Horizontal gene transfer from Eukarya to Bacteria and domain shuffling: the alpha-amylase model

[en] alpha-Amylases are present in all kingdoms of the living world. Despite strong conservation of the tertiary structure, only a few amino acids are conserved in interkingdom comparisons. Animal alpha-amylases are characterized by several typical motifs and biochemical properties. A few cases of such alpha-amylases have been previously reported in some eubacterial species. We screened the bacterial genomes available in the sequence databases for new occurrences of animal-like alpha-amylases. Three novel cases were found, which belong to unrelated bacterial phyla: Chloroflexus aurantiacus, Microbulbifer degradans, and Thermobifida fusca. All the animal-like alpha-amylases in Bacteria probably result from repeated horizontal gene transfer from animals. The M. degradans genome also contains bacterial-type and plant-type alpha-amylases in addition to the animal-type one. Thus, this species exhibits alpha-amylases of animal, plant, and bacterial origins. Moreover, the similarities in the extra C-terminal domains (different from both the alpha-amylase domain C and the starch-binding domain), when present, also suggest interkingdom as well as intragenomic shuffling.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Da Lage, J. L.

Feller, Georges ; Université de Liège - ULiège > Département des sciences de la vie > Labo de biochimie

Janecek, S.

Language :

English

Title :

Horizontal gene transfer from Eukarya to Bacteria and domain shuffling: the alpha-amylase model

Publication date :

January 2004

Journal title :

Cellular and Molecular Life Sciences

ISSN :

1420-682X

eISSN :

1420-9071

Publisher :

Birkhäuser, Basel, Switzerland

Volume :

Issue :

Pages :

97-109

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 26 January 2010

Statistics

Number of views

60 (1 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Janecek S. (1997) α-Amylase family: molecular biology and evolution. Prog. Biophys. Mol. Biol. 67: 67-97
Pujadas G. and Palau J. (2001) Evolution of α-amylases: architectural features and key residues in the stabilization of the (β/α)8 scaffold. Mol. Biol. Evol. 18: 38-54
Janecek S. (1994) Sequence similarities and evolutionary relationships of microbial, plant and animal α-amylases. Eur. J. Biochem. 224: 519-524
Da Lage J.-L., van Wormhoudt A. and Cariou M.-L. (2002) Diversity and evolution of the α-amylase genes in animals. Biol. Bratislava 57 (suppl. 11): 181-189
Janecek S., Lévêque E., Belarbi A. and Haye B. (1999) Close evolutionary relatedness of α-amylases from Archaea and plants. J. Mol. Evol. 48: 421-426
Long C. M., Virolle M.-J., Chang S.-Y., Chang S. and Bibb M. J. (1987) α-Amylase gene of Streptomyces limosus: nucleotide sequence, expression motifs, and amino acid sequence homology to mammalian and invertebrate α-amylases. J. Bacteriol. 169: 5745-5754
Mazodier P. and Davies J. (1991) Gene transfer between distantly related bacteria. Annu. Rev. Genet. 25: 147-171
Vigal T., Gil J. A., Daza A., Garcia-Gonzalez M. D. and Martin J. F. (1991) Cloning, characterization and expression of an α-amylase gene from Streptomyces griseus IMRU3570. Mol. Gen. Genet. 225: 278-288
Petricek M., Tichy P. and Kuncova M. (1992) Characterization of the α-amylase-encoding gene from Thermomonospora curvata. Gene 112: 77-83
Bahri S. M. and Ward J. M. (1993) Sequence of the Streptomyces thermoviolaceus CUB74 α-amylase-encoding gene and its transcription analysis in Streptomyces lividans. Gene 127: 133-137
Sumitani J. I., Nagae H., Kawaguchi T. and Arai M. (1998) Bacillus animal type α-amylase: cloning and sequencing of the gene, and comparison of the deduced amino acid sequence with that of other amylases. J. Ferment. Bioeng. 85: 428-432
Coronado M. J., Vargas C., Mellado E., Tegos G., Drainas C., Nieto J. J. et al. (2000) The α-amylase gene amyH of the moderate halophile Halomonas meridiana: cloning and molecular characterization. Microbiology 146: 861-868
Feller G., Lonhienne T., Deroanne C., Libioulle C., Van Beeumen J. and Gerday C. (1992) Purification, characterization and nucleotide sequence of the thermolabile α-amylase from the antarctic psychrotroph Alteromonas haloplanktis A23. J. Biol. Chem. 267: 5217-5221
Feller G., Le Bussy O., Houssier C. and Gerday C. (1996) Structural and functional aspects of chloride binding to Alteromonas haloplanctis α-amylase. J. Biol. Chem. 271: 23836-23841
Feller G., Payan F., Theys F., Quian M., Haser R. and Gerday C. (1994) Stability and structural analysis of α-amylase from the antarctic psychrophile Alteromonas haloplanctis A23. Eur. J. Biochem. 222: 441-447
Aghajari N., Feller G., Gerday C. and Haser R. (1998) Crystal structures of the psychrophilic α-amylase from Alteromonas haloplanctis in its native form and complexed with an inhibitor. Protein Sci 7: 564-572
Aghajari N., Feller G., Gerday C. and Haser R. (1998) Strucures of the psychrophilic Alteromonas haloplanctis α-amylase give insight into cold adaptation at a molecular level. Structure 6: 1503-1516
Svensson B. (1994) Protein engineering in the α-amylase family: catalytic mechanism, substrate specificity, and stability. Plant Mol. Biol. 25: 141-157
D'Amico S., Gerday C. and Feller G. (2000) Structural similarities and evolutionary relationships in chloride-dependent α-amylases. Gene 253: 95-105
Matsuura Y., Kusunoki M., Harada W. and Kakudo M. (1984) Structure and possible catalytic residues of Taka-amylase A. J. Biochem. (Tokyo) 95: 697-702
Machius M., Wiegand G. and Huber R. (1995) Crystal structure of calcium-depleted Bacillus licheniformis α-amylase at 2.2 Å resolution. J. Mol. Biol. 246: 545-559
Kadziola A., Sogaard M., Svensson B. and Haser R. (1998) Molecular structure of a barley α-amylase-inhibitor complex: implications for starch binding and catalysis. J. Mol. Biol. 278: 205-217
Svensson B., Jespersen H., Sierks M. R. and McGregor E. A. (1989) Sequence homology between putative raw-starch binding domains from different starch-degrading enzymes. Biochem. J. 264: 309-311
Janecek S. and Sevcik J. (1999) The evolution of starch-binding domain. FEBS Lett. 456: 119-125
Janecek S., Svensson B. and MacGregor E. A. (2003) Relation between domain evolution, specificity, and taxonomy of the α-amylase family members containing a C-terminal starch-binding domain. Eur. J. Biochem. 270: 635-645
Feller G., D'Amico S., Benotmane A. M., Joly F., Van Beeumen J. and Gerday C. (1998) Characterization of the C-terminal propeptide involved in bacterial wall spanning of α-amylase from the psychrophile Alteromonas haloplanktis. J. Biol. Chem. 273: 12109-12115
Benson D. A., Karsch-Mizrachi I., Lipman D. J., Ostell J., Rapp B. A. and Wheeler D. L. (2002) GenBank. Nucleic Acids Res. 30: 17-20
Altschul S. F., Gish W., Miller W., Myers E. W. and Lipman D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215: 403-410
Boer P. H. and Hickey D. A. (1986) The α-amylase gene in Drosophila melanogaster: nucleotide sequence, gene structure and expression motifs. Nucleic Acids Res. 14: 8399-8411
Tatusova T. A. and Madden T. L. (1999) Blast 2 sequences - a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 174: 247-250
Huang X. (1994) On global sequence alignment. CABIOS 10: 227-235
Thompson J. D., Higgins D. G. and Gibson T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680
Bairoch A. and Apweiler R. (2000) The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res. 28: 45-48
Janecek S. (2002) How many conserved sequence regions are there in the alpha-amylase family? Biol. Bratislava 57 (suppl. 11): 29-41
Saitou N. and Nei M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425
Page R. D. (1996) TreeView: an application to display phylogenetic trees on personal computers. CABIOS 12: 357-358
Doolittle R. F. (2002) Gene transfers between distantly related organisms. In: Horizontal Gene Transfer, pp. 269-275, Syvanen, M. & Kado, C. I. (eds), Adademic Press, London
Koonin E. V., Makarova K. S., Wolf Y. I. and Aravind L. (2002) Horizontal gene transfer and its role in the evolution of prokaryotes. In: Horizontal Gene Transfer, pp. 277-304, Syvanen, M. & Kado, C. I. (eds), Adademic Press, London
Demanèche S., Bertolla F., Buret F., Nalin R., Sailland A., Auriol P. et al. (2001) Laboratory-scale evidence for lightning-mediated gene transfer in soil. Appl. Environ. Microbiol. 67: 3440-3444
Gonzales J. M. and Weiner R. M. (2000) Phylogenetic characterization of marine bacterium strain 2-40, a degrader of complex polysaccharides. Int. J. Syst. Evol. Microbiol. 50: 831-834
Howard M. B., Ekborg N. A., Taylor L. E., Weiner R. M. and Hutcheson S. W. (2003) Genomic analysis and initial characterization of the chitinolytic system of Microbulbifer degradans strain 2-40. J. Bacteriol. 185: 3352-3360
Stoltzfus A., Logsdon J. M., Palmer J. D. and Doolittle W. F. (1997) Intron 'sliding' and the diversity of intron positions. Proc. Natl. Acad. Sci. USA 94: 10739-10744
Minassian B. A., Ianzano L., Meloche M., Andermann E., Rouleau G. A., Delgado-Escueta A. V. et al. (2000) Mutation spectrum and predicted function of laforin in Lafora's progressive myoclonus epilepsy. Neurology 55: 341-346
Janecek S. (2002) A motif of microbial starch-binding domain found in human genethonin. Bioinformatics 18: 1534-1537