Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae

Plant Physiology

Volumn 137, Issue 2, 2005, Pages 460-474

  Barbier, Guillaume ^a   Oesterhelt, Christine ^c   Larson, Matthew D ^a   Halgren, Robert G ^a   Wilkerson, Curtis ^a   Garavito, R Michael ^b   Benning, Christoph ^b   Weber, Andreas P M ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c UNIVERSITY OF POTSDAM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATES; ENZYMES; GENES; METABOLISM;

CARBOHYDRATE METABOLISM; GENOMIC SEQUENCES; UNICELLULAR ALGAE;

ALGAE;

ALGAE; GENES; METABOLISM;

ALGAE; CYANIDIOSCHYZON; CYANIDIOSCHYZON MEROLAE; GALDIERIA; GALDIERIA SULPHURARIA; RHODOPHYTA;

ALGAL PROTEIN; CARRIER PROTEIN;

ACTIVE TRANSPORT; ARTICLE; CARBOHYDRATE METABOLISM; CELL WALL; COMPARATIVE STUDY; GENETICS; GENOME; METABOLISM; MITOCHONDRION; PLASTID; RED ALGA; SPECIES DIFFERENCE;

ALGAE, RED; ALGAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; CARBOHYDRATE METABOLISM; CARRIER PROTEINS; CELL WALL; GENOME; MITOCHONDRIA; PLASTIDS; SPECIES SPECIFICITY;

EID: 19044379861     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.104.051169     Document Type: Article

References (106)

1. Albertano P, Ciniglia C, Pinto G, Pollio A (2000) The taxonomic position of Cyanidium, Cyanidioschyzon and Galdieria: an update. Hydrobiologia 433: 137-143
2. Allen RD, Naitoh Y (2002) Osmoregulation and contractile vacuoles of protozoa. Int Rev Cytol 215: 351-394
3. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402
4. Ara K, Saeki K, Igarashi K, Takaiwa M, Uemura T, Hagihara H, Kawai S, Ito S (1995) Purification and characterization of an alkaline amylopullulanase with both alpha-1,4 and alpha-1,6 hydrolytic activity from alkalophilic Bacillus sp. KSM-1378. Biochim Biophys Acta 1243: 315-324
5. Ball S, Guan HP, James M, Myers A, Keeling P, Mouille G, Buleon A, Colonna P, Preiss J (1996) From glycogen to amylopectin: a model for the biogenesis of the plant starch granule. Cell 86: 349-352
6. Bell W, Sun W, Hohmann S, Wera S, Reinders A, De Virgilio C, Wiemken A, Thevelein JM (1998) Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. J Biol Chem 273: 33311-33319
7. Brock TD (1978) The genus Cyanidium. In TD Brock, ed, Thermophilic Microorganisms and Life at High Temperatures. Springer-Verlag, New York, pp 255-302
8. Chen JT, Chen MC, Chen LL, Chu WS (2001) Structure and expression of an amylopullulanase gene from Bacillus stearothermophilus TS-23. Biotechnol Appl Biochem 33: 189-199
9. Chiu WL, Johnson EM, Kaplan SA, Blasko K, Sokalski MB, Wolfson R, Sears BB (1990) Oenothera chloroplast DNA polymorphisms associated with plastome mutator activity. Mol Gen Genet 221: 59-64
10. Ciniglia C, Yoon HS, Pollio A, Pinto G, Bhattacharya D (2004) Hidden biodiversity of the extremophilic Cyanidiales red algae. Mol Ecol 13: 1827-1838
11. Coppin A, Varré JS, Lienard L, Dauvillée D, Guérardel Y, Soyer-Gobillard MO, Buléon A, Ball S, Tomayo S (2005) Evolution of plant-like crystalline storage polysaccharide in the protozoan parasite Toxoplasma gondii argues for a red algal ancestry. J Mol Evol (in press)
12. Dauvillee D, Mestre V, Colleoni C, Slomianny M-C, Mouille G, Delrue B, d'Hulst C, Bliard C, Nuzillard J-M, Ball S (2000) The debranching enzyme complex missing in glycogen accumulating mutants of Chlamydomonas reinhardtii displays an isoamylase-type specificity. Plant Sci 157: 145-156
13. Davies DR, Plaskitt A (1971) Genetical and structural analyses of cell-wall formation in Chlamydomonas reinhardtii. Genet Res 17: 33-43
14. de Groot BL, Grubmuller H (2001) Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science 294: 2353-2357
15. De Luca P, Moretti A (1983) Floridosides in Cyanidium caldarium, Cyanidioschyzon merolae and Galdieria sulphuraria (Rhodophyta, Cyanidiophyceae). J Phycol 19: 368-369
16. Dutcher SK (2000) Chlamydomonas reinhardtii: biological rationale for genomics. J Eukaryot Microbiol 47: 340-349
17. Elbein AD (1969) Biosynthesis of a cell wall glucomannan in mung bean seedlings. J Biol Chem 244: 1608-1616
18. Glöckner G, Rosenthal A, Valentin K (2000) The structure and gene repertoire of an ancient red algal plastid genome. J Mol Evol 51: 382-390
19. Goddijn O, Smeekens S (1998) Sensing trehalose biosynthesis in plants. Plant J 14: 143-146
20. Gross W (1999) Revision of comparative traits for the acido- and thermophilic red algae Cyanidium and Galdieria. In J Seckbach, ed, Enigmatic Microorganisms and Life in Extreme Environments. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 437-446
21. Gross W, Heilmann I, Lenze D, Schnarrenberger C (2001) Biogeography of the Cyanidiaceae (Rhodophyta) based on 18S ribosomal RNA sequence data. Eur J Phycol 36: 275-280
22. Gross W, Kuver J, Tischendorf G, Bouchaala N, Busch W (1998) Cryptoendolithic growth of the red alga Galdieria sulphuraria in volcanic areas. Eur J Phycol 33: 25-31
23. Gross W, Oesterhelt C (1999) Ecophysiological studies on the red alga Galdieria sulphuraria isolated from southwest Iceland. Plant Biol (Stuttg) 1: 694-700
24. Gross W, Schnarrenberger C (1995a) Heterotrophic growth of 2 strains of the acido-thermophilic red alga Galdieria sulphuraria. Plant Cell Physiol 36: 633-638
25. Gross W, Schnarrenberger C (1995b) Purification and characterization of a galactose-1-phosphate-UDP-glucose uridyltransferase from the red alga Galdieria sulphuraria. Eur J Biochem 234: 258-263
26. Hanna R, Brummell DA, Camirand A, Hensel A, Russell EF, Maclachlan GA (1991) Solubilization and properties of GDP-fucose: xyloglucan 1,2-alpha-L-fucosyltransferase from pea epicotyl membranes. Arch Biochem Biophys 290: 7-13
27. Hardison RC (2003) Comparative genomics. PLoS Biol 1: E58
28. Harris EH (2001) Chlamydomonas as a model organism. Annu Rev Plant Physiol Plant Mol Biol 52: 363-406
29. Heilmann I, Schnarrenberger C, Gross W (1997) Mannose metabolizing enzymes from the red alga Galdieria sulphuraria. Phytochemistry 45: 903-906
30. Herold A, Lewis DH (1977) Mannose and green plants: occurrence, physiology and metabolism, and use as a tool to study role of orthophosphate. New Phytol 79: 1-40
31. Hicks GR, Hironaka CM, Dauvillee D, Funke RP, D'Hulst C, Waffenschmidt S, Ball SG (2001) When simpler is better: unicellular green algae for discovering new genes and functions in carbohydrate metabolism. Plant Physiol 127: 1334-1338
32. Hounsa CG, Brandt EV, Thevelein J, Hohmann S, Prior BA (1998) Role of trehalose in survival of Saccharomyces cerevisiae under osmotic stress. Microbiology 144: 671-680
33. Hussain H, Mant A, Seale R, Zeeman S, Hinchliffe E, Edwards A, Hylton C, Bornemann S, Smith AM, Martin C, et al (2003) Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans. Plant Cell 15: 133-149
34. Karsten U, Barrow KD, King RJ (1993) Floridoside, L-isofloridoside, and D-isofloridoside in the red alga Porphyra columbina: seasonal and osmotic effects. Plant Physiol 103: 485-491
35. Karsten U, West JA, Zuccarello GC, Nixdorf O, Barrow KD, King RJ (1999) Low molecular weight carbohydrate patterns in the Bangiophyceae (Rhodophyta). J Phycol 35: 967-976
36. Kremer BP, Kirst GO (1981) Biosynthesis of 2-O-D-glycerol-alpha-D- galactopyranoside (floridoside) in marine Rhodophyceae. Plant Sci Lett 23: 349-357
37. Kubo A, Fujita N, Harada K, Matsuda T, Satoh H, Nakamura Y (1999) The starch-debranching enzymes isoamylase and pullulanase are both involved in amylopectin biosynthesis in rice endosperm. Plant Physiol 121: 399-409
38. Kuroiwa T, Kuroiwa H, Sakai A, Takahashi H, Toda K, Itoh R (1998) The division apparatus of plastids and mitochondria. Int Rev Cytol 181: 1-41
39. Li SY, Lellouche JP, Shabtai Y, Arad S (2001) Fixed carbon partitioning in the red microalga Porphyridium sp (Rhodophyta). J Phycol 37: 289-297
40. Li SY, Shabtai Y, Arad S (2002) Floridoside as a carbon precursor for the synthesis of cell-wall polysaccharide in the red microalga Porphyridium sp (Rhodophyta). J Phycol 38: 931-938
41. Linka N, Hurka H, Lang BF, Burger G, Winkler HH, Stamme C, Urbany C, Seil I, Kusch J, Neuhaus HE (2003) Phylogenetic relationships of non-mitochondrial nucleotide transport proteins in bacteria and eukaryotes. Gene 306: 27-35
42. Lomako J, Lomako WM, Whelan WJ (1988) A self-glucosylating protein is the primer for rabbit muscle glycogen biosynthesis. FASEB J 2: 3097-3103
43. Lomako J, Lomako WM, Whelan WJ (2004) Glycogenin: the primer for mammalian and yeast glycogen synthesis. Biochim Biophys Acta 1673: 45-55
44. Londesborough J, Vuorio OE (1993) Purification of trehalose synthase from baker's yeast: its temperature-dependent activation by fructose 6-phosphate and inhibition by phosphate. Eur J Biochem 216: 841-848
45. Lunn JE, Ashton A, Hatch MD, Heldt HW (2000) Purification, molecular cloning, and sequence analysis of sucrose-6-phosphate phosphorylase from plants. Proc Natl Acad Sci USA 97: 12914-12919
46. Lunn JE, MacRae E (2003) New complexities in the synthesis of sucrose. Curr Opin Plant Biol 6: 208-214
47. Luykx P, Hoppenrath M, Robinson DG (1997a) Osmoregulatory mutants that affect the function of the contractile vacuole in Chlamydomonas reinhardtii. Protoplasma 200: 99-111
48. Luykx P, Hoppenrath M, Robinson DG (1997b) Structure and behavior of contractile vacuoles in Chlamydomonas reinhardtii. Protoplasma 198: 73-84
49. Marquardt J, Wans S, Rhiel E, Randolf A, Krumbein WE (2000) Intron-exon structure and gene copy number of a gene encoding for a membrane-intrinsic light-harvesting polypeptide of the red alga Galdieria sulphuraria. Gene 255: 257-265
50. Mathupala SP, Lowe SE, Podkovyrov SM, Zeikus JG (1993) Sequencing of the amylopullulanase (apu) gene of Thermoanaerobacter ethanolicus 39E, and identification of the active site by site-directed mutagenesis. J Biol Chem 268: 16332-16344
51. Matsuzaki M, Misumi O, Shin IT, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Yoshida Y, et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428: 653-657
52. Meeuse BJ (1960) Floridean starch. J Exp Bot 11: 129-140
53. Meeuse BJ, Kreger DR (1954) On the nature of floridean starch and Ulva starch. Biochim Biophys Acta 13: 593-595
54. Meng J, Srivastava LM (1993) Variations in floridoside content and floridoside phosphate synthase activity in Porphyra perforata (Rhodophyta). J Phycol 29: 82-84
55. Miller PW, Dunn WI, Schmidt RR (1998) Alternative splicing of a precursor-mRNA encoded by the Chlorella sorokiniana NADP-specific glutamate dehydrogenase gene yields mRNAs for precursor proteins of isozyme subunits with different ammonium affinities. Plant Mol Biol 37: 243-263
56. Minoda A, Sakagami R, Yagisawa F, Kuroiwa T, Tanaka K (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 45: 667-671
57. Miyagishima SY, Nishida K, Kuroiwa T (2003) An evolutionary puzzle: chloroplast and mitochondrial division rings. Trends Plant Sci 8: 432-438
58. Moreira D, Lopezarchilla AI, Amils R, Marin I (1994) Characterization of 2 new thermoacidophilic microalgae: genome organization and comparison with Galdieria sulphuraria. FEMS Microbiol Lett 122: 109-114
59. Muravenko OV, Selyakh IO, Kononenko NV, Stadnichuk IN (2001) Chromosome numbers and nuclear DNA contents in the red microalgae Cyanidium caldarium and three Galdieria species. Eur J Phycol 36: 227-232
60. Nagasaka S, Nishizawa NK, Mori S, Yoshimura EY (2004) Metal metabolism in the red alga Cyanidium caldarium and its relationship to metal tolerance. Biometals 17: 177-181
61. Nagasaka S, Nishizawa NK, Negishi T, Satake K, Mori S, Yoshimura E (2002) Novel iron-storage particles may play a role in aluminum tolerance of Cyanidium caldarium. Planta 215: 399-404
62. Nagashima H, Fukuda I (1983) Floridosides in unicellular hot-spring algae. Phytochemistry 22: 1949-1951
63. Nagashima H, Nakamura S, Nisizawa K, Hori T (1971) Enzymic synthesis of floridean starch in a red alga, Serraticardia maxima. Plant Cell Physiol 12: 243-253
64. Nakamura Y, Kubo A, Shimamune T, Matsuda T, Harada K, Satoh H (1997) Correlation between activities of starch debranching enzyme and α-polyglucan structure in endosperms of sugary-1 mutants of rice. Plant J 12: 143-153
65. Nyvall Collén P, Camitz A, Hancock RD, Viola R, Pedersén M (2004) Effect of nutrient deprivation and resupply on metabolites and enzymes related to carbon allocation in Gracilaria tenuistipatata (Rhodophyta). J Phycol 40: 305-314
66. Oesterhelt C, Gross W (2002) Different sugar kinases are involved in the sugar sensing of Galdieria sulphuraria. Plant Physiol 128: 291-299
67. Oesterhelt C, Schnarrenberger C, Gross W (1996) Phosphomannomutase and phosphoglucomutase in the red alga Galdieria sulphuraria. Plant Sci 121: 19-27
68. Oesterhelt C, Schnarrenberger C, Gross W (1999) Characterization of a sugar/polyol uptake system in the red alga Galdieria sulphuraria. Eur J Phycol 34: 271-277
69. Ohta N, Matsuzaki M, Misumi O, Miyagishima SY, Nozaki H, Tanaka K, Shin IT, Kohara Y, Kuroiwa T (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10: 67-77
70. Ohta N, Sato N, Kuroiwa T (1998) Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucleic Acids Res 26: 5190-5198
71. Perrir RM, DeRocher AE, Bar-Peled M, Zeng W, Norambuena L, Orellana A, Raikhel NV, Keegstra K (1999) Xyloglucan fucosyltransferase, an enzyme involved in plant cell wall biosynthesis. Science 284: 1976-1979
72. Prosselkov PV, Gross W, Igamberdiev AU, Schnarrenberger C (1996) Purification and characterization of UDP-D-galactose 4-epimerase from the red alga Galdieria sulphuraria. Physiol Plant 98: 753-758
73. Raven JA, Johnston AM, MacFarlane JJ (1990) Carbon metabolism. In KM Cole, RG Sheath, eds, Biology of the Red Algae. Cambridge University Press, Cambridge, UK, pp 172-202
74. Renné P, Dreßen U, Hebbeker U, Hille D, Flügge UI, Westhoff P, Weber APM (2003) The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2. Plant J 35: 316-331
75. Rigano C, Aliotta G, Rigano VD, Fuggi A, Vona V (1977) Heterotrophic growth patterns in the unicellular alga Cyanidium caldarium: a possible role for threonine dehydrase. Arch Microbiol 113: 191-196
76. Rigano C, Fuggi A, Martino D, Rigano V, Aliotta G (1976) Studies on utilization of 2-ketoglutarate, glutamate and other amino acids by the unicellular alga Cyanidium caldarium. Arch Microbiol 107: 133-138
77. Ritte G, Lloyd JR, Eckermann N, Rottmann A, Kossmann J, Steup M (2002) The starch-related R1 protein is an alpha-glucan, water dikinase. Proc Natl Acad Sci USA 99: 7166-7171
78. Roberts RM, Heishman A, Wickling C (1971) Growth inhibition and metabolite pool levels in plants tissues fed with D-glucosamine and D-galactose. Plant Physiol 48: 36-42
79. Rochaix JD (1995) Chlamydomonas reinhardtii as the photosynthetic yeast. Annu Rev Genet 29: 209-230
80. Rochaix JD (2002) Chlamydomonas, a model system for studying the assembly and dynamics of photosynthetic complexes. FEBS Lett 529: 34-38
81. Rose JKC, Bennett AB (1999) Cooperative disassembly of the cellulose-xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant Sci 4: 176-183
82. Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M (2003) Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 6849-6854
83. Schluepmann H, van Dijken A, Aghdasi M, Wobbes B, Paul M, Smeekens S (2004) Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol 135: 879-890
84. Seckbach J (1994) The natural history of Cyanidium (Geitler 1933): past and present perspectives. In J Seckbach, ed, Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells, Vol 91. Kluwer Academic Publishers, Dordrecht, The Netherlands, p 99
85. Seifert GJ (2004) Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. Curr Opin Plant Biol 7: 277-284
86. Smith AM (1999) Making starch. Curr Opin Plant Biol 2: 223-229
87. Smith AM, Denyer K, Martin C (1997) The synthesis of the starch granule. Annu Rev Plant Physiol Plant Mol Biol 48: 67-87
88. Stein R, Gross W, Schnarrenberger C (1997) Characterization of a xylitol dehydrogenase and a D-arabitol dehydrogenase from the thermo- and acidophilic red alga Galdieria sulphuraria. Planta 202: 487-493
89. Stroud RM, Miercke LJ, O'Connell J, Khademi S, Lee JK, Remis J, Harries W, Robles Y, Akhavan D (2003) Glycerol facilitator GlpF and the associated aquaporin family of channels. Curr Opin Struct Biol 13: 424-431
90. Thomas D, Bron P, Ranchy G, Duchesne L, Cavalier A, Rolland JP, Raguenes-Nicol C, Hubert JF, Haase W, Delamarche C (2002) Aquaglyceroporins, one channel for two molecules. Biochim Biophys Acta 1555: 181-186
91. Thorstenson YR, Hunicke-Smith SP, Oefner PJ, Davis RW (1998) An automated hydrodynamic process for controlled, unbiased DNA shearing. Genome Res 8: 848-855
92. van Dijken AJ, Schluepmann H, Smeekens SC (2004) Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol 135: 969-977
93. Viola R, Nyvall P, Pedersen M (2001) The unique features of starch metabolism in red algae. Proc R Soc Lond B Biol Sci 268: 1417-1422
94. Wang T, Bogracheva T, Hedley C (1998) Starch: as simple as A, B, C? J Exp Bot 49: 481-502
95. Weber A, Flügge UI (2002) Interaction of cytosolic and plastidic nitrogen metabolism in plants. J Exp Bot 53: 865-874
96. Weber A, Menzlaff E, Arbinger B, Gutensohn M, Eckerskorn C, Flügge UI (1995) The 2-oxoglutarate/malate translocator of chloroplast envelope membranes: molecular cloning of a transporter containing a 12-helix motif and expression of the functional protein in yeast cells. Biochemistry 34: 2621-2627
97. Weber APM (2004) Solute transporters as connecting elements between cytosol and plastid stroma. Curr Opin Plant Biol 7: 247-253
98. Weber APM, Oesterhelt C, Gross W, Bräutigam A, Imboden LA, Krassovskaya I, Linka N, Truchina J, Schneidereit J, Voll H, et al (2004) EST-analysis of the thermo-acidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol Biol 55: 17-32
99. Weber APM, Schneidereit J, Voll LM (2004) Using mutants to probe the in vivo function of plastid envelope membrane metabolite transporters. J Exp Bot 55: 1231-1244
100. Werner R (2002) Chlamydomonas reinhardtii as a unicellular model for circadian rhythm analysis. Chronobiol Int 19: 325-343
101. Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21: 809-818
102. Yoon HS, Hackett JD, Pinto G, Bhattacharya D (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci USA 99: 15507-15512
103. Yoshimura E, Nagasaka S, Satake K, Mori S (2000) Mechanism of aluminium tolerance in Cyanidium caldarium. Hydrobiologia 433: 57-60
104. Yoshimura E, Nagasaka S, Sato Y, Satake K, Mori S (1999) Extraordinary high aluminium tolerance of the acidophilic thermophilic alga, Cyanidium caldarium. Soil Sci Plant Nutr 45: 721-724
105. Yu TS, Kofler H, Häusler RE, Hille D, Flügge UI, Zeeman SC, Smith AM, Kossmann J, Lloyd J, Ritte G, et al (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell 13: 1907-1918
106. Zeeman SC, Umemoto T, Lue WL, Au-Yeung P, Martin C, Smith AM, Chen J (1998) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10: 1699-1712