anaerobes. Antonie van Leeuwenhoek 1994, 66:223-237.
44. + translocating ferredoxin oxidation. Biochim. Biophys. Acta 2013, 1827:94-113.
45. Boiangiu C.D., et al. Sodium ion pumps and hydrogen production in glutamate fermenting anaerobic bacteria. J. Mol. Microbiol. Biotechnol. 2005, 10:105-119.
46. + oxidoreductase. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:18138-18142.
47. Hetzel M., et al. Acryloyl-CoA reductase from Clostridium propionicum. An enzyme complex of propionyl-CoA dehydrogenase and electron-transferring flavoprotein. Eur. J. Biochem. 2003, 270:902-910.
48. Buckel W., et al. Enzyme catalyzed radical dehydrations of hydroxy acids. Biochim. Biophys. Acta 2012, 1824:1278-1290.
49. Fonknechten N., et al. Clostridium sticklandii, a specialist in amino acid degradation: Revisiting its metabolism through its genome sequence. BMC Genomics 2010, 11:555.
50. Buckel W., Golding B.T. Radical enzymes in anaerobes. Annu. Rev. Microbiol. 2006, 60:27-49.
51. Buckel W., Barker H.A. Two pathways of glutamate fermentation by anaerobic bacteria. J. Bacteriol. 1974, 117:1248-1260.
52. Buckel W. Unusual enzymes involved in five pathways of glutamate fermentation. Appl. Microbiol. Biotechnol. 2001, 57:263-273.
53. Buckel W. Biotin-dependent decarboxylases as bacterial sodium pumps: purification and reconstitution of glutaconyl-CoA decarboxylase from Acidaminococcus fermentans. Methods Enzymol. 1986, 125:547-558.
54. Ramezani M., et al. Glutamate racemization and catabolism in Fusobacterium varium. FEBS J. 2011, 278:2540-2551.
55. Schuchmann K., Müller V. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat. Rev. Microbiol. 2014, 12:809-821.
56. Schut G.J., et al. The modular respiratory complexes involved in hydrogen and sulfur metabolism by heterotrophic hyperthermophilic archaea and their evolutionary implications. FEMS Microbiol. Rev. 2013, 37:182-203.
57. Liu Y., et al. Sulfur metabolism in archaea reveals novel processes. Environ. Microbiol. 2012, 14:2632-2644.
58. Adams M.W.W., et al. Key role for sulfur in peptide metabolism and in regulation of three hydrogenases in the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 2001, 183:716-724.
59. Kletzin A., et al. Dissimilatory oxidation and reduction of elemental sulfur in thermophilic archaea. J. Bioenerg. Biomembr. 2004, 36:77-91.
60. Bridger S.L., et al. Deletion strains reveal metabolic roles for key elemental sulfur-responsive proteins in Pyrococcus furiosus. J. Bacteriol. 2011, 193:6498-6504.
61. Gibson M.I. The structure of an oxalate oxidoreductase provides insight into microbial 2-oxoacid metabolism. Biochemistry 2015, 54:4112-4120.
62. Wolfe A.J. Physiologically relevant small phosphodonors link metabolism to signal transduction. Curr. Opin. Microbiol. 2010, 13:204-209.
63. Musfeldt M., et al. Acetyl coenzyme A synthetase (ADP forming) from the hyperthermophilic archaeon Pyrococcus furiosus: identification, cloning, separate expression of the encoding genes, acdAI and acdBI in Escherichia coli, and in vitro reconstitution of the active heterotetrameric enzyme from its recombinant subunits. J. Bacteriol. 1999, 181:5885-5888.
64. Bräsen C., et al. Reaction mechanism and structural model of ADP-forming acetyl-CoA synthetase from the hyperthermophilic archaeon Pyrococcus furiosus - evidence for a second active site histidine residue. J. Biol. Chem. 2008, 283:15409-15418.
65. Musfeldt M., Schönheit P. Novel type of ADP-forming acetyl coenzyme A synthetase in hyperthermophilic archaea: heterologous expression and characterization of isoenzymes from the sulfate reducer Archaeoglobus fulgidus and the methanogen Methanococcus jannaschii. J. Bacteriol. 2002, 184:636-644.
66. Scott J.W., et al. Characterization of ten heterotetrameric NDP-dependent acyl-CoA synthetases of the hyperthermophilic archaeon Pyrococcus furiosus. Archaea 2014, 2014:176863.
67. Awano T., et al. Characterization of two members among the five ADP-forming acyl coenzyme A (acyl-CoA) synthetases reveals the presence of a 2-(imidazol-4-yl)acetyl-CoA synthetase in Thermococcus kodakarensis. J. Bacteriol. 2014, 196:140-147.
68. Elkins J.G., et al. A korarchaeal genome reveals insights into the evolution of the Archaea. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8102-8107.
69. Schmidt M., Schönheit P. Acetate formation in the photoheterotrophic bacterium Chloroflexus aurantiacus involves an archaeal type ADP-forming acetyl-CoA synthetase isoenzyme I. FEMS Microbiol. Lett. 2013, 349:171-179.
70. Bock A.K., et al. Purification and characterization of two extremely thermostable enzymes, phosphate acetyltransferase and acetate kinase, from the hyperthermophilic eubacterium Thermotoga maritima. J. Bacteriol. 1999, 181:1861-1867.
71. Amend J.P., Shock E.L. Energetics of amino acids synthesis in hydrothermal ecosystems. Science 1998, 281:1659-1662.
72. Amend J.P., et al. The energetics of organic synthesis inside and outside the cell. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2013, 368:20120255.
73. Schink B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 1997, 61:262-280.
74. Hattori S., et al. Operation of the CO dehydrogenase/acetyl coenzyme A pathway in both acetate oxidation and acetate formation by the syntrophically acetate-oxidizing bacterium Thermacetogenium phaeum. J. Bacteriol. 2005, 187:3471-3476.
75. Oehler D., et al. Genome-guided analysis of physiological and morphological traits of the fermentative acetate oxidizer Thermacetogenium phaeum. BMC Genomics 2012, 13:723.
76. 2- and CO-dependent chemolithotrophic potentials of the acetogens Clostridium thermoaceticum and Acetogenium kivuit. J. Bacteriol. 1990, 172:4464-4471.
77. Thauer R.K., et al. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 2008, 6:579-591.
78. McCollom T.M., Amend J.P. A thermodynamic assessment of energy requirements for biomass synthesis by chemolithoautotrophic microorganisms in oxic and anoxic environments. Geobiology 2005, 3:135-144.
79. Thauer R.K., et al. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 1977, 41:100-180.
80. Kelley D.S., et al. Volcanoes, fluids, and life at mid-ocean ridge spreading centers. Annu. Rev. Earth Planet. Sci. 2002, 30:385-491.
81. Zinder S.H. Syntrophic acetate oxidation and 'reversible acetogenesis'. Acetogenesis 1994, 386-415. Chapman and Hall. H.L. Drake (Ed.).
82. Vogels G.D., van der Drift C. Degradation of purines and pyrimidines by microorganisms. Bacteriol. Rev. 1976, 40:403-468.
83. Andreesen J.R. Degradation of heterocyclic compounds. Handbook on Clostridia 2005, 221-273. CRC Press. P. Dürre (Ed.).
84. Wang S., et al. Clostridium acidiurici electron-bifurcating formate dehydrogenase. Appl. Environ. Microbiol. 2013, 79:6176-6179.
85. Decker K., et al. Energy production in anaerobic organisms. Angew. Chem. Int. Ed. 1970, 9:138-158.
86. Hartwich K., et al. The purine-utilizing bacterium Clostidium acidiurici 9a: a genome-guided metabolic reconsideration. PLoS ONE 2012, 7:e51662.
87. Wachsman J.T., Barker H.A. Characterization of an orotic acid fermenting bacterium, Zymobacterium oroticum, nov. gen, nov. spec. J. Bacteriol. 1954, 68:400-404.
88. Hilton M.G., et al. Metabolism of pyrimidines by proteolytic clostridia. Arch. Microbiol. 1975, 102:145-149.
89. Herrmann G., et al. Two beta-alanyl-CoA:ammonia lyases in Clostridium propionicum. FEBS J. 2008, 272:813-821.
90. Sato T., Atomi H. Novel metabolic pathways in archaea. Curr. Opin. Microbiol. 2011, 14:307-314.
91. Johnsen U., et al. XacR - a novel transcriptional regulator of D-xylose and L-arabinose catabolism in the haloarchaeon Haloferax volcanii. Environ. Microbiol. 2015, 17:1663-1676.
92. Grochowski L.L., et al. Ribose-5-phosphate biosynthesis in Methanocaldococcus jannaschii occurs in the absence of a pentose-phosphate pathway. J. Bacteriol. 2005, 187:7382-7389.
93. Bräsen C., et al. Carbohydrate metabolism in archaea: Current insights into unusual enzymes and pathways and their regulation. Microbiol. Mol. Biol. Rev. 2014, 78:89-175.
94. Pickl A., Schönheit P. The oxidative pentose phosphate pathway in the haloarchaeon Haloferax volcanii involves a novel type of glucose-6-phosphate dehydrogenase - the archaeal Zwischenferment. FEBS Lett. 2015, 589:1105-1111.
95. Nelson-Sathi S., et al. Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature 2015, 517:77-80.
96. Siebers B., Schönheit P. Unusual pathways and enzymes of central carbohydrate metabolism in archaea. Curr. Opin. Microbiol. 2005, 8:695-705.
97. Kandler O., Konig H. Cell wall polymers in Archaea (Archaebacteria). Cell Mol. Life Sci. 1998, 54:305-308.
98. Arnfors L., et al. Structure of Methanocaldococcus jannaschii nucleoside kinase: an archaeal member of the ribokinase family. Acta Crystallogr. D: Biol. Crystallogr. 2006, 62:1085-1097.
99. Schäfer T., et al. Acetyl-CoA synthetase (ADP forming) in archaea, a novel enzyme involved in acetate formation and ATP synthesis. Arch. Microbiol. 1993, 159:72-83.
100. Glasemacher J., et al. Purification and properties of acetyl-CoA synthetase (ADP-forming), an archaeal enzyme of acetate formation and ATP synthesis, from the hyperthermophile Pyrococcus furiosus. Eur. J. Biochem. 1997, 244:561-567.
101. Mai X., Adams M.W. Purification and characterization of two reversible and ADP-dependent acetyl coenzyme A synthetases from the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 1996, 178:5897-5903.
102. Sato T., et al. Archaeal type III RuBisCOs function in a pathway for AMP metabolism. Science 2007, 315:1003-1006.
103. Aono R., et al. Enzymatic characterization of AMP phosphorylase and ribose-1,5-bisphosphate isomerase functioning in an archaeal AMP metabolic pathway. J. Bacteriol. 2012, 194:6847-6855.
104. Aono R., et al. A pentose bisphosphate pathway for nucleoside degradation in Archaea. Nat. Chem. Biol. 2015, 11:355-360.
105. Wrighton K.C., et al. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 2012, 337:1661-1665.
106. Rueter P., et al. Anaerobic oxidation of hydrocarbons in crude oil by new types of sulphate-reducing bacteria. Nature 1994, 372:455-458.
107. Harder J., Probian C. Microbial degradation of monoterpenes in the absence of molecular oxygen. Appl. Environ. Microbiol. 1995, 61:3804-3808.
108. Boyd E.S., et al. A late methanogen origin for molybdenum-dependent nitrogenase. Geobiology 2011, 9:221-232.
109. Stüeken E.E., et al. Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr. Nature 2015, 520:666-669.
110. Dörr M., et al. A possible prebiotic formation of ammonia from dinitrogen on iron sulfide surfaces. Angew. Chem. Int. Ed. Engl. 2003, 42:1540-1543.
111. Brandes J.A., et al. Abiotic nitrogen reduction on the early earth. Nature 1998, 395:365-367.
112. Hilpert W., et al. Life by a new decarboxylation-dependent energy conservation mechanism with Na as coupling ion. EMBO J. 1984, 3:1665-1670.
113. Anantharam V., et al. Oxalate:formate exchange. The basis for energy coupling in Oxalobacter. J. Biol. Chem. 1989, 264:7244-7250.
114. Drake H.L., et al. Old acetogens, new light. Ann. N. Y. Acad. Sci. 2008, 1125:100-128.
115. Rabus R., et al. A post-genomic view of the ecophysiology, catabolism and biotechnological relevance of sulphate-reducing prokaryotes. Adv. Microb. Physiol. 2015, 66:55-321.