Identification and first insights into the structure and biosynthesis of chitin from the freshwater sponge Spongilla lacustris

Journal of Structural Biology

Volumn 183, Issue 3, 2013, Pages 474-483

  Ehrlich, Hermann ^a,c   Kaluzhnaya, Oksana V ^b,c   Brunner, Eike ^c   Tsurkan, Mikhail V ^d   Ereskovsky, Alexander ^e   Ilan, Micha ^f   Tabachnick, Konstantin R ^g   Bazhenov, Vasilii V ^a   Paasch, Silvia ^c   Kammer, Martin ^c   Born, René ^c   Stelling, Allison ^h   Galli, Roberta ^h   Belikov, Sergei ^b   Petrova, Olga V ⁱ   Sivkov, Victor V ⁱ   Vyalikh, Denis ^c   Hunoldt, Sebastian ^c   Wörheide, Gert ^j,k  

^a TU BERGAKADEMIE FREIBERG   (Germany)

^b LIMNOLOGICAL INSTITUTE   (Russian Federation)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d LEIBNIZ INSTITUTE OF POLYMER RESEARCH DRESDEN   (Germany)

^e AIX MARSEILLE UNIVERSITY   (France)

^f TEL AVIV UNIVERSITY   (Israel)

^g SHIRSHOV INSTITUTE OF OCEANOLOGY   (Russian Federation)

^h UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

ⁱ INSTITUTE OF BIOLOGY   (Russian Federation)

^j UNIVERSITY OF MUNICH   (Germany)

^k BAYERISCHE STAATSSAMMLUNG FÜR PALÄONTOLOGIE UND GEOLOGIE   (Germany)

more..

Author keywords

Bioanalytics; Chitin; Chitin synthase; Skeleton; Sponges

Indexed keywords

ALPHA CHITIN; BETA CHITIN; BIOPOLYMER; CHITIN; CHITIN DERIVATIVE; CHITIN SYNTHASE; FRESH WATER; UNCLASSIFIED DRUG;

ARTICLE; ASSAY; BIOSYNTHESIS; CARBON 13 SOLID STATE NUCLEAR MAGNETIC RESONANCE; CARBON NUCLEAR MAGNETIC RESONANCE; ELECTROSPRAY MASS SPECTROMETRY; GENETIC ANALYSIS; INFRARED SPECTROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAMAN SPECTROMETRY; SPONGE (PORIFERA); SPONGILLA LACUSTRIS; STAINING;

ANIMALIA; HEXACTINELLIDA; SPONGILLA LACUSTRIS; SPONGILLIDAE;

BIOANALYTICS; CHITIN; CHITIN SYNTHASE; SKELETON; SPONGES;

ACETYLGLUCOSAMINE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CHITIN; CHITIN SYNTHASE; CLONING, MOLECULAR; MOLECULAR SEQUENCE DATA; PORIFERA; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; X-RAY ABSORPTION SPECTROSCOPY;

EID: 84883466136     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2013.06.015     Document Type: Article

References (65)

1. Addis J.S., Peterson K.J. Phylogenetic relationships of freshwater sponges (Porifera, Spongillina) inferred from analyses of 18S rDNA, COI mtDNA, and ITS2 rDNA sequences. Zool. Scripta 2005, 34:549-557.
2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
3. Banks I.R., Specht C.A., Donlin M.J., Gerik K.J., Levitz S.M., et al. A chitin synthase and its regulator protein are critical for chitosan production and growth of the fungal pathogen Cryptococcus neoformans. Eukaryot. Cell. 2005, 4:1902-1912.
4. Banoub J., Boullanger P., Lafont D., Cohen A., El Aneed A., et al. In situ formation of c-glycosides during electrospray ionization tandem mass spectrometry of a series of synthetic amphiphilic cholesteryl polyethoxy neoglycolipids containing N-acetyl-d-glucosamine. J. Am. Soc. Mass Spectrom. 2005, 16:565-570.
5. Boden N., Sommer U., Spindler K.-D. Demonstration and characterization of chitinases in the Drosophila-K-cell line. Insect. Biochem. 1985, 15:19-23.
6. Boury-Esnault N. Systematics and evolution of Demospongiae. Can. J. Zool. 2006, 84:205-224.
7. Brunner E., Ehrlich H., Schupp P., Hedrich R., Hunoldt S., et al. Chitin-based scaffolds are an integral part of the skeleton of the marine demosponge Ianthella basta. J. Struct. Biol. 2009, 168:539-547.
8. Brunner E., Richthammer P., Ehrlich H., Paasch S., Simon P., et al. Chitin-based organic networks: An integral part of cell wall biosilica in the diatom Thalassiosira pseudonana. Angew. Chem. Int. 2009, 48:9724-9727.
9. Bulawa C.E. Genetics and molecular biology of chitin synthesis in fungi. Ann. Rev. Microbiol. 1993, 47:505-534.
10. Dauby P., Jeuniaux C. Origine exogene de la chitine d'cel'e chez les Spongiares. Cah. Biol. Mar. 1986, 28:121-129.
11. Dembo, M.G., 1996. Ecophysiology and biology of Lake Kinneret sponges. M.Sc. thesis, Department of Zoology, Tel Aviv University.
12. Dohrmann M., Wörheide G. Novel scenarios of early animal evolution - Is it time to rewrite textbooks?. Integr. Comp. Biol. 2013, pp. 1-9. 10.1093/icb/ict008.
13. Ehrlich H. Chitin and collagen as universal and alternative templates in biomineralization. Int. Geol. Rev. 2010, 52:661-699.
14. Ehrlich H., Maldonado M., Spindler K.-D., Eckert C., Hanke T., et al. First evidence of chitin as a component of the skeletal fibers of marine sponges. Part I. Verongidae (Demospongia: Porifera). J. Exp. Zool. A. Mol. Dev. Evol. 2007, 308B:347-356.
15. Ehrlich H., Krautter M., Hanke T., Simon P., Knieb C., et al. First evidence of the presence of chitin in skeletons of marine sponges. Part II. Glass sponges (Hexactinellida: Porifera). J. Exp. Zool. A. Mol. Dev. Evol. 2007, 308B:473-483.
16. Ehrlich H., Worch H. Sponges as natural composites: from biomimetic potential to development of new biomaterials. Porifera Research: Biodiversity, Innovation and Sustainability 2007, 217-223. Museu Nacional, Rio de Janeiro. E. Hajdu (Ed.).
17. Ehrlich H., Janussen D., Simon P., Heinemann S., Bazhenov V.V., et al. Nanostructural organization of naturally occurring composites: Part II. Silica-chitin-based biocomposites. J. Nanomater. 2008, 10.1155/2008/623838.
18. Ehrlich H., Deutzmann R., Brunner E., Cappellini E., Koon H., et al. Mineralization of the metre-long biosilica structures of glass sponges is templated on hydroxylated collagen. Nature Chem. 2010, 2:1084-1088.
19. Ehrlich H., Hanke T., Simon P., Born R., Fischer C., et al. Carboxymethylation of the fibrillar collagen with respect to formation of hydroxyapatite. J. Biomed. Mater. Res. B. Appl. Biomater. 2010, 92:542-551.
20. Ehrlich H., Ilan M., Maldonado M., Muricy G., Bavestrello G., et al. Three-dimensional chitin-based scaffolds from Verongida sponges (Demospongiae: Porifera). Part I. Isolation and identification of chitin. Int. J. Biol. Macromol. 2010, 47:132-140.
21. Ehrlich H., Kaluzhnaya O.V., Tsurkan M.V., Ereskovsky A., Tabachnick K.R., et al. First report on chitinous holdfast in sponges (Porifera). Proc. Royal Soc. B 2013, 280:20130339.
22. Erpenbeck D., Weier T., de Voogd N.J., Wörheide G., Sutcliffe P., et al. Insights into the evolution of freshwater sponges (Porifera: Demospongiae: Spongillina): Barcoding and phylogenetic data from Lake Tanganyika endemics indicate multiple invasions and unsettle existing taxonomy. Mol. Phyl. Evol. 2011, 61:231-236.
23. Erwin D.H., Laflamme M., Tweedt S.M., Sperling E.A., Pisani D., et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 2011, 334:1091-1097.
24. Frost, T.M. (1978). The ecology of the freshwater sponge Spongilla lacustris. Thesis, Dartmouth College, Hanover.
25. Frost T.M. Clearance rate determinations for the freshwater sponge Spongilla lacustris: effect of temperature, particle type and concentration, and sponge size. Arch. Hydrobiol. 1980, 90:330-356.
26. Frost T.M. Porifera. Ecology and Classification of North American Freshwater Invertebrates 1991, 95-124. Academic Press Inc., San Diego. J.H. Thorp, A.P. Covich (Eds.).
27. Frost T.M., Williamson C.E. In situ determination of the effect of symbiotic algae on the growth of the freshwater sponge Spongilla lacustris. Ecology 1980, 6:1361-1370.
28. Frost T.M., de Nagy G.S., Gilbert J.J. Population dynamics and standing biomass of the freshwater sponge Spongilla lacustris. Ecology 1982, 63:1203-1210.
29. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nulc. Acids Symp. 1999, 41:95-98.
30. Harrison F.W. Sponges (Porifera: Spongillidae). Pollution Ecology of Freshwater Invertebrates 1974, 29-66. Academic Press, New York. C.V. Hart, L.H. Fuller (Eds.).
31. Hickey P.C., Swift S.M., Roca M.G., Read N.D. Live-cell imaging of filamentous fungi using vital fluorescent dyes. Meth. Microbiol. 2005, 34:63-87.
32. Hogenkamp D.G., Arakane Y., Zimoch L., Merzendorfer H., Kramer K.J., et al. Chitin synthase genes in Manduca sexta: Characterization of a gut-specific transcript and differential tissue expression of alternately spliced mRNAs during development. Insect Biochem. Mol. Biol. 2005, 35:529-540.
33. Hsu J., Chang S.J., Fran A.L. MALDI-TOF and ESI-MS analysis of oligosaccharides labeled with a new multifunctional oligosaccharide tag. J. Am. Soc. Mass Spectrom. 2006, 17:194-204.
34. Ilan M., Dembo M.G., Gasith A. Gemmules of sponges from a warm lake. Freshwater Biology 1996, 35:165-172.
35. Jackson D.J., Macis L., Reitner J., Degnan B.M., Wörheide G. Sponge paleogenomics reveals an ancient role for carbonic anhydrase in skeletogenesis. Science 2007, 316:1893-1895.
36. Jayakumar R., Tamura H. Synthesis, characterization and thermal properties of chitin-g-poly(ε-caprolactone) copolymers by using chitin hydrogel. Int. J. Biol. Macromol. 2008, 43:32-36.
37. Jeuniaux C. Chitine et Chitinolyse: un Chapitre de la Biologie Moleculaire 1963, Masson et Cie, Paris.
38. Kahl K., Konopacka A. Oligochaeta inhabiting the colonies of the sponge Spongilla lacustris (L.) in the river Gac. Acta Hydrobiol. 1981, 23:243-249.
39. 13C solid-state NMR. Macromol. Biosci. 2005, 5:103-106.
40. 13C resonance assignment of α- and β-chitin. Biopolymers 2004, 75:255-263.
41. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
42. Kunike G. Nachweis und Verbreitung organischer Skelettsubstanzen bei Tieren. Zeitschr. Vergl. Physiol. 1925, 2:233-253.
43. Linnaeus, C., 1759. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, Tomus II. Editio decima, reformata. Laurentii Salvii, Holmiae.
44. Manconi, R., Pronzato, R., 2002. Suborder Spongillina subord. nov. freshwater sponges. In: Hooper, J.N.A., van Soest, R.W.M. (Eds.), Systema Porifera. A Guide to the Classification of Sponges 1, Springer, pp. 921-1019.
45. Manconi R., Pronzato R. Global diversity of sponges (Porifera: Spongillina) in freshwater. Hydrobiology 2008, 595:27-33.
46. Meixner M.J., Luter C., Eckert C., Itskovich V., Janussen D., et al. Phylogenetic analysis of freshwater sponges provide evidence for endemism and radiation in ancient lakes. Mol. Phylogenet. Evol. 2007, 45:875-886.
47. Nguyen T.H., Fleet G.H., Rogers P.L. Composition of the cell walls of several yeast species. Appl. Microbiol. Biotechnol. 1998, 50:206-212.
48. Noishiki Y., Takami H., Nishiyama Y., Wada M., Okada S., et al. Alkali-induced conversion of β-chitin to α -chitin. Biomacromolecules 2003, 4:869-899.
49. Odier A. Memoire sur la composition chimique des parties cornees des insects. Mem. Soc. Hist. Nat. Paris 1823, 1:29-42.
50. Peter M.G. Chitin and chitosan in fungi. Biopolymers. 6, Polysaccharides II 2002, Wiley-VCH, Weinheim. A. Steinbüchel (Ed.).
51. Pfannkuchen M., Brümmer F. Heterologous expression of DsRed2 in young sponges (Porifera). Int. J. Dev. Biol. 2009, 53:1113-1117.
52. Philippe H., Derelle R., Lopez P., Pick K., Borchiellini C., et al. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 2009, 19:706-712.
53. Pick K.S., Philippe H., Schreiber F., Erpenbeck D., Jackson D.J., et al. Improved phylogenomic taxon sampling noticeably affects non-bilaterian relationships. Mol. Biol. Evol. 2010, 27:1983-1987.
54. Ramirez G.M., Avelizapa R.L.I., Avelizapa R.N.G., Camarillo C.R. Colloidal chitin stained with Remazol Brilliant Blue R, a useful substrate to select chitinolytic microorganisms and to evaluate chitinases. J. Microbiol. Meth. 2004, 56:213-219.
55. Reitner J., Wörheide G. Non-lithistid fossil demospongiae? Origins of their palaeobiodiversity and highlights in history of preservation. Systema Porifera. A Guide to the Classification of Sponges 2002, 52-68. Kluwer Academic/Plenum Publishers, NY. J.N.A. Hooper, R.W.M. van Soest (Eds.).
56. Rost B., Yachdav G., Liu J. The predict protein server. Nucleic Acids Res. 2004, 32:W321-W326.
57. Saller U. Microscopical aspects on symbiosis of Spongilla lacustris (Porifera, Spongillidae) and green algae. Zoomorphism 1989, 108:291-296.
58. Saller U., Weissenfels N. The development of Spongilla lacustris from the oocyte to the free larva (Porifera, Spongillidae). Zoomorphism 1985, 105:367-374.
59. Sonnhammer E.L., Eddy S.R., Birney E., Bateman A., Durbin R. Pfam: multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res. 1998, 26:320-322.
60. Srivastava M., Simakov O., Chapman J., Fahey B., Gauthier M.E., et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 2010, 466:720-726.
61. Stach S. Polysaccharide aus marinen Bakterien und der Mikroalge Chlorella vulgaris 2005, Cuvillier, Göttingen.
62. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
63. Weissenfels N. Biologie und Mikroskopische Anatomie der Süßwasserschwämme (Spongillidae) 1989, Urban and Fischer, Munchen.
64. Wörheide G., Dohrmann M., Erpenbeck D., Larroux C., Maldonado M., et al. Deep phylogeny and evolution of sponges (Phylum Porifera). Adv. Mar. Biol. 2012, 61:1-78.
65. Yao Y.Y., Shrestha K.L., Wu Y.J., Tasi H.J., Chen C.C., et al. Structural simulation and protein engineering to convert an endo-chitosanase to an exo-chitosanase. Protein Eng. Des. Sel. 2008, 21:561-566.