Widespread decay of vitamin-related pathways: Coincidence or consequence?

Trends in Genetics

Volumn 29, Issue 8, 2013, Pages 469-478

  Helliwell, Katherine E ^a   Wheeler, Glen L ^b,c   Smith, Alison G ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b PLYMOUTH MARINE LABORATORY   (United Kingdom)

^c THE LABORATORY   (United Kingdom)

Author keywords

Algae; Comparative genomics; Evolution; Pseudogenes; Symbiosis; Vitamin auxotrophy

Indexed keywords

ASCORBIC ACID; BIOTIN; COBALAMIN; FOLIC ACID; PYRIDOXINE; THIAMINE; THIAMINE PYROPHOSPHOKINASE; VITAMIN;

ALOUATTA; ARABIDOPSIS THALIANA; ASPERGILLUS ORYZAE; AUXOTROPHY; CHLAMYDOMONAS REINHARDTII; DICTYOSTELIUM DISCOIDEUM; ENTAMOEBA HISTOLYTICA; ESCHERICHIA COLI; EUKARYOTE; GENE LOSS; GORILLA; HETEROTROPHY; NONHUMAN; OSTREOCOCCUS; PARASITISM; PHAEODACTYLUM TRICORNUTUM; PLASMODIUM CHABAUDI; PLASMODIUM FALCIPARUM; PLASMODIUM YOELII; PRIORITY JOURNAL; PSEUDOGENE; REVIEW; SACCHAROMYCES CEREVISIAE; SPIDER MONKEY; SUBERITES; SYMBIOSIS; TRYPANOSOMA BRUCEI; VITAMIN METABOLISM; WIGGLESWORTHIA GLOSSINIDIA; WOLBACHIA;

ALGAE; COMPARATIVE GENOMICS; EVOLUTION; PSEUDOGENES; SYMBIOSIS; VITAMIN AUXOTROPHY;

ANIMALS; EUKARYOTA; EVOLUTION, MOLECULAR; GENE DELETION; HUMANS; METABOLIC NETWORKS AND PATHWAYS; METAGENOMICS; PSEUDOGENES; SYMBIOSIS; VITAMINS;

ALGAE; EUKARYOTA;

EID: 84880926390     PISSN: 01689525     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tig.2013.03.003     Document Type: Review

References (82)

1. Funk C. The substance from yeast and certain foodstuffs which prevents polyneuritis (beri-beri). Br. Med. J. 1912, 1912:787.
2. Smith A.G., et al. Plants need their vitamins too. Curr. Opin. Plant Biol. 2007, 10:266-275.
3. Lachapelle M.Y., Drouin G. Inactivation dates of the human and guinea pig vitamin C genes. Genetica 2011, 139:199-207.
4. Zhang Z.D., et al. Identification and analysis of unitary pseudogenes: historic and contemporary gene losses in humans and other primates. Genome Biol. 2010, 11:R26.
5. Linster C.L., Van Schaftingen E. Vitamin C - biosynthesis, recycling and degradation in mammals. FEBS J. 2007, 274:1-22.
6. Drouin G., et al. The Genetics of Vitamin C Loss in Vertebrates. Curr. Genomics 2011, 12:371-378.
7. Hiller M., et al. A "forward genomics" approach links genotype to phenotype using independent phenotypic losses among related species. Cell Rep. 2012, 2:817-823.
8. Nishikimi M., et al. Cloning and chromosomal mapping of the human nonfunctional gene for L-gulono-gamma-lactone oxidase, the enzyme for L-ascorbic-acid biosynthesis missing in man. J. Biol. Chem. 1994, 269:13685-13688.
9. Nishikimi M., et al. Guinea pigs possess a highly mutated gene for L-gulono-gamma-lactone oxidase, the key enzyme for L-ascorbic acid biosynthesis missing in this species. J Biol Chem. 1992, 267:21967-21972.
10. Cui J., et al. Recent loss of vitamin C biosynthesis ability in bats. PLoS ONE 2011, 6:e27114.
11. Cui J., et al. Progressive pseudogenization: vitamin C synthesis and its loss in bats. Mol. Biol. Evol. 2011, 28:1025-1031.
12. Martinez Del Rio C. Can passerines synthesize vitamin C?. Auk 1997, 114:513.
13. 6 biosynthesis: not that different after all. Biochem. J. 2007, 407:1-13.
14. 6 biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:9374-9378.
15. Osmani A.H., et al. The extremely conserved pyroA gene of Aspergillus nidulans is required for pyridoxine synthesis and is required indirectly for resistance to photosensitizers. J. Biol. Chem. 1999, 274:23565-23569.
16. Craig J.P., et al. Analysis of a horizontally transferred pathway involved in vitamin B(6) biosynthesis from the soybean cyst nematode Heterodera glycines. Mol. Biol. Evol. 2008, 25:2085-2098.
17. 6 biosynthesis in higher plants. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:13687-13692.
18. Seack J., et al. Identification of highly conserved genes: SNZ and SNO in the marine sponge Suberites domuncula: their gene structure and promoter activity in mammalian cells. Biochim. Biophys. Acta. 2001, 1520:21-34.
19. 6 (Pyridoxine) metabolism by gain and loss of genes. Mol. Biol. Evol. 2005, 22:243-250.
20. Webb M.E., et al. Elucidating biosynthetic pathways for vitamins and cofactors. Nat. Prod. Rep. 2007, 24:988-1008.
21. Alban C., et al. Biotin metabolism in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2000, 51:17-47.
22. Croft et al. Algae need their vitamins. Eukaryot. Cell 2006, 5:1175-1183.
23. Hall C., Dietrich F.S. The reacquisition of biotin prototrophy in Saccharomyces cerevisiae involved horizontal gene transfer, gene duplication and gene clustering. Genetics 2007, 177:2293-2307.
24. 12 auxotrophs. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:20756-20761.
25. Bertrand E.M., Allen A.E. Influence of vitamin B auxotrophy on nitrogen metabolism in eukaryotic phytoplankton. Front. Microbiol. 2012, 3:375.
26. Worden A.Z., et al. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 2009, 325:147.
27. 12 auxotrophy from sequenced algal genomes. Mol. Biol. Evol. 2011, 28:2921-2933.
28. 12 through a symbiotic relationship with bacteria. Nature 2005, 438:90-93.
29. 7 in Heterodera glycines. J. Nematol. 2009, 41:281-290.
30. Pombert J-F., et al. Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:12638-12643.
31. Holliday G.L., et al. Evolution of enzymes and pathways for the biosynthesis of cofactors. Nat. Prod. Rep. 2007, 24:972-987.
32. 12): synthesis and biological significance. Annu. Rev. Microbiol. 1996, 50:137-181.
33. Gonzalez J.C., et al. Comparison of cobalamin-independent and cobalamin-dependent methionine synthases from Escherichia coli: 2 solutions to the same chemical problem. Biochemistry 1992, 31:6045-6056.
34. Denslow S.A., et al. Regulation of biosynthetic genes and antioxidant properties of vitamin B-6 vitamers during plant defense responses. Physiol. Mol. Plant Pathol. 2005, 66:244-255.
35. Smirnoff N. Ascorbate biosynthesis and function in photoprotection. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2000, 355:1455-1464.
36. 12). Nat. Prod. Rep. 2002, 19:390-412.
37. McCutcheon J.P., et al. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:15394-15399.
38. Giovannoni S.J., et al. Genome streamlining in a cosmopolitan oceanic bacterium. Science 2005, 309:1242-1245.
39. Chatterjee A., et al. Saccharomyces cerevisiae THI4p is a suicide thiamine thiazole synthase. Nature 2011, 478:542-546.
40. 1. J. Mol. Biol. 2004, 344:1147-1157.
41. Lotierzo M., et al. Biotin synthase mechanism: an overview. Biochem. Soc. Trans. 2005, 33:820-823.
42. Banhegyi G., et al. Ascorbate synthesis-dependent glutathione consumption in mouse liver. FEBS Lett. 1996, 381:39-41.
43. Wheeler G.L., et al. The biosynthetic pathway of vitamin C in higher plants. Nature 1998, 393:365-369.
44. Romanes G.J. Darwin, and after Darwin 1896, Open Court.
45. Lahti D.C., et al. Relaxed selection in the wild. Trends Ecol. Evol. 2009, 24:487-496.
46. Bertrand E.M., et al. Influence of cobalamin scarcity on diatom molecular physiology and identification of a cobalamin acquisition protein. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E1762-E1771.
47. Wu H., et al. Identification and characterization of a novel biotin biosynthesis gene in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2005, 71:6845-6855.
48. Winkler W., et al. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 2002, 419:952-956.
49. Thore S., et al. Structural basis of thiamine pyrophosphate analogues binding to the eukaryotic riboswitch. J. Am. Chem. Soc. 2008, 130:8116-8117.
50. Cheah M.T., et al. Control of alternative RNA splicing and gene expression by eukaryotic riboswitches. Nature 2007, 447:497-500.
51. Croft M.T., et al. Thiamine biosynthesis in algae is regulated by riboswitches. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:20770-20775.
52. Milton K., Jenness R. Ascorbic-acid content of neotropical plant-parts available to wild monkeys and bats. Experientia 1987, 43:339-342.
53. Wagner-Dobler I., et al. The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea. ISME J. 2010, 4:61-77.
54. 12-dependent algae and heterotrophic bacteria exhibit regulation. Environ. Microbiol. 2012, 14:1466-1476.
55. Giovannoni S.J. Vitamins in the sea. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:13888-13889.
56. Belda E., et al. Mobile genetic element proliferation and gene inactivation impact over the genome structure and metabolic capabilities of Sodalis glossinidius, the secondary endosymbiont of tsetse flies. BMC Genomics 2010, 11:449.
57. Morett E., et al. Sensitive genome-wide screen for low secondary enzymatic activities: the YjbQ family shows thiamin phosphate synthase activity. J. Mol. Biol. 2008, 376:839-853.
58. Lima T., et al. HAMAP: a database of completely sequenced microbial proteome sets and manually curated microbial protein families in UniProtKB/Swiss-Prot. Nucleic Acids Res. 2009, 37:D471-D478.
59. Nogge G. Significance of symbionts for the maintenance of an optimal nutritional state for successful reproduction in hematophagous arthropods. Parasitology 1981, 82:101-104.
60. Wu D., et al. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 2006, 4:1079-1092.
61. Burke G.R., Moran N.A. Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol. Evol. 2011, 3:195-208.
62. Lamelas A., et al. Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet. 2011, 7:e1002357.
63. Nikoh N., et al. Reductive evolution of bacterial genome in insect gut environment. Genome Biol. Evol. 2011, 3:702-714.
64. 1 de novo synthesis in the human malaria parasite Plasmodium falciparum depends on external provision of 4-amino-5-hydroxymethyl-2-methylpyrimidine. Biol. Chem. 2006, 387:41-51.
65. 6 in the malaria parasite: requisite or dispensable?. Braz. J. Med. Biol. Res. 2008, 41:82-88.
66. Mueller S., Kappes B. Vitamin and cofactor biosynthesis pathways in Plasmodium and other apicomplexan parasites. Trends Parasitol. 2007, 23:112-121.
67. Divo A.A., et al. Nutritional-requirements of Plasmodium falciparum in culture .1. Exogenously supplied dialyzable components necessary for continuous growth. J. Protozool. 1985, 32:59-64.
68. Frech C., Chen N. Genome comparison of human and non-human malaria parasites reveals species subset-specific genes potentially linked to human disease. PLoS Comput. Biol. 2011, 7:e1002320.
69. Garnham P. Malaria Parasites and Other Haemosporidia 1966, Blackwell Scientific.
70. Dorrell R.G., Smith A.G. Do red and green make brown? Perspectives on plastid acquisitions within Chromalveolates. Eukaryot. Cell 2011, 10:856-868.
71. Herron M.D., et al. Triassic origin and early radiation of multicellular volvocine algae. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3254-3258.
72. Lewin J.C. Vitamin-bezonoj de algoj. Sciencaj Studoj 1958,187-192. Modersmaalet. P. Neergaard (Ed.).
73. Stein J.R. Growth and mating of Gonium pectorale (Volvocales) in defined media. J. Phycol. 1966, 2:23-28.
74. Saito S. Growth of Gonium multicoccum in synthetic media. J. Phycol. 1972, 8:169.
75. Pintner I.J., Provasoli L. The nutrition of Volvox globator and V. tertius. Proc IX Int Bot Congr Montreal 1959,300-301. Abstr. 9e.
76. Pringsheim E.G. Identification and cultivation of European Volvox sp. Antonie Leeuwenhoek. J. Microbiol. Serol. 1970, 36:33-43.
77. Hallmann A. Morphogenesis in the family Volvocaceae: different tactics for turning an embryo right-side out. Protist 2006, 157:445-461.
78. Hallmann A. Evolution of reproductive development in the volvocine algae. Sex. Plant Reprod. 2011, 24:97-112.
79. Solari C.A., et al. Multicellularity and the functional interdependence of motility and molecular transport. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:1353-1358.
80. Elischewski F., et al. Pantothenate production in Escherichia coli K12 by enhanced expression of the panE gene encoding ketopantoate reductase. J. Biotechnol. 1999, 75:135-146.
81. Primerano D.A., Burns R.O. Role of acetohydroxy acid isomeroreductase in biosynthesis of pantothenic-acid in Salmonella typhimurium. J. Bacteriol. 1983, 153:259-269.
82. Merkamm M., et al. Ketopantoate reductase activity is only encoded by ilvC in Corynebacterium glutamicum. J. Biotechnol. 2003, 104:253-260.