Evolution of vacuolar proton pyrophosphatase domains and volutin granules: Clues into the early evolutionary origin of the acidocalcisome

Biology Direct

Volumn 6, Issue , 2011, Pages

  Seufferheld, Manfredo J ^a   Kim, Kyung M ^a,b   Whitfield, James ^a   Valerio, Alejandro ^c   Caetano Anollés, Gustavo ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGROBACTERIUM TUMEFACIENS; ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA; RHODOSPIRILLUM RUBRUM;

ACID; CALCIUM; INORGANIC PYROPHOSPHATASE; POLYPHOSPHATE;

ARCHAEBACTERIUM; ARTICLE; BACTERIUM; BAYES THEOREM; CELL GRANULE; CELL VACUOLE; CLASSIFICATION; ELECTRON MICROSCOPY; ENZYMOLOGY; EUKARYOTE; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; PROTEIN DATABASE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; ULTRASTRUCTURE;

ACIDS; ARCHAEA; BACTERIA; BAYES THEOREM; CALCIUM; CYTOPLASMIC GRANULES; DATABASES, PROTEIN; EUKARYOTA; EVOLUTION, MOLECULAR; INORGANIC PYROPHOSPHATASE; MICROSCOPY, ELECTRON; PHYLOGENY; POLYPHOSPHATES; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; VACUOLES;

EID: 80053496265     PISSN: None     EISSN: 17456150     Source Type: Journal    
DOI: 10.1186/1745-6150-6-50     Document Type: Article

References (85)

1. Margulis L. Symbiotic theory of the origin of eukaryotic organelles; criteria for proof. Symp Soc Exp Biol 1975, 21-38.
2. Martin W, Russell MJ. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos Trans R Soc Lond B Biol Sci 2003, 358:59-83. discussion 83-55., 10.1098/rstb.2002.1183, 1693102, 12594918.
3. Dyall SD, Brown MT, Johnson PJ. Ancient invasions: from endosymbionts to organelles. Science 2004, 304:253-257. 10.1126/science.1094884, 15073369.
4. Bhattacharya D, Yoon HS, Hackett JD. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 2004, 26:50-60. 10.1002/bies.10376, 14696040.
5. Stiller JW. Plastid endosymbiosis, genome evolution and the origin of green plants. Trends in Plant Science 2007, 12:391-396. 10.1016/j.tplants.2007.08.002, 17698402.
6. Jones LJ, Carballido-Lopez R, Errington J. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 2001, 104:913-922. 10.1016/S0092-8674(01)00287-2, 11290328.
7. van den Ent F, Amos LA, Lowe J. Prokaryotic origin of the actin cytoskeleton. Nature 2001, 413:39-44. 10.1038/35092500, 11544518.
8. Shih YL, Rothfield L. The bacterial cytoskeleton. Microbiol Mol Biol Rev 2006, 70:729-754. 10.1128/MMBR.00017-06, 1594594, 16959967.
9. Seufferheld MJ, Vieira MC, Ruiz FA, Rodrigues CO, Moreno SN, Docampo R. Identification of organelles in bacteria similar to acidocalcisomes of unicellular eukaryotes. J Biol Chem 2003, 278:29971-29978. 10.1074/jbc.M304548200, 12783865.
10. Seufferheld MJ, Lea CR, Vieira M, Oldfield E, Docampo R. The H+-pyrophosphatase of Rhodospirillum rubrum is predominantly located in polyphosphate-rich acidocalcisomes. J Biol Chem 2004, 279:1193-51202.
11. Docampo R, de Souza W, Miranda K, Rohloff P, Moreno SN. Acidocalcisomes - conserved from bacteria to man. Nat Rev Microbiol 2005, 3:251-261. 10.1038/nrmicro1097, 15738951.
12. Motta LS, Ramos IB, Gomes FM, de Souza W, Champagne DE, Santiago MF, Docampo R, Miranda K, Machado EA. Proton-pyrophosphatase and polyphosphate in acidocalcisome-like vesicles from oocytes and eggs of Periplaneta americana. Insect Mol Biol 2009, 39:198-206.
13. Kornberg A. Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J Bacteriol 1995, 177:491-496. 176618, 7836277.
14. Meyer A. Orientierende untersuchungen ueber verbreitung. morphologie, und chemie des volutins. Bot Zeit 1904, 62:113-152.
15. Vercesi AE, Moreno SNJ, Docampo R. Ca2+/H+ Exchange in acidic vacuoles of Trypanosoma brucei. Biochem J 1994, 304:227-233. 1137476, 7998937.
16. Shiba T, Tsutsumi K, Yano H, Ihara Y, Kameda A, Tanaka K, Takahashi H, Munekata M, Rao NN, Kornberg A. Inorganic polyphosphate and the induction of rpoS expression. Proc Natl Acad Sci USA 1997, 94:11210-11215. 10.1073/pnas.94.21.11210, 23418, 9326588.
17. Nomura K, Kato J, Takiguchi N, Ohtake H, Kuroda A. Inorganic polyphosphate stimulates Lon-mediated proteolysis of nucleoid proteins in Escherichia coli. Cell Mol Biol 2006, 52:22-29.
18. Kulaev I, Kulakovskaya T. Polyphosphate and phosphate pump. Annu Rev Microbiol 2000, 54:709-734. 10.1146/annurev.micro.54.1.709, 11018142.
19. Kulaev IS, Bagabov VM, Kulakovskaia TV, Andreeva NA, Lichko LP, Trilisenko LV. [Peculiarities of metabolism and functions of high-molecular inorganic polyphosphates in yeasts as representatives of lower eukaryotes]. Mol Biol (Mosk) 2005, 39:567-580.
20. McInerney P, Mizutani T, Shiba T. Inorganic polyphosphate interacts with ribosomes and promotes translation fidelity in vitro and in vivo. Mol Microbiol 2006, 60:438-447. 10.1111/j.1365-2958.2006.05103.x, 16573692.
21. Cannon GC, Bradburne CE, Aldrich HC, Baker SH, Heinhorst S, Shively JM. Microcompartments in prokaryotes: carboxysomes and related polyhedra. Appl Environ Microbiol 2001, 67:5351-5361. 10.1128/AEM.67.12.5351-5361.2001, 93316, 11722879.
22. Komeili A, Vali H, Beveridge TJ, Newman DK. Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation. Proc Natl Acad Sci USA 2004, 101:3839-3844. 10.1073/pnas.0400391101, 374331, 15004275.
23. Caetano-anollés G, Wang M, Caetano-anollés D, Mittenthal JE. The origin, evolution and structure of the protein world. Biochem J 2009, 417:621-637. 10.1042/BJ20082063, 19133840.
24. Moore AD, Bjorklund AK, Ekman D, Bornberg-Bauer E, Elofsson A. Arrangements in the modular evolution of proteins. Trends Biochem Sci 2008, 33:444-451. 10.1016/j.tibs.2008.05.008, 18656364.
25. Wang M, Caetano-Anollés G. The evolutionary mechanics of domain Organization in Proteomes and the rise of modularity in the protein world. Structure 2009, 17:66-78. 10.1016/j.str.2008.11.008, 19141283.
26. Drozdowicz YM, Lu YP, Patel V, Fitz-Gibbon S, Miller JH, Rea PA. A thermostable vacuolar-type membrane pyrophosphatase from the archaeon Pyrobaculum aerophilum: implications for the origins of pyrophosphate-energized pumps. Febs Letters 1999, 460:505-512. 10.1016/S0014-5793(99)01404-0, 10556526.
27. Moreno SN, Zhong L. Acidocalcisomes in Toxoplasma gondii tachyzoites. Biochem J 1996, 313(Pt 2):655-659. 1216957, 8573106.
28. Marchesini N, Luo S, Rodrigues CO, Moreno SN, Docampo R. Acidocalcisomes and a vacuolar H+-pyrophosphatase in malaria parasites. Biochem J 2000, 347(Pt 1):243-253. 1220954, 10727425.
29. Ruiz FA, Marchesini N, Seufferheld MJ, Govindjee, Docampo R. The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. J Biol Chem 2001, 276:46196-46203. 10.1074/jbc.M105268200, 11579086.
30. Docampo R, Ulrich P, Moreno SNJ. Evolution of acidocalcisomes and their role in polyphosphate storage and osmoregulation in eukaryotic microbes. Philos Trans R Soc London [Biol] 2010, 365:775-784.
31. Rodrigues CO, Scott DA, Docampo R. Characterization of a vacuolar pyrophosphatase in Trypanosoma brucei and its localization to acidocalcisomes. Mol Cell Biol 1999, 19:7712-7723. 84816, 10523660.
32. Scott DA, de Souza W, Benchimol M, Zhong L, Lu HG, Moreno SNJ, Docampo R. Presence of a plant-like proton-pumping pyrophosphatase in acidocalcisomes of Trypanosoma cruzi. J Biol Chem 1998, 273:22151-22158. 10.1074/jbc.273.34.22151, 9705361.
33. Lemercier G, Dutoya S, Luo S, Ruiz FA, Rodrigues CO, Baltz T, Docampo R, Bakalara N. A vacuolar-type H+-pyrophosphatase governs maintenance of functional acidocalcisomes and growth of the insect and mammalian forms of Trypanosoma brucei. J Biol Chem 2002, 277:37369-37376. 10.1074/jbc.M204744200, 12121996.
34. Jiang L, Phillips TE, Hamm CA, Drozdowicz YM, Rea PA, Maeshima M, Rogers SW, Rogers JC. The protein storage vacuole: a unique compound organelle. J Cell Biol 2001, 155:991-1002. 10.1083/jcb.200107012, 2150895, 11739409.
35. Scherer PA, Bochem HP. Energy-dispersive X-ray microanalysis of the methanogen Methanosarcina barkeri 'Fusaro' grown on methanol and in the presence of heavy metals. Curr Microbiol 1983, 9:187-193.
36. Remonsellez F, Orell A, Jerez CA. Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism. Microbiology 2006, 152:59-66. 10.1099/mic.0.28241-0, 16385115.
37. Alvarez S, Jerez CA. Copper ions stimulate polyphosphate degradation and phosphate efflux in Acidithiobacillus ferrooxidans. Appl Environ Microbiol 2004, 70:5177-5182. 10.1128/AEM.70.9.5177-5182.2004, 520870, 15345397.
38. Nichols R. Gene trees and species trees are not the same. Trends Ecol Evolut 2001, 16:358-364.
39. Illergard K, Ardell DH, Elofison A. Structure is three to ten times more conserved than sequence-A study of structural response in protein cores. Proteins-Structure Function and Bioinformatics 2009, 77:499-508.
40. Elofsson A, von Heijne G. Membrane protein structure: prediction versus reality. Annu Rev Biochem 2007, 76:125-140. 10.1146/annurev.biochem.76.052705.163539, 17579561.
41. Hedlund J, Roberto C, Margareta B, Herrick B, Bengt P. Analysis of ancient sequence motifs in the H+-PPase family. FEBS Journal 2006, 273:5183-5193. 10.1111/j.1742-4658.2006.05514.x, 17054711.
42. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A. The Pfam protein families database. Nucleic Acids Res 2008, 36:D281-288. 10.1093/nar/gkn226, 2238907, 18039703.
43. Kurland CG, Collins LJ, Penny D. Genomics and the irreducible nature of eukaryote cells. Science 2006, 312:1011-1014. 10.1126/science.1121674, 16709776.
44. Poole A, Jeffares D, Penny D. Early evolution: prokaryotes, the new kids on the block. Bioessays 1999, 21:880-889. 10.1002/(SICI)1521-1878(199910)21:10<880::AID-BIES11>3.0.CO;2-P, 10497339.
45. Penny D, Poole A. The nature of the last universal common ancestor. Curr Opin Genetics Dev 1999, 9:672-677.
46. Embley TM, Martin W. Eukaryotic evolution, changes and challenges. Nature 2006, 440:623-630. 10.1038/nature04546, 16572163.
47. Collins L, Penny D. Complex spliceosomal organization ancestral to extant eukaryotes. Mol Biol Evol 2005, 22:1053-1066. 10.1093/molbev/msi091, 15659557.
48. Tiedemann H. "Killer" Impacts and life's origins. Science 1997, 277:1687-1688. 10.1126/science.277.5332.1687, 9287226.
49. Kornberg A, Rao NN, Ault-Riche D. Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem 1999, 68:89-125. 10.1146/annurev.biochem.68.1.89, 10872445.
50. Yamagata Y, Watanabe H, Saitoh M, Namba T. Volcanic production of polyphosphates and its relevance to prebiotic evolution. Nature 1991, 352:516-519. 10.1038/352516a0, 11536483.
51. Pasek MA. Rethinking early earth phosphorus geochemistry. Proc Natl Acad Sci USA 2008, 105:853-858. 10.1073/pnas.0708205105, 2242691, 18195373.
52. Hagan W, Parker A, Steuerwald A, Hathaway M. Phosphate solubility and the cyanate-mediated synthesis of pyrophosphate. Origins of Life and Evolution of Biospheres 2007, 37:113-122.
53. Grotzinger JP, Kasting JF. New Constraints on precambrian ocean composition. The Journal of Geology 1993, 101:235-243. 10.1086/648218, 11537740.
54. Jekely G. Did the last common ancestor have a biological membrane?. Biology Direct 2006, 1:35. 10.1186/1745-6150-1-35, 1675992, 17129384.
55. Drory O, Nelson N. The emerging structure of vacuolar ATPases. Physiology 2006, 21:317-325. 10.1152/physiol.00017.2006, 16990452.
56. Forterre P, Benachenhou-Lahfa N, Confalonieri F, Duguet M, Elie C, Labedan B. The nature of the last universal ancestor and the root of the tree of life, still open questions. BioSystems 1992, 28:15. 10.1016/0303-2647(92)90004-I, 1337989.
57. Scott DA, Docampo R. Characterization of isolated acidocalcisomes of Trypanosoma cruzi. J Biol Chem 2000, 275:24215-24221. 10.1074/jbc.M002454200, 10816577.
58. Rocha Facanha A, de Meis L. Reversibility of H+-ATPase and H+-pyrophosphatase in tonoplast vesicles from maize coleoptiles and seeds. Plant Physiol 1998, 116:1487-1495. 10.1104/pp.116.4.1487, 35057, 9536067.
59. Au KM, Barabote RD, Hu KY, Saier MH. Evolutionary appearance of H+-translocating pyrophosphatases. Microbiology 2006, 152:1243-1247. 10.1099/mic.0.28581-0, 16622041.
60. Siu PML, Wood HG. Phosphoenolpyruvic carboxytransphosphorylase, a CO2 fixation enzyme from propionic acid bacteria. J Biol Chem 1962, 237:3044-3051.
61. Heinonen JK. Biological role of inorganic pyrophosphate 2001, Springer.
62. Baltscheffsky M, Baltscheffsky H. Alternative photophosphorylation, inorganic pyrophosphate synthase and inorganic pyrophosphate. Photosynth Res 1995, 46:87-91.
63. Brown MR, Kornberg A. Inorganic polyphosphate in the origin and survival of species. Proc Natl Acad Sci USA 2004, 101:16085-16087. 10.1073/pnas.0406909101, 528972, 15520374.
64. Seufferheld MJ, Alvarez HM, Farias ME. Role of polyphosphates in microbial adaptation to extreme environments. Appl Environ Microbiol 2008, 74:5867-5874. 10.1128/AEM.00501-08, 2565944, 18708516.
65. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680. 10.1093/nar/22.22.4673, 308517, 7984417.
66. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999, 41:95-98.
67. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25:1189-1191. 10.1093/bioinformatics/btp033, 2672624, 19151095.
68. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574. 10.1093/bioinformatics/btg180, 12912839.
69. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 1992, 8:275-282.
70. Huson D, Richter D, Rausch C, Dezulian T, Franz M, Rupp R. Dendroscope: An interactive viewer for large phylogenetic trees. BMC Bioinformatics 2007, 8:460. 10.1186/1471-2105-8-460, 2216043, 18034891.
71. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol
72. Burnsel A, Viklund H, Falk J, Lindahl E, von Heijne G, Elofsson A. Prediction of membrane-protein topology from first principles. Proc Natl Acad Sci USA 2008, 105:7177-7181. 10.1073/pnas.0711151105, 2438223, 18477697.
73. Kahsay R, Liao L, Gao G. An improved hidden Markov model for transmembrane protein topology prediction and its applications to complete genomes. Bioinformatics 2005, 21:1853-1858. 10.1093/bioinformatics/bti303, 15691854.
74. Burnsel A, Viklund H, Hennerdal A, Elofsson A. TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res 2009, 37:W465-W468. 10.1093/nar/gkp363, 2703981, 19429891.
75. Durbin R, Eddy SR, Krogh A, Mitchison G. Biological sequence analysis: probabilistic models of proteins and nucleic acids. 1998, Cambridge: Cambridge University Press.
76. Murzin AG, Brenner SE, Hubbard T, Chothia C. SCOP: A structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 1995, 247:536.
77. Wilson D, Pethica R, Zhou Y, Talbot C, Vogel C, Madera M, Chothia C, Gough J. SUPERFAMILY--sophisticated comparative genomics, data mining, visualization and phylogeny. Nucl Acids Res 2009, 37:D380-386. 10.1093/nar/gkn762, 2686452, 19036790.
78. Gough J, Chothia C. SUPERFAMILY: HMMs representing all proteins of known structure. SCOP sequence searches, alignments and genome assignments. Nucl Acids Res 2002, 30:268-272. 10.1093/nar/30.1.268, 99153, 11752312.
79. Wilson D, Madera M, Vogel C, Chothia C, Gough J. The SUPERFAMILY database in 2007: families and functions. Nucl Acids Res 2007, 35:D308-313. 10.1093/nar/gkl910, 1669749, 17098927.
80. Sowers KR, Ferry JG. Isolation and characterization of a methylotrophic marine methanogen, Methanococcoides-Methylutens Gen-Nov, Sp-Nov. Appl Environ Microbiol 1983, 45:684-690. 242344, 16346215.
81. Caetano-Anollés G, Mittenthal JE. Exploring the interplay of stability and function in protein evolution. Bioessays 2010, 32:655-658. 10.1002/bies.201000038, 20658703.
82. Kim KM, Caetano-Anollés G. The proteomic complexity and rise of the primordial ancestor of diversified life. BMC Evol Biol 2011, 11:140. 10.1186/1471-2148-11-140, 3123224, 21612591.
83. Ingber DE. The origin of cellular life. Bioessays 2000, 22:1100-1170.
84. Morris CE. How did cells get their size?. Anat Rec 2002, 268:239-251. 10.1002/ar.10158, 12382322.
85. Hanczyc MM, Fujikawa SM, Szostak JW. Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 2003, 302:618-622. 10.1126/science.1089904, 14576428.