Evolution of the biosynthesis of di-myo-inositol phosphate, a marker of adaptation to hot marine environments

Environmental Microbiology

Volumn 14, Issue 3, 2012, Pages 691-701

  Gonçalves, Luís G ^a   Borges, Nuno ^a   Serra, François ^b   Fernandes, Pedro L ^c   Dopazo, Hernán ^b   Santos, Helena ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; INOSITOL 1-PHOSPHATE; INOSITOL PHOSPHATE; NUCLEOTIDYLTRANSFERASE; SEA WATER;

ACCLIMATIZATION; ARCHAEON; ARTICLE; BACTERIUM; BIOSYNTHESIS; CHEMISTRY; ENVIRONMENT; GENETICS; GENOME; HEAT; HORIZONTAL GENE TRANSFER; METABOLISM; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY;

ACCLIMATIZATION; ARCHAEA; BACTERIA; BIOLOGICAL MARKERS; ENVIRONMENT; GENE TRANSFER, HORIZONTAL; GENOME; HOT TEMPERATURE; INOSITOL PHOSPHATES; NUCLEOTIDYLTRANSFERASES; PHYLOGENY; SEAWATER;

CRENARCHAEOTA; THERMOTOGA;

EID: 84857855641     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02621.x     Document Type: Article

References (43)

1. Abascal, F., Zardoya, R., and Posada, D. (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
2. Aravind, L., Tatusov, R.L., Wolf, Y.I., Walker, D.R., and Koonin, E.V. (1998) Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends Genet 14: 442-444.
3. Borges, N., Gonçalves, L.G., Rodrigues, M.V., Ventura, R., Maycock, C., Lamosa, P., and Santos, H. (2006) Biosynthetic pathways of inositol and glycerol phosphodiesters used for stress adaptation in Archaeoglobus fulgidus. J Bacteriol 188: 8128-8135.
4. Borges, N., Matsumi, R., Imanaka, T., Atomi, H., and Santos, H. (2010) Thermococcus kodakarensis mutants deficient in di-myo-inositol phosphate use aspartate to cope with heat stress. J Bacteriol 192: 191-197.
5. Boussau, B., Guéguen, L., and Gouy, M. (2008) Accounting for horizontal gene transfers explains conflicting hypotheses regarding the position of Aquificales in the phylogeny of Bacteria. BMC Evol Biol 8: 272.
6. Brito, J.A., Borges, N., Vonrhein, C., Santos, H., and Archer, M. (2011) Crystal structure of Archaeoglobus fulgidus CTP:inositol-1-phosphate cytidylyltransferase, a key enzyme for di-myo-inositol-phosphate synthesis in (hyper)thermophiles. J Bacteriol 193: 2177-2185.
7. Brochier-Armanet, C., and Forterre, P. (2007) Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers. Archaea 2: 83-93.
8. Capella-Gutierrez, S., Silla-Martinez, J.M., and Gabaldon, T. (2009) TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973.
9. Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
10. Forterre, P., Bouthier, D.L., Tour, C., Philippe, H., and Duguet, M. (2000) Reverse gyrase from hyperthermophiles: probable transfer of a thermoadaptation trait from archaea to bacteria. Trends Genet 16: 152-154.
11. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
12. Heine, M., and Chandra, S.B. (2009) The linkage between reverse gyrase and hyperthermophiles: a review of their invariable association. J Microbiol 47: 229-234.
13. Kikuchi, A., and Asai, K. (1984) Reverse gyrase-a topoisomerase which introduces positive superhelical turns into DNA. Nature 309: 677-681.
14. Koga, Y., and Morii, H. (2007) Biosynthesis of ether-type polar lipids in archaea and evolutionary considerations. Microbiol Mol Biol Rev 71: 97-120.
15. Koga, Y., and Nakano, M. (2008) A dendrogram of archaea based on lipid component parts composition and its relationship to rRNA phylogeny. Syst Appl Microbiol 31: 169-182.
16. Koonin, E.V., Makarova, K.S., and Aravind, L. (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55: 709-742.
17. Lamosa, P., Martins, L.O., da Costa, M.S., and Santos, H. (1998) Effects of temperature, salinity, and medium composition on compatible solute accumulation by Thermococcus spp. Appl Environ Microbiol 64: 3591-3598.
18. Lamosa, P., Gonçalves, L.G., Rodrigues, M.V., Martins, L.O., Raven, N.D., and Santos, H. (2006) Occurrence of 1-glyceryl-1-myo-inosityl phosphate in hyperthermophiles. Appl Environ Microbiol 72: 6169-6173.
19. Logsdon, J.M., and Faguy, D.M. (1999) Thermotoga heats up lateral gene transfer. Curr Biol 9: R747-R751.
20. Majumder, A.L., Chatterjee, A., Ghosh Dastidar, K., and Majee, M. (2003) Diversification and evolution of L-myo-inositol 1-phosphate synthase. FEBS Lett 553: 3-10.
21. Martins, L.O., Carreto, L.S., da Costa, M.S., and Santos, H. (1996) New compatible solutes related to di-myo-inositol-phosphate in members of the order Thermotogales. J Bacteriol 178: 5644-5651.
22. Michell, R.H. (2008) Inositol derivatives: evolution and functions. Nat Rev Mol Cell Biol 9: 151-161.
23. Michell, R.H. (2011) Inositol and its derivatives: Their evolution and functions. Adv Enzyme Regul 51: 84-90.
24. Morii, H., Kiyonari, S., Ishino, Y., and Koga, Y. (2009) A novel biosynthetic pathway of archaetidyl-myo-inositol via archaetidyl-myo-inositol phosphate from CDP-archaeol and d-glucose 6-phosphate in methanoarchaeon Methanothermobacter thermautotrophicus cells. J Biol Chem 284: 30766-30774.
25. Morii, H., Ogawa, M., Fukuda, K., Taniguchi, H., and Koga, Y. (2010) A revised biosynthetic pathway for phosphatidylinositol in Mycobacteria. J Biochem 148: 593-602.
26. Nanavati, D.M., Thirangoon, K., and Noll, K.M. (2006) Several archaeal homologs of putative oligopeptide-binding proteins encoded by Thermotoga maritima bind sugars. Appl Environ Microbiol 72: 1336-1345.
27. Neelon, K., Wang, Y., Stec, B., and Roberts, M.F. (2005) Probing the mechanism of the Archaeoglobus fulgidus inositol-1-phosphate synthase. J Biol Chem 280: 11475-11482.
28. Nelson, K.E., Clayton, R.A., Gill, S.R., Gwinn, M.L., Dodson, R.J., Haft, D.H., etal. (1999) Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399: 323-329.
29. Nesbø, C.L., L'Haridon, S., Stetter, K.O., and Doolittle, W.F. (2001) Phylogenetic analyses of two 'archaeal' genes in Thermotoga maritima reveal multiple transfers between archaea and bacteria. Mol Biol Evol 18: 362-375.
30. Niederberger, T.D., Gotz, D.K., McDonald, I.R., Ronimus, R.S., and Morgan, H.W. (2006) Ignisphaera aggregans gen. nov., sp. nov., a novel hyperthermophilic crenarchaeote isolated from hot springs in Rotorua and Tokaanu, New Zealand. Int J Syst Evol Microbiol 56: 965-971.
31. Noll, K.M., Lapierre, P., Gogarten, J.P., and Nanavati, D.M. (2008) Evolution of mal ABC transporter operons in the Thermococcales and Thermotogales. BMC Evol Biol 8: 7.
32. Nunes, O.C., Manaia, C.M., da Costa, M.S., and Santos, H. (1995) Compatible solutes in the thermophilic bacteria Rhodothermus marinus and 'Thermus thermophilus'. Appl Environ Microbiol 61: 2351-2357.
33. Pruesse, E., Quast, C., Knittel, K., Fuchs, B., Ludwig, W., Peplies, J., and Glöckner, F.O. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
34. Rodionov, D.A., Kurnasov, O.V., Stec, B., Wang, Y., Roberts, M.F., and Osterman, A.L. (2007) Genomic identification and in vitro reconstitution of a complete biosynthetic pathway for the osmolyte di-myo-inositol-phosphate. Proc Natl Acad Sci USA 104: 4279-4284.
35. Rodrigues, M.V., Borges, N., Henriques, M., Lamosa, P., Ventura, R., Fernandes, C., etal. (2007) Bifunctional CTP:inositol-1-phosphate cytidylyltransferase/CDP inositol:inositol-1-phosphate transferase, the key enzyme for di-myo-inositol-phosphate synthesis in several (hyper)thermophiles. J Bacteriol 189: 5405-5412.
36. Rodrigues, M.V., Borges, N., Almeida, C.P., Lamosa, P., and Santos, H. (2009) A unique β-1, 2-mannosyltransferase of Thermotoga maritima that uses di-myo-inositol phosphate as the mannosyl acceptor. J Bacteriol 191: 6105-6115.
37. Ronquist, F., and Huelsenbeck, J.P. (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
38. Santos, H., Lamosa, P., Borges, N., Gonçalves, L.G., Pais, T.M., and Rodrigues, M.V. (2011) Organic compatible solutes of prokaryotes that thrive in hot environments: the importance of ionic compounds for thermostabilization. In Extremophiles Handbook. Horikoshi, K., Antranikian, G., Bull, A.T., Robb, F.T., and Stetter, K.O. (eds). Tokyo: Springer, pp. 497-520.
39. Scholz, S., Sonnenbichler, J., Schäfer, W., and Hensel, R. (1992) Di-myo-inositol-1, 1'-phosphate: a new inositol phosphate isolated from Pyrococcus woesei. FEBS Letters 306: 239-242.
40. Shibata, T., Nakasu, S., Yasui, K., and Kikuchi, A. (1987) Intrinsic DNA-dependent ATPase activity of reverse gyrase. J Biol Chem 262: 10419-10421.
41. Silva, Z., Borges, N., Martins, L.O., Wait, R., da Costa, M.S., and Santos, H. (1999) Combined effect of the growth temperature and salinity of the medium on the accumulation of compatible solutes by Rhodothermus marinus and Rhodothermus obamensis. Extremophiles 3: 163-172.
42. Swoboda, J.G., Campbell, J., Meredith, T.C., and Walker, S. (2010) Wall teichoic acid function, biosynthesis, and inhibition. Chembiochem 11: 35-45.
43. Yanai, I., Wolf, Y.I., and Koonin, E.V. (2002) Evolution of gene fusions: horizontal transfer versus independent events. Genome Biol 3: research0024.