1887

Abstract

Collagen molecules are structural in nature and primarily found in eukaryotic, multicellular organisms. Recently, a collagen-like protein, TrpA, was identified and characterized in the marine cyanobacterium IMS 101, and it was shown to be involved in maintaining the structural integrity of the trichomes. The TrpA protein contains one glycine interruption in the otherwise perfectly uninterrupted collagenous domain. In this study, we used phylogenetic analysis to determine that the TrpA protein sequence is most closely associated with non-fibril-forming collagen proteins. Structural modelling and circular dichroism data suggest that the glycine insertion decreases the stability of TrpA compared to uninterrupted collagen sequences. Additionally, scanning electron microscopy revealed that TrpA is expressed entirely on the surface of the trichomes, with no specific pattern of localization. These data indicate that the TrpA protein is part of the outer sheath of this organism. As such, this protein may function to promote adhesion between individual . trichomes, and between this organism and heterotrophic bacteria found in the same environment.

Funding
This study was supported by the:
  • National Science Foundation (Award CMMI-0900101)
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2014-10-01
2024-04-19
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References

  1. Arnold K., Bordoli L., Kopp J., Schwede T. ( 2006). The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201 [View Article][PubMed]
    [Google Scholar]
  2. Bächinger H. P., Morris N. P., Lunstrum G. P., Keene D. R., Rosenbaum L. M., Compton L. A., Burgeson R. E. ( 1990). The relationship of the biophysical and biochemical characteristics of type VII collagen to the function of anchoring fibrils. J Biol Chem 265:10095–10101[PubMed]
    [Google Scholar]
  3. Bella J., Liu J., Kramer R., Brodsky B., Berman H. M. ( 2006). Conformational effects of Gly-X-Gly interruptions in the collagen triple helix. J Mol Biol 362:298–311 [View Article][PubMed]
    [Google Scholar]
  4. Bordoli L., Kiefer F., Arnold K., Benkert P., Battey J., Schwede T. ( 2008). Protein structure homology modeling using SWISS-MODEL workspace. Nat Protoc 4:1–13 [View Article][PubMed]
    [Google Scholar]
  5. Boydston J. A., Chen P., Steichen C. T., Turnbough C. L. Jr ( 2005). Orientation within the exosporium and structural stability of the collagen-like glycoprotein BclA of Bacillus anthracis . J Bacteriol 187:5310–5317 [View Article][PubMed]
    [Google Scholar]
  6. Brodsky B., Ramshaw J. A. ( 1997). The collagen triple-helix structure. Matrix Biol 15:545–554 [View Article][PubMed]
    [Google Scholar]
  7. Burgeson R. E. ( 1993). Type VII collagen, anchoring fibrils, and epidermolysis bullosa. J Invest Dermatol 101:252–255 [View Article][PubMed]
    [Google Scholar]
  8. Capone D. G., Zehr J. P., Paerl H. W., Bergman B., Carpenter E. J. ( 1997). Trichodesmium, a globally significant marine cyanobacterium. Science 276:1221–1229 [View Article]
    [Google Scholar]
  9. Exposito J.-Y., Garrone R. ( 1990). Characterization of a fibrillar collagen gene in sponges reveals the early evolutionary appearance of two collagen gene families. Proc Natl Acad Sci U S A 87:6669–6673 [View Article][PubMed]
    [Google Scholar]
  10. Exposito J. Y., Cluzel C., Garrone R., Lethias C. ( 2002). Evolution of collagens. Anat Rec 268:302–316 [View Article][PubMed]
    [Google Scholar]
  11. Flores E., Pernil R., Muro-Pastor A. M., Mariscal V., Maldener I., Lechno-Yossef S., Fan Q., Wolk C. P., Herrero A. ( 2007). Septum-localized protein required for filament integrity and diazotrophy in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 189:3884–3890 [View Article][PubMed]
    [Google Scholar]
  12. Geer L. Y., Marchler-Bauer A., Geer R. C., Han L., He J., He S., Liu C., Shi W., Bryant S. H. ( 2010). The NCBI BioSystems database. Nucleic Acids Res 38:Database issueD492–D496 [View Article][PubMed]
    [Google Scholar]
  13. Gouy M., Guindon S., Gascuel O. ( 2010). SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224 [View Article][PubMed]
    [Google Scholar]
  14. Guex N., Peitsch M. C. ( 1997). SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723 [View Article][PubMed]
    [Google Scholar]
  15. Guindon S., Lethiec F., Duroux P., Gascuel O. ( 2005). PHYML Online a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:Suppl. 2W557–W559 [View Article][PubMed]
    [Google Scholar]
  16. Hulmes D. J. ( 2002). Building collagen molecules, fibrils, and suprafibrillar structures. J Struct Biol 137:2–10 [View Article][PubMed]
    [Google Scholar]
  17. Hwang E. S., Brodsky B. ( 2012). Folding delay and structural perturbations caused by type IV collagen natural interruptions and nearby Gly missense mutations. J Biol Chem 287:4368–4375 [View Article][PubMed]
    [Google Scholar]
  18. Kadler K. E., Baldock C., Bella J., Boot-Handford R. P. ( 2007). Collagens at a glance. J Cell Sci 120:1955–1958 [View Article][PubMed]
    [Google Scholar]
  19. Kielty C. M., Grant M. E. ( 2003). The collagen family: structure, assembly, and organization in the extracellular matrix. . Connective Tissue and its Heritable Disorders: Molecular, Genetic and Medical Aspects, 2nd edn.159–221 Royce P. M., Steinmann B. Hoboken, NJ: John Wiley & sons;
    [Google Scholar]
  20. Krane D. E., Raymer M. ( 2003). Fundamental Concepts of Bioinformatics San Francisco, CA: Benjamin Cummings;
    [Google Scholar]
  21. Kustka A. B., Sañudo-Wilhelmy S. A., Carpenter E. J., Capone D., Burns J., Sunda W. G. ( 2003). Iron requirements for dinitrogen- and ammonium-supported growth in cultures of Trichodesmium (IMS101): comparison with nitrogen fixation rates and iron : carbon ratios in field populations. Limnol Oceanogr 48:1869–1884 [View Article]
    [Google Scholar]
  22. Layton B. E., D’Souza A. J., Dampier W., Zeiger A., Sabur A., Jean-Charles J. ( 2008). Collagen’s triglycine repeat number and phylogeny suggest an interdomain transfer event from a Devonian or Silurian organism into Trichodesmium erythraeum . J Mol Evol 66:539–554 [View Article][PubMed]
    [Google Scholar]
  23. Lenes J. M., Darrow B. P., Cattrall C., Heil C. A., Callahan M., Vargo G. A., Byrne R. H., Prospero J. M., Bates D. E., Fanning K. A. ( 2001). Iron fertilization and the Trichodesmium response on the West Florida shelf. Limnol Oceanogr 46:1261–1277 [View Article]
    [Google Scholar]
  24. Letunic I., Bork P. ( 2011). Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:Suppl. 3W475–W478 [View Article][PubMed]
    [Google Scholar]
  25. Mann K., Gaill F., Timpl R. ( 1992). Amino-acid sequence and cell-adhesion activity of a fibril-forming collagen from the tube worm Riftia pachyptila living at deep sea hydrothermal vents. Eur J Biochem 210:839–847 [View Article][PubMed]
    [Google Scholar]
  26. Marga F., Grandbois M., Cosgrove D. J., Baskin T. I. ( 2005). Cell wall extension results in the coordinate separation of parallel microfibrils: evidence from scanning electron microscopy and atomic force microscopy. Plant J 43:181–190 [View Article][PubMed]
    [Google Scholar]
  27. Mariscal V., Herrero A., Nenninger A., Mullineaux C. W., Flores E. ( 2011). Functional dissection of the three-domain SepJ protein joining the cells in cyanobacterial trichomes. Mol Microbiol 79:1077–1088 [View Article][PubMed]
    [Google Scholar]
  28. Mohs A., Silva T., Yoshida T., Amin R., Lukomski S., Inouye M., Brodsky B. ( 2007). Mechanism of stabilization of a bacterial collagen triple helix in the absence of hydroxyproline. J Biol Chem 282:29757–29765 [View Article][PubMed]
    [Google Scholar]
  29. Pêcher J., Pires V., Djaafri I., Da Nascimento S., Fauvel-Lafève F., Legrand C., Sonnet P. ( 2009). Circular dichroism studies of type III collagen mimetic peptides with anti- or pro-aggregant activities on human platelets. Eur J Med Chem 44:2643–2650 [View Article][PubMed]
    [Google Scholar]
  30. Price S., Anandan S. ( 2013). Characterization of a novel collagen-like protein TrpA in the cyanobacterium Trichodesmium erythraeum IMS 101. J Phycol 49:758–764 [View Article]
    [Google Scholar]
  31. Rasmussen M., Jacobsson M., Björck L. ( 2003). Genome-based identification and analysis of collagen-related structural motifs in bacterial and viral proteins. J Biol Chem 278:32313–32316 [View Article][PubMed]
    [Google Scholar]
  32. Roe K. L., Barbeau K., Mann E. L., Haygood M. G. ( 2012). Acquisition of iron by Trichodesmium and associated bacteria in culture. Environ Microbiol 14:1681–1695 [View Article][PubMed]
    [Google Scholar]
  33. Roy, A., Kucukural, A. & Zhang,Y. ( 2010) I-Tasser: a unified platform for automated protein structure and function prediction. Nat Protoc 5725–738 [CrossRef]
    [Google Scholar]
  34. Rubin M., Berman-Frank I., Shaked Y. ( 2011). Dust- and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium . Nat Geosci 4:529–534 [View Article]
    [Google Scholar]
  35. Schwede T., Kopp J. R., Guex N., Peitsch M. C. ( 2003). SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381–3385 [View Article][PubMed]
    [Google Scholar]
  36. Shoulders M. D., Raines R. T. ( 2009). Collagen structure and stability. Annu Rev Biochem 78:929–958 [View Article][PubMed]
    [Google Scholar]
  37. Sicot F.-X., Exposito J.-Y., Masselot M., Garrone R., Deutsch J., Gaill F. ( 1997). Cloning of an annelid fibrillar-collagen gene and phylogenetic analysis of vertebrate and invertebrate collagens. Eur J Biochem 246:50–58 [View Article][PubMed]
    [Google Scholar]
  38. Sylvestre P., Couture-Tosi E., Mock M. ( 2002). A collagen-like surface glycoprotein is a structural component of the Bacillus anthracis exosporium. Mol Microbiol 45:169–178 [View Article][PubMed]
    [Google Scholar]
  39. Toal S., Amidi O., Schweitzer-Stenner R. ( 2011). Conformational changes of trialanine induced by direct interactions between alanine residues and alcohols in binary mixtures of water with glycerol and ethanol. J Am Chem Soc 133:12728–12739 [View Article][PubMed]
    [Google Scholar]
  40. Whatmore A. M. ( 2001). Streptococcus pyogenes sclB encodes a putative hypervariable surface protein with a collagen-like repetitive structure. Microbiology 147:419–429[PubMed]
    [Google Scholar]
  41. Zhang Y. ( 2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40 [View Article][PubMed]
    [Google Scholar]
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