Skip to main content
Log in

Tracing the spread of fibronectin type III domains in bacterial glycohydrolases

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • 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 31:2068–2073

    Google Scholar 

  • Bazan JF (1990) Structural design and molecular evolution of a cytokine receptor superfamily. Proc Natl Acad Sci USA 87:6934–6938

    Google Scholar 

  • 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 214:659–669

    Google Scholar 

  • Bork P, Doolittle RF (1992) Proposed acquisition of an animal protein domain by bacteria. Proc Natl Acad Sci USA 89:8990–8994

    Google Scholar 

  • Bork P, Doolittle RF (1994) The Drosophila kelch motif is derived from a common enzyme fold. J Mol Biol 236:1277–1288

    Google Scholar 

  • Brisson-Noël A, Arthur M, Courvalin P (1988) Evidence for natural gene transfer from gram-positive cocci to Escherichia coli. J Bacteriol 170:1739–1745

    Google Scholar 

  • 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 22:91–95

    Google Scholar 

  • 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 191:177–185

    Google Scholar 

  • deVos AM, Ultsch M, Kossiakoff AA (1992) Human growth hormone and extracellular domain of its receptor—crystal structure of the complex. Science 255:306–312

    Google Scholar 

  • Doolittle RF (1987) Of URFs and ORFs. A primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley, CA

    Google Scholar 

  • 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 659–669

    Google Scholar 

  • 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: 451–453

    Google Scholar 

  • Feng D-F, Doolittle RF (1987) Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol 25:351–360

    Google Scholar 

  • 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 375–387

    Google Scholar 

  • Fujii T, Miyashita K (1993) Multiple domain structure in a chitinase gene (chiC) of Streptomyces lividans. J Gen Microbiol 139:677–686

    Google Scholar 

  • 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 175:1891–1899

    Google Scholar 

  • 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 55:303–315

    Google Scholar 

  • 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 217:70–76

    Google Scholar 

  • 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 106:109–114

    Google Scholar 

  • Hansen CK (1992) Fibronectin type III-like sequences and a new domain type in prokaryotic depolymerases with insoluble substrates. FEBS Lett 305:91–96

    Google Scholar 

  • 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 172:4988–4995

    Google Scholar 

  • Heinemann JA (1991) Genetics of gene transfer between species. Trends Genet 7:181–185

    Google Scholar 

  • Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:309–316

    Google Scholar 

  • Henrissat B, Bairoch A (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J (1993) 293:781–788

    Google Scholar 

  • Holt JG, ed (1984) Bergey's manual of systematic bacteriology, volumes 1–4. Williams & Wilkins, Baltimore, MD

    Google Scholar 

  • 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 32:12548–12553

    Google Scholar 

  • 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 258:987–991

    Google Scholar 

  • Mathupala S, Saha BC, Zeikus JG (1990) Substrate competition and specificity at the active site of amylopullulanase from Clostridium thermohydrosulfuricum. Biochem Biophys Res Commun 166:126–132

    Google Scholar 

  • Mazodier P, Davies J (1991) Gene transfer between distantly related bacteria. Annu Rev Genet 25:147–171

    Google Scholar 

  • Médigue C, Rouxel T, Vigier P, Hénaut A, Danchin A (1991) Evidence for horizontal gene transfer in Escherichia coil speciation. J Mol Biol 222:851–856

    Google Scholar 

  • 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 173:7126–7135

    Google Scholar 

  • 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 173:308–314

    Google Scholar 

  • 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: 1910–1918

    Google Scholar 

  • Melasniemi H, Paloheimo M, Hemiö L (1990) Nucleotide sequence of the α-amylase-pullulanase gene from Clostridium thermohydrosulfuricum. J Gen Microbiol 136:447–454

    Google Scholar 

  • Parkinson JS, Kofoid EC (1992) Communication modules in bacterial signaling proteins. Ann Rev Genet 26:71–112

    Google Scholar 

  • Patthy L (1990) Homology of a domain of the growth hormone/ prolactin receptor family with type III modules of fibronectin. Cell 61:13–14

    Google Scholar 

  • Robbins PW, Overbye K, Albright C, Benfield B, Pero J (1992) Cloning and high-level expression of chitinase-encoding gene of Streptomyces plicatus. Gene 111:69–76

    Google Scholar 

  • Rohde K, Bork P (1993) A fast, sensitive pattern-matching approach for protein sequences. CABIOS 9:183–189

    Google Scholar 

  • 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 171:184–189

    Google Scholar 

  • 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 304:89–92

    Google Scholar 

  • Siggens KW (1987) Molecular cloning and characterization of the beta-amylase gene from Bacillus circulans. Mol Microbiol 1:86–91

    Google Scholar 

  • Smith JM (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126–129

    Google Scholar 

  • Smith MW, Feng D-F, Doolittle RF (1992) Evolution by acquisition: the case for horizontal gene transfers. TIBS 17:489–493

    Google Scholar 

  • 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 4:3585–3587

    Google Scholar 

  • 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: 113–117

    Google Scholar 

  • 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 171:375–382

    Google Scholar 

  • 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 175:1293–1302

    Google Scholar 

  • 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 265:15659–15665

    Google Scholar 

  • 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 174:408–414

    Google Scholar 

  • Whittam TS (1992) Sex in the soil. Curr Biol 2:676–678

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Correspondence to: R.F. Doolittle

Rights and permissions

Reprints and permissions

About this article

Cite this article

Little, E., Bork, P. & Doolittle, R.F. Tracing the spread of fibronectin type III domains in bacterial glycohydrolases. J Mol Evol 39, 631–643 (1994). https://doi.org/10.1007/BF00160409

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00160409

Key words

Navigation