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Journal of Molecular Evolution

, Volume 39, Issue 6, pp 631–643 | Cite as

Tracing the spread of fibronectin type III domains in bacterial glycohydrolases

  • Elizabeth Little
  • Peer Bork
  • Russell F. Doolittle
Article

Abstract

The evolutionary spread of 22 fibronectin type III (Fn3) sequences among a dozen bacterial enzymes has been traced by searching databases with the non-Fn3 parts of the enzyme sequences. Numerous homologues were found that lacked the Fn3 domains. In each case the related sequences were aligned, phylogenetic trees were constructed, and the occurrences of Fn3 units on the trees were noted. Comparison with phylogenetic trees prepared from the Fn3 segments themselves allowed inferences to be made about when the Fn3 units were shuffled into their present positions.

Key words

Fibronectin type III Bacteria Glycohydrolases Phylogeny Horizontal gene transfers 

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References

  1. Baron M, Main AL, Driscoll PC, Mardon HJ, Boyd J, Campbell ID (1992) 1H NMR assignment and secondary structure of the cell adhesion type III module of fibronectin. Biochemistry 31:2068–2073Google Scholar
  2. Bazan JF (1990) Structural design and molecular evolution of a cytokine receptor superfamily. Proc Natl Acad Sci USA 87:6934–6938Google Scholar
  3. Blaak H, Schnellmann J, Walter S, Henrissat B, Schrempf H (1993) Characteristics of an exochitinase from Streptomyces olivaceoviridis, its corresponding gene, putative protein domains and relationship to other chitinases. Eur J Biochem 214:659–669Google Scholar
  4. Bork P, Doolittle RF (1992) Proposed acquisition of an animal protein domain by bacteria. Proc Natl Acad Sci USA 89:8990–8994Google Scholar
  5. Bork P, Doolittle RF (1994) The Drosophila kelch motif is derived from a common enzyme fold. J Mol Biol 236:1277–1288Google Scholar
  6. Brisson-Noël A, Arthur M, Courvalin P (1988) Evidence for natural gene transfer from gram-positive cocci to Escherichia coli. J Bacteriol 170:1739–1745Google Scholar
  7. Burchhardt G, Wienecke A, Bahl H (1991) Isolation of the pullulanase gene from Clostridium thermosulfurogenes (DM 3896) and its expression in Escherichia coli. Curr Microbiol 22:91–95Google Scholar
  8. Candussio A, Schmid G, Böck A (1990) Biochemical and genetic analysis of a maltopentaose-producing amylase from an alkaliphilic Gram-positive bacterium. Eur J Biochem 191:177–185Google Scholar
  9. deVos AM, Ultsch M, Kossiakoff AA (1992) Human growth hormone and extracellular domain of its receptor—crystal structure of the complex. Science 255:306–312Google Scholar
  10. Doolittle RF (1987) Of URFs and ORFs. A primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley, CAGoogle Scholar
  11. Doolittle RF, Feng D-F (1990) Nearest neighbor procedure for relating progressively aligned amino acid sequences. In: Doolittle RF (ed) Molecular evolution: computer analysis of protein and nucleic acid sequences. Academic Press, New York, pp 659–669Google Scholar
  12. Doolittle RF, Johnson MS, Husain I, Van Houten B, Thomas DC, Sancar A (1986) Domainal evolution of a prokaryotic DNA-repair protein and its relationship to active-transport proteins. Nature 323: 451–453Google Scholar
  13. Feng D-F, Doolittle RF (1987) Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol 25:351–360Google Scholar
  14. Feng D-F, Doolittle RF (1990) Progressive alignment and phylogenetic tree construction of protein sequences. In: Doolittle RF (ed) Molecular evolution: computer analysis of protein and nucleic acid sequences. Academic Press, New York, pp 375–387Google Scholar
  15. Fujii T, Miyashita K (1993) Multiple domain structure in a chitinase gene (chiC) of Streptomyces lividans. J Gen Microbiol 139:677–686Google Scholar
  16. Fujino T, Béguin P, Aubert J-P (1993) Organization of a Clostridium thermocellum gene cluster encoding the cellulosomal scaffolding protein CipA and a protein possibly involved in attachment of the cellulosome to the cell surface. J Bacteriol 175:1891–1899Google Scholar
  17. Gilkes NR, Henrissat B, Kilburn DG, Miller RC Jr, Warren RAJ (1991) Domains in microbial β-1,4-glycanases: sequence conservation, function, and enzyme families. Microbiol Rev 55:303–315Google Scholar
  18. Gräbnitz F, Rücknagel KP, Seiss M, Staudenbauer WL (1989) Nucleotide sequence of the Clostridium thermocellum bglB gene encoding thermostable β-glucosidase B: homology to fungal β-glucosidases. Mol Gen Genet 217:70–76Google Scholar
  19. Guiseppi A, Aymeric JL, Cami B, Barras F, Creuzet N (1991) Sequence analysis of the cellulase-encoding celY gene of Erwinia chrysanthemi: a possible case of interspecies gene transfer. Gene 106:109–114Google Scholar
  20. Hansen CK (1992) Fibronectin type III-like sequences and a new domain type in prokaryotic depolymerases with insoluble substrates. FEBS Lett 305:91–96Google Scholar
  21. He SY, Collmer A (1990) Molecular cloning, nucleotide sequence, and marker exchange mutagenesis of the exo-poly-α-D-galacturonosidase-encoding pehX gene of Erwinia chrysanthemi EC16. J Bacteriol 172:4988–4995Google Scholar
  22. Heinemann JA (1991) Genetics of gene transfer between species. Trends Genet 7:181–185Google Scholar
  23. Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:309–316Google Scholar
  24. Henrissat B, Bairoch A (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J (1993) 293:781–788Google Scholar
  25. Holt JG, ed (1984) Bergey's manual of systematic bacteriology, volumes 1–4. Williams & Wilkins, Baltimore, MDGoogle Scholar
  26. Ingham KC, Brew SA, Migliorini MM, Busby TF (1993) Binding of heparin by type III domains and peptides from the carboxy terminal Hep-2 region of fibronectin. Biochemistry 32:12548–12553Google Scholar
  27. Leahy DJ, Hendrickson WA, Aukhil I, Erickson HP (1992) Structure of a fibronectin type III domain from tenascin phased by MAD analysis of the selenomethyionyl protein. Science 258:987–991Google Scholar
  28. Mathupala S, Saha BC, Zeikus JG (1990) Substrate competition and specificity at the active site of amylopullulanase from Clostridium thermohydrosulfuricum. Biochem Biophys Res Commun 166:126–132Google Scholar
  29. Mazodier P, Davies J (1991) Gene transfer between distantly related bacteria. Annu Rev Genet 25:147–171Google Scholar
  30. Médigue C, Rouxel T, Vigier P, Hénaut A, Danchin A (1991) Evidence for horizontal gene transfer in Escherichia coil speciation. J Mol Biol 222:851–856Google Scholar
  31. Meinke A, Gilkes NR, Kilburn DG, Miller RC Jr, Warren RAJ (1991a) Multiple domains in endoglucanase B (CenB) from Cellulomonas fimi: functions and relatedness to domains in other polypeptides. J Bacteriol 173:7126–7135Google Scholar
  32. Meinke A, Braun C, Gilkes NR, Kilburn DG, Miller RC Jr, Warren RAJ (1991b) Unusual sequence organization in CenB, an inverting endoglucanase from Cellulomonas fimi. J Bacteriol 173:308–314Google Scholar
  33. Meinke A, Gilkes NR, Kilburn DG, Miller RC Jr, Warren RAJ (1993) Cellulose-binding polypeptides from Cellulomonas fimi: endoglucanase D (CenD), a family A β-1,4-glucanase. J Bacteriol 175: 1910–1918Google Scholar
  34. Melasniemi H, Paloheimo M, Hemiö L (1990) Nucleotide sequence of the α-amylase-pullulanase gene from Clostridium thermohydrosulfuricum. J Gen Microbiol 136:447–454Google Scholar
  35. Parkinson JS, Kofoid EC (1992) Communication modules in bacterial signaling proteins. Ann Rev Genet 26:71–112Google Scholar
  36. Patthy L (1990) Homology of a domain of the growth hormone/ prolactin receptor family with type III modules of fibronectin. Cell 61:13–14Google Scholar
  37. Robbins PW, Overbye K, Albright C, Benfield B, Pero J (1992) Cloning and high-level expression of chitinase-encoding gene of Streptomyces plicatus. Gene 111:69–76Google Scholar
  38. Rohde K, Bork P (1993) A fast, sensitive pattern-matching approach for protein sequences. CABIOS 9:183–189Google Scholar
  39. Saito T, Suzuki K, Yamamoto J, Fukui T, Miwa K, Tomita K, Nakanishi S, Odani S, Suzuki J-I, Ishikawa K (1989) Cloning, nucleotide sequence, and expression in Escherichia coli of the gene for poly(3hydroxybutyrate) depolymerase from Alcaligenes faecalis. J Bacteriol 171:184–189Google Scholar
  40. Salamitou, Tokatlidis K, Béguin, Aubert J-P (1992) Involvement of separate domains of the cellulosomal protein S1 of Clostridium thermocellum in binding to cellulose and in anchoring of catalytic subunits to the cellulosome. FEBS Lett 304:89–92Google Scholar
  41. Siggens KW (1987) Molecular cloning and characterization of the beta-amylase gene from Bacillus circulans. Mol Microbiol 1:86–91Google Scholar
  42. Smith JM (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126–129Google Scholar
  43. Smith MW, Feng D-F, Doolittle RF (1992) Evolution by acquisition: the case for horizontal gene transfers. TIBS 17:489–493Google Scholar
  44. Trieu-Cuot P, Gerbaud G, Lambert T, Courvalin P (1985) In vivo transfer of genetic information between gram-positive and gram-negative bacteria. EMBO J 4:3585–3587Google Scholar
  45. Tsujibo H, Endo H, Minoura K, Miyamoto K, Inamori Y (1993) Cloning and sequence analysis of the gene encoding a thermostable chitinase from Streptomyces thermoviolaceus OPC-520. Gene 134: 113–117Google Scholar
  46. Uozumi N, Sakurai K, Sasaki T, Takekawa S, Yamagata H, Tsukagoshi N, Udaka S (1989) A single gene directs synthesis of a precursor protein with β- and α-amylase activities in Bacillus polymyxa. J Bacteriol 171:375–382Google Scholar
  47. Wang WK, Kruss K, Wu JHD (1993) Cloning and DNA sequence of the gene coding for Clostridium thermocellum cellulase Ss (CelS), a major cellulosome component. J Bacteriol 175:1293–1302Google Scholar
  48. Watanabe T, Suzuki K, Oyanagi W, Ohnishi K, Tanaka H (1990) Gene cloning of chitinase A1 from Bacillus circulans WL-12 revealed its evolutionary relationship to Serratia chitinase and to the type III homology units of fibronectin. J Biol Chem 265:15659–15665Google Scholar
  49. Watanabe T, Oyanagi W, Suzuki K, Ohnishi K, Tanaka H (1992) Structure of the gene encoding chitinase D of Bacillus circulans WL-12 and possible homology of the enzyme to other prokaryotic chitinases and class III plant chitinases. J Bacteriol 174:408–414Google Scholar
  50. Whittam TS (1992) Sex in the soil. Curr Biol 2:676–678Google Scholar

Copyright information

© Springer-Verlag New York Inc 1994

Authors and Affiliations

  • Elizabeth Little
    • 1
  • Peer Bork
    • 1
  • Russell F. Doolittle
    • 1
  1. 1.Center for Molecular GeneticsUniversity of CaliforniaSan Diego, La JollaUSA

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