Abstract
Compared with the large corpus of published work devoted to the study of the origin and early development of anabolism, little attention has been given to the discussion of the early evolution of catabolism in spite of its significance. In the present study, we have used comparative genomics to explore the evolution and phylogenetic distribution of the enzymes that catalyze the extant catabolic pathways of the monosaccharides glucose and ribose, as well as those of the nucleobases adenine, guanine, cytosine, uracil, and thymine. Based on the oxygen dependence of the enzymes, their conservation, and evolution, we speculate on the relative antiquity of the pathways. Our results allow us to suggest which catabolic pathways and enzymes may have already been present in the last common ancestor. We conclude that the enzymatic degradations of ribose, as well as those of purines adenine and guanine, are among the most ancient catabolic pathways which can be traced by protein-based methodologies.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410
Barker HA, Beck JV (1941) The fermentetive decomposition of purines by Clostridium acidi-urici and Clostridium cylindrosporum. J Biol Chem 141:3–27
Becerra A, Lazcano A (1998) The role of gene duplication in the evolution of purine nucleotide salvage pathways. Orig Life Evol Biosph 28(4–6):539–553
Becerra A, Delaye L, Islas S, Lazcano A (2007) The very early stages of biological evolution and the nature of the last common ancestor of the three major cell domains. Annu Rev Ecol Evol Syst 38(1):361–379
Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H et al (2000) The Protein Data Bank. Nucleic Acids Res 28(1):235–242
Burton AS, Stern JC, Elsila JE, Glavin DP, Dworkin JP (2012) Understanding prebiotic chemistry through the analysis of extraterrestrial amino acids and nucleobases in meteorites. Chem Soc Rev 41(16):5459–5472
Caetano-Anollés K, Caetano-Anollés G (2013) Structural phylogenomics reveals gradual evolutionary replacement of abiotic chemistries by protein enzymes in purine metabolism. PLoS ONE 8(3):e59300
Caetano-Anollés G, Kim HS, Mittenthal JE (2007) The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture. Proc Natl Acad Sci USA 104(22):9358–9363
Callahan MP, Smith KE, Cleaves HJ, Ruzicka J, Stern JC, Glavin DP et al (2011) Carbonaceous meteorites contain a wide range of extraterrestrial nucleobases. Proc Natl Acad Sci USA 108(34):13995–13998
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al (2009) BLAST+: architecture and applications. BMC Bioinformatics 10(1):421
Canfield DE (2005) The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu Rev Earth Planet Sci 33(1):1–36
Caspi R, Altman T, Billington R, Dreher K, Foerster H, Fulcher CA et al (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 42(Database issue):D459–D471
Chothia C, Lesk AM (1986) The relation between the divergence of sequence and structure in proteins. EMBO J 5(4):823–826
Clarke PH, Elsden SR (1980) The earliest catabolic pathways. J Mol Evol 15(4):333–338
Cooper G, Kimmich N, Belisle W, Sarinana J, Brabham K, Garrel L (2001) Carbonaceous meteorites as a source of sugar-related organic compounds for the early Earth. Nature 414(6866):879–883
Delaye L, Becerra A, Lazcano A (2005) The last common ancestor: what’s in a name? Orig Life Evol Biosph 35(6):537–554
Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7(10):e1002195
Edgar RC (2004a) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113
Edgar RC (2004b) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797
Embley TM, Williams TA (2015) Steps on the road to eukaryotes. Nature 521(7551):169–170
Ferris JP, Sanchez RA, Orgel LE (1968) Studies in prebiotic synthesis: synthesis of pyrimidines from cyanoacetylene and cyanate. J Mol Biol 33(3):693–704
Ferris JP, Joshi PC, Edelson EH, Lawless JG (1978) HCN: A plausible source of purines, pyrimidines and amino acids on the primitive earth. J Mol Evol 11(4):293–311
Finn RD, Mistry J, Schuster-Böckler B, Griffiths-Jones S, Hollich V, Lassmann T et al (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34(Database issue):D247–D251
Forterre P, Gribaldo S (2010) Bacteria with a eukaryotic touch: a glimpse of ancient evolution? Proc Natl Acad Sci USA 107(29):12739–12740
Fothergill-Gilmore LA (1986) The evolution of the glycolytic pathway. Trends Biochem Sci 11(1):47–51
Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28(23):3150–3152
Geer LY, Marchler-Bauer A, Geer RC, Han L, He J, He S et al (2010) The NCBI BioSystems database. Nucleic Acids Res 38(Database issue):D492–D496
Goldfine H (1965) The evolution of oxygen as a biosynthetic reagent. J Gen Physiol 49(1):Suppl:253–274
Goldman AD, Beatty JT, Landweber LF (2016) The TIM barrel architecture facilitated the early evolution of protein-mediated metabolism. J Mol Evol 82(1):17–26
Harris JK, Kelley ST, Spiegelman GB, Pace NR (2003) The genetic core of the universal ancestor. Genome Res 13(3):407–412
Hayaishi O, Kornberg A (1952) Metabolism of cytosine, thymine, uracil, and barbituric acid by bacterial enzymes. J Biol Chem 197(2):717–732
Irving JA, Whisstock JC, Lesk AM (2001) Protein structural alignments and functional genomics. Proteins 42(3):378–382
Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30
Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M (2014) Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42(Database issue):D199–D205
Katsuragi T, Sakai T, Tonomura K (1986) Affinity chromatography of cytosine deaminase from Escherichia coli with immobilized pyrimidine compounds. Agric Biol Chem 50(7):1713–1719
Keefe AD, Lazcano A, Miller SL (1995) Evolution of the biosynthesis of the branched-chain amino acids. Orig Life Evol Biosph 25(1–3):99–110
Keller MA, Piedrafita G, Ralser M (2015) The widespread role of non-enzymatic reactions in cellular metabolism. Curr Opin Biotechnol 34C:153–161
Kim KM, Caetano-Anollés G (2011) The proteomic complexity and rise of the primordial ancestor of diversified life. BMC Evol Biol 11(1):140
Knoll AH, Nowak MA (2017) The timetable of evolution. Sci Adv 3(5):e1603076
Krebs HA (1981) The evolution of metabolic pathways. In: Carlile JF (ed) Molecular and cellular aspects of microbial evolution. Cambridge University Press, Cambridge, pp 215–228
Krebs HA, Kornberg HL (1957) Energy transformations in living matter. Springer, Berlin
Lara FJS (1952) On the decomposition of pyrimidines by bacteria. II. Studies with cell-free enzyme preparations. J Bacteriol 64(2):279–285
Larralde R, Robertson MP, Miller SL (1995) Rates of decomposition of ribose and other sugars: implications for chemical evolution. Proc Natl Acad Sci USA 92(18):8158–8160
Lazcano A (2010) Which way to life? Orig Life Evol Biosph 40(2):161–167
Lazcano A (2016) Alexandr I: oparin and the origin of life—a historical reassessment of the heterotrophic theory. J Mol Evol 83(5–6):214–222
Lazcano A, Miller SL (1999) On the origin of metabolic pathways. J Mol Evol 49(4):424–431
Levy M, Miller SL (1998) The stability of the RNA bases: implications for the origin of life. Proc Natl Acad Sci USA 95(14):7933–7938
Loh KD, Gyaneshwar P, Markenscoff Papadimitriou E, Fong R, Kim K-S, Parales R et al (2006) A previously undescribed pathway for pyrimidine catabolism. Proc Natl Acad Sci USA 103(13):5114–5119
Lyons TW, Reinhard CT, Planavsky NJ (2014) The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506(7488):307–315
Magrane M, Consortium U (2011) UniProt knowledgebase: a hub of integrated protein data. Database 2011(0):bar009
McMurry J, Begley TP (2005) The organic chemistry of biological pathways. Roberts and Company Publishers, Englewood
Michal G (ed) (1998) Biochemical pathways: an atlas of biochemistry and molecular biology (First). Wiley, New York
Michal G, Schomburg D (eds) (2012) Biochemical pathways: an atlas of biochemistry and molecular biology (Second). Wiley, Hoboken
Miller SL, Orgel LE (1974) The origins of life on the Earth. Prentice-Hall, Englewood Cliffs
Mirkin B, Fenner T, Galperin M, Koonin E (2003) Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes. BMC Evol Biol 3(1):2
Mistry J, Finn RD, Eddy SR, Bateman A, Punta M (2013) Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res 41:e121
Nagano N, Orengo CA, Thornton JM (2002) One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J Mol Biol 321(5):741–765
Nishino T, Okamoto K, Kawaguchi Y, Hori H, Matsumura T, Eger BT et al (2005) Mechanism of the conversion of xanthine dehydrogenase to xanthine oxidase: identification of the two cysteine disulfide bonds and crystal structure of a non-convertible rat liver xanthine dehydrogenase mutant. J Biol Chem 280(26):24888–24894
Oparin AI (1924) The origin of life (Russian). Moscow Worker, Moscow
Oparin AI (1938) The origin of life (English) (First Engl). The Macmillan Company, New York
Oró J (1960) Synthesis of adenine from ammonium cyanide. Biochem Biophys Res Commun 2(6):407–412
Oró J (1961) Mechanism of synthesis of adenine from hydrogen cyanide under possible primitive Earth conditions. Nature 191(4794):1193–1194
Porter DJ, Austin EA (1993) Cytosine deaminase: the roles of divalent metal ions in catalysis. J Biol Chem 268(32):24005–24011
Powner MW, Gerland B, Sutherland JD (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459(7244):239–242
Prlic A, Bliven S, Rose PW, Bluhm WF, Bizon C, Godzik A, Bourne PE (2010) Pre-calculated protein structure alignments at the RCSB PDB website. Bioinformatics 26(23):2983–2985
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C et al (2012) The Pfam protein families database. Nucleic Acids Res 40(Database issue):D290–D301
Rabinowitz JC (1956) Purine fermentation by Clostridium cylindrosporum: III—4-Amino-5-imidazolecarboxylic acid and 4-aminoimidazole. J Biol Chem 218(1):175–187
Rabinowitz JC, Barker HA (1956a) Purine fermentation by Clostridium cylindrosporum: I—tracer experiments on the fermentation of guanine. J Biol Chem 218(1):147–160
Rabinowitz JC, Barker HA (1956b) Purine fermentation by Clostridium cylindrosporum: II—purine transformations. J Biol Chem 218(1):161–173
Rabinowitz JC, Pricer WE (1956a) Purine fermentation by Clostridium cylindrosporum: IV—4-ureido-5-imidazolecarboxylic acid. J Biol Chem 218(1):189–199
Rabinowitz JC, Pricer WE (1956b) Purine fermentation by Clostridium cylindrosporum: V—formiminoglycine. J Biol Chem 222(2):537–554
Ranea JAG, Sillero A, Thornton JM, Orengo CA (2006) Protein superfamily evolution and the last universal common ancestor (LUCA). J Mol Evol 63(4):513–525
Rauchfuss H (2008) Chemical evolution and the origin of life (First). Springer, Heidelberg
Raymond J, Blankenship RE (2004) Biosynthetic pathways, gene replacement and the antiquity of life. Geobiology 2(4):199–203
Reeves RE, South DJ, Blytt HJ, Warren LG (1974) Pyrophosphate: d-fructose 6-phosphate 1-phosphotransferase: a new enzyme with the glycolytic function of 6-phosphofructokinase. J Biol Chem 249(24):7737–7741
Reid C, Orgel LE (1967) Model for origin of monosaccharides: Synthesis of sugars in potentially prebiotic conditions. Nature 216(5114):455–455
Ritson D, Sutherland JD (2012) Prebiotic synthesis of simple sugars by photoredox systems chemistry. Nat Chem 4(11):895–899
Sakai T, Yu T-S, Taniguchi K, Omata S (1975) Purification of cytosine deaminase from Pseudomonas aureofaciens. Agric Biol Chem 39(10):2015–2020
Saladino R, Crestini C, Cossetti C, Di Mauro E, Deamer D (2011) Catalytic effects of murchison material: prebiotic synthesis and degradation of RNA precursors. Orig Life Evol Biosph 41(5):437–451
Schomburg I, Chang A, Placzek S, Söhngen C, Rother M, Lang M, … Schomburg D (2013) BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA. Nucleic Acids Res 41(Database issue):D764–D772
Schönheit P, Buckel W, Martin WF (2016) On the origin of heterotrophy. Trends Microbiol 24(1):12–25
Shapiro R (1988) Prebiotic ribose synthesis: a critical analysis. Orig Life Evol Biosph 18(1–2):71–85
Shapiro R (1999) Prebiotic cytosine synthesis: a critical analysis and implications for the origin of life. Proc Natl Acad Sci USA 96(8):4396–4401
Shindyalov IN, Bourne PE (1998) Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng 11(9):739–747
Subbiah S, Laurents DV, Levitt M (1993) Structural similarity of DNA-binding domains of bacteriophage repressors and the globin core. Curr Biol 3(3):141–148
The UniProt Consortium (2012) Reorganizing the protein space at the universal protein resource (UniProt). Nucleic Acids Res, 40(Database issue), D71–D75
The UniProt Consortium (2014) Activities at the universal protein resource (UniProt). Nucleic Acids Res, 42(Database issue), D191–D198
Verhees CH, Kengen SWM, Tuininga JE, Schut GJ, Adams MWW, De Vos WM, Van Der Oost J (2003) The unique features of glycolytic pathways in Archaea. Biochem J 375(Pt 2):231–246
Yang S, Doolittle RF, Bourne PE (2005) Phylogeny determined by protein domain content. Proceedings of the National Academy of Sciences of the USA, 102(2):373–378
Ye Y, Godzik A (2003) Flexible structure alignment by chaining aligned fragment pairs allowing twists. Bioinformatics 19(Suppl 2):ii246–ii255
Acknowledgements
Mario Rivas Medrano is a doctoral student from the Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México (UNAM) and received fellowship 255708 from CONACYT. Financial support to AB and AL from the PAPIIT-UNAM (IN223916) is gratefully acknowledged. We are indebted to Ricardo Hernandez-Morales for his technical support in the preparation of the manuscript. We appreciate the advice of Claudia Alvarez-Carreño while analyzing the crystallographic structures of proteins, and the programing skills of César Antonio Martínez Gutiérrez while developing the scripts and routines used in the present work.
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Rivas, M., Becerra, A. & Lazcano, A. On the Early Evolution of Catabolic Pathways: A Comparative Genomics Approach. I. The Cases of Glucose, Ribose, and the Nucleobases Catabolic Routes. J Mol Evol 86, 27–46 (2018). https://doi.org/10.1007/s00239-017-9822-8
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DOI: https://doi.org/10.1007/s00239-017-9822-8