One-carbon metabolic pathway rewiring in Escherichia coli reveals an evolutionary advantage of 10-formyltetrahydrofolate synthetase (Fhs) in survival under hypoxia

Journal of Bacteriology

Volumn 197, Issue 4, 2015, Pages 717-726

  Sah, Shivjee ^a   Aluri, Srinivas ^a   Rex, Kervin ^a   Varshney, Umesh ^a,b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; FORMATE TETRAHYDROFOLATE LIGASE; FORMIC ACID; GLYCINE; METHYLENETETRAHYDROFOLATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PURINE DERIVATIVE; PURINE NUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRANSFER RNA; BACTERIAL PROTEIN; ESCHERICHIA COLI PROTEIN; FOLINIC ACID; OXYGEN;

ANAEROBIC BACTERIUM; ARTICLE; AUXOTROPHY; BACTERIAL GROWTH; BACTERIAL STRAIN; CARBON METABOLISM; CLOSTRIDIUM PERFRINGENS; ESCHERICHIA COLI; FORMYLATION; GENE DELETION; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; ONE CARBON METABOLISM; PLASMID; PRIORITY JOURNAL; ENZYMOLOGY; EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL VIABILITY; MOLECULAR CLONING;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM PERFRINGENS; ESCHERICHIA COLI;

BACTERIAL PROTEINS; BIOLOGICAL EVOLUTION; CARBON; CLONING, MOLECULAR; CLOSTRIDIUM PERFRINGENS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FORMATE-TETRAHYDROFOLATE LIGASE; FORMYLTETRAHYDROFOLATES; METABOLIC NETWORKS AND PATHWAYS; METHYLENETETRAHYDROFOLATE DEHYDROGENASE (NADP); MICROBIAL VIABILITY; OXYGEN;

EID: 84921739011     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02365-14     Document Type: Article

References (53)

1. Smith DR, Doucette-Stamm LA, Deloughery C, Lee H, Dubois J, Aldredge T, Bashirzadeh R, Blakely D, Cook R, Gilbert K, Harrison D, Hoang L, Keagle P, Lumm W, Pothier B, Qiu D, Spadafora R, Vicaire R, Wang Y, Wierzbowski J, Gibson R, Jiwani N, Caruso A, Bush D, Dafer H, Patwell D, Prabhakar S, McDougall S, Shimer G, Goyal A, Pietrokovski S, Church GM, Daniels CJ, Mao J-I, Rice P, Nolling J, Reeve JN. 1997. Complete genome sequence of Methanobacterium thermoautotrophicum ΔH: functional analysis and comparative genomics. J Bacteriol 179:7135-7155.
2. Wasserfallen A, Nolling J, Pfister P, Reeve J, Conway de Macario E. Phylogenetic analysis of 18 thermophilic Methanobacterium isolates supports the proposals to create a new genus, Methanothermobacter gen. nov., and to reclassify several isolates in three species, Methanothermobacter thermautotrophicus comb. nov., Methanothermobacter wolfeii comb. nov., and Methanothermobacter marburgensis sp. nov. Int J Syst Evol Microbiol 50:43-53. http://dx.doi.org/10.1099/00207713-50-1-43.
3. Bult CJ, White O, Olsen GJ, Zhou L, Fleischmann RD, Sutton GG, Blake JA, FitzGerald LM, Clayton RA, Gocayne JD, Kerlavage AR, Dougherty BA, Tomb JF, Adams MD, Reich CI, Overbeek R, Kirkness EF, Weinstock KG, Merrick JM, Glodek A, Scott JL, Geoghagen NS, Venter JC. 1996. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058-1073. http://dx.doi.org/10.1126/science.273.5278.1058.
4. Slesarev AI, Mezhevaya KV, Makarova KS, Polushin NN, Shcherbinina OV, Shakhova VV, Belova GI, Aravind L, Natale DA, Rogozin IB, Tatusov RL, Wolf YI, Stetter KO, Malykh AG, Koonin EV, Kozyavkin SA. 2002. The complete genome of hyperthermophile Methanopyrus kandleri AV19 and monophyly of archaeal methanogens. Proc Natl Acad Sci U S A 99:4644-4649. http://dx.doi.org/10.1073/pnas.032671499.
5. Buchenau B, Thauer RK. 2004. Tetrahydrofolate-specific enzymes in Methanosarcina barkeri and growth dependence of this methanogenic archaeon on folic acid or p-aminobenzoic acid. Arch Microbiol 182:313-325. http://dx.doi.org/10.1007/s00203-004-0714-0.
6. Maeder DL, Anderson I, Brettin TS, Bruce DC, Gilna P, Han CS, Lapidus A, Metcalf WW, Saunders E, Tapia R, Sowers KR. 2006. The Methanosarcina barkeri genome: comparative analysis with Methanosarcina acetivorans and Methanosarcina mazei reveals extensive rearrangement within methanosarcinal genomes. J Bacteriol 188:7922-7931. http://dx.doi.org/10.1128/JB.00810-06.
7. Rabinowitz JC, Pricer WE, Jr. 1962. Formyltetrahydrofolate synthetase. Isolation and crystallization of enzyme. J Biol Chem 237:2898-2902.
8. D'Ari L, Rabinowitz JC. 1991. Purification, characterization, cloning, and amino acid sequence of the bifunctional enzyme 5,10-methylenetetrahydrofolate dehydrogenase/5,10-methenyltetrahydrofolate cyclohydrolase from Escherichia coli. J Biol Chem 266:23953-23958.
9. Pino P, Aeby E, Foth BJ, Sheiner L, Soldati T, Schneider A, Soldati-Favre D. 2010. Mitochondrial translation in absence of local tRNA aminoacylation and methionyl tRNA Met formylation in Apicomplexa. Mol Microbiol 76::706-718. http://dx.doi.org/10.1111/j.1365-2958.2010.07128.x.
10. Paukert JL, Straus LD, Rabinowitz JC. 1976. Formyl-methylmethylenetetrahydrofolate synthetase-(combined). An ovine protein with multiple catalytic activities. J Biol Chem 251:5104-5111.
11. Paukert JL, Williams GR, Rabinowitz JC. 1977. Formyl-methenylmethylenetetrahydrofolate synthetase (combined); correlation of enzymic activities with limited proteolytic degradation of the protein from yeast. Biochem Biophys Res Commun 77:147-154. http://dx.doi.org/10.1016/S0006-291X(77)80176-9.
12. Whitehead TR, Park M, Rabinowitz JC. 1988. Distribution of 10-formyltetrahydrofolate synthetase in eubacteria. J Bacteriol 170:995-997.
13. Crowley PJ, Gutierrez JA, Hillman JD, Bleiweis AS. 1997. Genetic and physiologic analysis of a formyl-tetrahydrofolate synthetase mutant of Streptococcus mutans. J Bacteriol 179:1563-1572.
14. Johnson JL, Hamm-Alvarez S, Payne G, Sancar GB, Rajagopalan KV, Sancar A. 1988. Identification of the second chromophore of Escherichia coli and yeast DNA photolyases as 5,10-methenyltetrahydrofolate. Proc Natl Acad Sci U S A 85:2046-2050. http://dx.doi.org/10.1073/pnas.85.7.2046.
15. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2:2006.0008. http://dx.doi.org/10.1038/msb4100050.
16. Stover P, Schirch V. 1990. Serine hydroxymethyltransferase catalyzes the hydrolysis of 5,10-methenyltetrahydrofolate to 5-formyltetrahydrofolate. J Biol Chem 265:14227-14233.
17. Murta SM, Vickers TJ, Scott DA, Beverley SM. 2009. Methylene tetrahydrofolate dehydrogenase/cyclohydrolase and the synthesis of 10-CHOTHF are essential in Leishmania major. Mol Microbiol 71:1386-1401. http://dx.doi.org/10.1111/j.1365-2958.2009.06610.x.
18. Li Y, Holmes WB, Appling DR, RajBhandary UL. 2000. Initiation of protein synthesis in Saccharomyces cerevisiae mitochondria without formylation of the initiator tRNA. J Bacteriol 182:2886-2892. http://dx.doi.org/10.1128/JB.182.10.2886-2892.2000.
19. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Saka K, Tadenuma M, Nakade S, Tanaka N, Sugawara H, Nishikawa K, Ichiyoshi N, Kitagawa M, Mori H, Ogasawara N, Nishimura A. 2005. A complete set of Escherichia coli open reading frames in mobile plasmids facilitating genetic studies. DNA Res 12:63-68. http://dx.doi.org/10.1093/dnares/12.1.63.
21. Schirch L, Gross T. 1968. Serine transhydroxymethylase. Identification as the threonine and allothreonine aldolases. J Biol Chem 243:5651-5655.
22. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
23. R cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14. http://dx.doi.org/10.1016/0378-1119(95)00193-A.
24. Yu DG, Ellis HM, Lee EC, Jenkins NA, Copeland NG, Court DL. 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci U S A 97:5978-5983. http://dx.doi.org/10.1073/pnas.100127597.
25. Cheng YS, Shen Y, Rudolph J, Stern M, Stubbe J, Flannigan KA, Smith JM. 1990. Glycinamide ribonucleotide synthetase from Escherichia coli: cloning, overproduction, sequencing, isolation, and characterization. Biochemistry 29:218-227. http://dx.doi.org/10.1021/bi00453a030.
26. Smith GK, Benkovic PA, Benkovic SJ. 1981. L(-)-10-Formyltetrahydrofolate is the cofactor for glycinamide ribonucleotide transformylase from chicken liver. Biochemistry 20:4034-4036. http://dx.doi.org/10.1021/bi00517a013.
27. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein M, Frank ED, Gerdes S, Glass EM, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy AC, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, Pusch GD, Rodionov DA, Ruckert C, Steiner J, Stevens R, Thiele I, Vassieva O, Ye Y, Zagnitko O, Vonstein V. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33:5691-5702. http://dx.doi.org/10.1093/nar/gki866.
28. Taneja NK, Dhingra S, Mittal A, Naresh M, Tyagi JS. 2010. Mycobacterium tuberculosis transcriptional adaptation, growth arrest and dormancy phenotype development is triggered by vitamin C. PLoS One 5:e10860. http://dx.doi.org/10.1371/journal.pone.0010860.
29. Verma SC, Mahadevan S. 2012. The chbG gene of the chitobiose (chb) operon of Escherichia coli encodes a chitooligosaccharide deacetylase. J Bacteriol 194:4959-4971. http://dx.doi.org/10.1128/JB.00533-12.
30. Eudes A, Kunji ER, Noiriel A, Klaus SM, Vickers TJ, Beverley SM, Gregory JF, III, Hanson AD. 2010. Identification of transport-critical residues in a folate transporter from the folate-biopterin transporter (FBT) family. J Biol Chem 285:2867-2875. http://dx.doi.org/10.1074/jbc. M109.063651.
31. Bailey LB (ed). 2010. Folate in health and disease, 2nd ed. CRC Press, Boca Raton, FL.
32. Fowler B. 1998. Genetic defects of folate and cobalamin metabolism. Eur J Pediatr 157:S60-S66. http://dx.doi.org/10.1007/PL00014306.
33. Rosenblatt D, Fowler B. 2006. Disorders of cobalamin and folate transport and metabolism, p 341-356. In Fernandes J, Saudubray J-M, Berghe G, Walter J (ed), Inborn metabolic diseases. Springer, Berlin, Germany.
34. Duthie SJ. 2011. Folate and cancer: how DNA damage, repair and methylation impact on colon carcinogenesis. J Inherit Metab Dis 34:101-109. http://dx.doi.org/10.1007/s10545-010-9128-0.
35. Blount BC, Mack MM, Wehr CM, MacGregor JT, Hiatt RA, Wang G, Wickramasinghe SN, Everson RB, Ames BN. 1997. Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc Natl Acad Sci U S A 94:3290-3295. http://dx.doi.org/10.1073/pnas.94.7.3290.
36. Melnyk S, Pogribna M, Miller BJ, Basnakian AG, Pogribny IP, James SJ. 1999. Uracil misincorporation, DNA strand breaks, and gene amplification are associated with tumorigenic cell transformation in folate deficient/repleted Chinese hamster ovary cells. Cancer Lett 146:35-44. http://dx.doi.org/10.1016/S0304-3835(99)00213-X.
37. Nagy PL, Marolewski A, Benkovic SJ, Zalkin H. 1995. Formyltetrahydrofolate hydrolase, a regulatory enzyme that functions to balance pools of tetrahydrofolate and one-carbon tetrahydrofolate adducts in Escherichia coli. J Bacteriol 177:1292-1298.
38. Sawers G, Bock A. 1988. Anaerobic regulation of pyruvate formate-lyase from Escherichia coli K-12. J Bacteriol 170:5330-5336.
39. Rebelo J, Auerbach G, Bader G, Bracher A, Nar H, Hosl C, Schramek N, Kaiser J, Bacher A, Huber R, Fischer M. 2003. Biosynthesis of pteridines. Reaction mechanism of GTP cyclohydrolase I. J Mol Biol 326::503-516. http://dx.doi.org/10.1016/S0022-2836(02)01303-7.
40. Fan J, Ye J, Kamphorst JJ, Shlomi T, Thompson CB, Rabinowitz JD. 2014. Quantitative flux analysis reveals folate-dependent NADPH production. Nature 510:298-302. http://dx.doi.org/10.1038/nature13236.
41. Hitchings GH, Burchall JJ. 1965. Inhibition of folate biosynthesis and function as a basis for chemotherapy. Adv Enzymol Relat Areas Mol Biol 27:417-468.
42. Temple CJ, Bennett LL, Jr, Rose JD, Elliott RD, Montgomery JA, Mangum JH. 1982. Synthesis of pseudo cofactor analogues as potential inhibitors of the folate enzymes. J Med Chem 25:161-166. http://dx.doi.org/10.1021/jm00344a014.
43. Eadsforth TC, Maluf FV, Hunter WN. 2012. Acinetobacter baumannii FolD ligand complexes-potent inhibitors of folate metabolism and a re-evaluation of the structure of LY374571. FEBS J 279:4350-4360. http://dx.doi.org/10.1111/febs.12025.
44. Ordal EJ, Halvorson HO. 1939. A comparison of hydrogen production from sugars and formic acid by normal and variant strains of Escherichia coli. J Bacteriol 38:199-220.
45. Knappe J. 1987. Anaerobic dissimilation of pyruvate, p 199-220. In Neidhardt FC, Ingraham JL (ed), Escherichia coli and Salmonella: cellular and molecular biology. American Society for Microbiology, Washington, DC.
46. Leibig M, Liebeke M, Mader D, Lalk M, Peschel A, Gotz F. 2011. Pyruvate formate lyase acts as a formate supplier for metabolic processes during anaerobiosis in Staphylococcus aureus. J Bacteriol 193:952-962. http://dx.doi.org/10.1128/JB.01161-10.
47. Warnecke T, Gill RT. 2005. Organic acid toxicity, tolerance, and production in Escherichia coli biorefining applications. Microb Cell Fact 4:25. http://dx.doi.org/10.1186/1475-2859-4-25.
48. Nygaard P, Smith JM. 1993. Evidence for a novel glycinamide ribonucleotide transformylase in Escherichia coli. J Bacteriol 175:3591-3597.
49. Beyer L, Doberenz C, Falke D, Hunger D, Suppmann B, Sawers RG. 2013. Coordination of FocA and pyruvate formate-lyase synthesis in Escherichia coli demonstrates preferential translocation of formate over other mixed-acid fermentation products. J Bacteriol 195:1428-1435. http://dx.doi.org/10.1128/JB.02166-12.
50. - recipient strains of Escherichia coli K12. Proc Natl Acad Sci U S A 60:160-167. http://dx.doi.org/10.1073/pnas.60.1.160.
51. Guyer MS, Reed RR, Steitz JA, Low KB. 1981. Identification of a sexfactor-affinity site in E. coli as gamma delta. Cold Spring Harbor Symp Quant Biol 45:135-140. http://dx.doi.org/10.1101/SQB.1981.045.01.022.
52. Rao AR, Varshney U. 2002. Characterization of Mycobacterium tuberculosis ribosome recycling factor (RRF) and a mutant lacking six amino acids from the C-terminal end reveals that the C-terminal residues are important for its occupancy on the ribosome. Microbiology 148:3913-3920.
53. Singh NS, Ahmad R, Sangeetha R, Varshney U. 2008. Recycling of ribosomal complexes stalled at the step of elongation in Escherichia coli. J Mol Biol 380:451-464. http://dx.doi.org/10.1016/j.jmb.2008.05.033.