Differences in protein structural regions that impact functional specificity in GT2 family β-glucan synthases.
Journal
PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081
Informations de publication
Date de publication:
2019
2019
Historique:
received:
01
07
2019
accepted:
14
10
2019
entrez:
31
10
2019
pubmed:
31
10
2019
medline:
18
3
2020
Statut:
epublish
Résumé
Most cell wall and secreted β-glucans are synthesised by the CAZy Glycosyltransferase 2 family (www.cazy.org), with different members catalysing the formation of (1,4)-β-, (1,3)-β-, or both (1,4)- and (1,3)-β-glucosidic linkages. Given the distinct physicochemical properties of each of the resultant β-glucans (cellulose, curdlan, and mixed linkage glucan, respectively) are crucial to their biological and biotechnological functions, there is a desire to understand the molecular evolution of synthesis and how linkage specificity is determined. With structural studies hamstrung by the instability of these proteins to solubilisation, we have utilised in silico techniques and the crystal structure for a bacterial cellulose synthase to further understand how these enzymes have evolved distinct functions. Sequence and phylogenetic analyses were performed to determine amino acid conservation, both family-wide and within each sub-family. Further structural analysis centred on comparison of a bacterial curdlan synthase homology model with the bacterial cellulose synthase crystal structure, with molecular dynamics simulations performed with their respective β-glucan products bound in the trans-membrane channel. Key residues that differentially interact with the different β-glucan chains and have sub-family-specific conservation were found to reside at the entrance of the trans-membrane channel. The linkage-specific catalytic activity of these enzymes and hence the type of β-glucan chain built is thus likely determined by the different interactions between the proteins and the first few glucose residues in the channel, which in turn dictates the position of the acceptor glucose. The sequence-function relationships for the bacterial β-glucan synthases pave the way for extending this understanding to other kingdoms, such as plants.
Identifiants
pubmed: 31665152
doi: 10.1371/journal.pone.0224442
pii: PONE-D-19-18555
pmc: PMC6821405
doi:
Substances chimiques
Bacterial Proteins
0
beta-Glucans
0
Glucosyltransferases
EC 2.4.1.-
cellulose synthase
EC 2.4.1.-
1,3-beta-glucan synthase
EC 2.4.1.34
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e0224442Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Mol Microbiol. 2007 Aug;65(4):876-95
pubmed: 17645452
Glycobiology. 1999 Jan;9(1):31-41
pubmed: 9884404
Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W526-31
pubmed: 15215442
Plant Physiol. 2018 Jul;177(3):1124-1141
pubmed: 29780036
Nat Protoc. 2015 Jun;10(6):845-58
pubmed: 25950237
Plant Physiol. 2017 Feb;173(2):970-983
pubmed: 27923988
J Mol Graph. 1996 Feb;14(1):33-8, 27-8
pubmed: 8744570
Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W197-201
pubmed: 18463136
J Comput Chem. 2004 Aug;25(11):1400-15
pubmed: 15185334
Proc Natl Acad Sci U S A. 2013 Apr 30;110(18):7512-7
pubmed: 23592721
J Mol Biol. 1999 Sep 17;292(2):195-202
pubmed: 10493868
J Mol Biol. 1993 Dec 5;234(3):779-815
pubmed: 8254673
Curr Opin Biotechnol. 2018 Feb;49:163-171
pubmed: 28915438
Plant Physiol. 2002 Feb;128(2):336-40
pubmed: 11842136
Glycobiology. 2003 Oct;13(10):693-706
pubmed: 12851288
Plant Cell. 2014 Jul;26(7):2996-3009
pubmed: 25012190
Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21
pubmed: 20057044
Biochemistry. 2012 Feb 14;51(6):1148-59
pubmed: 22217153
Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W244-8
pubmed: 15980461
J Biol Chem. 2006 Oct 13;281(41):30310-4
pubmed: 16920715
BMC Plant Biol. 2017 Jul 10;17(1):119
pubmed: 28693426
Plant Cell. 2008 Mar;20(3):720-38
pubmed: 18349153
Sci Adv. 2015 Jun 12;1(5):e1500069
pubmed: 26601199
J Comput Chem. 2008 Nov 30;29(15):2543-64
pubmed: 18470966
Plant Physiol. 2009 Jan;149(1):27-37
pubmed: 19126692
Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12907-11
pubmed: 7528927
Mol Biol Evol. 2008 Jul;25(7):1307-20
pubmed: 18367465
Nat Methods. 2015 Jan;12(1):7-8
pubmed: 25549265
J Comput Chem. 2005 Dec;26(16):1781-802
pubmed: 16222654
Proc Natl Acad Sci U S A. 2015 Feb 17;112(7):E757-65
pubmed: 25650430
Carbohydr Res. 2010 Feb 26;345(4):474-86
pubmed: 20079487
Annu Rev Biochem. 2010;79:471-505
pubmed: 20235827
Curr Opin Struct Biol. 2015 Oct;34:78-86
pubmed: 26342143
J Phys Chem B. 2015 Jun 4;119(22):6525-35
pubmed: 25942604
Glycoconj J. 2010 May;27(4):461-76
pubmed: 20473714
Science. 2006 Mar 31;311(5769):1940-2
pubmed: 16574868
FEMS Microbiol Rev. 2016 Jan;40(1):133-59
pubmed: 25862689
Proc Natl Acad Sci U S A. 2009 Apr 7;106(14):5996-6001
pubmed: 19321749
Nat Struct Mol Biol. 2014 May;21(5):489-96
pubmed: 24704788
Curr Opin Chem Biol. 2006 Oct;10(5):492-7
pubmed: 16935022
Bioinformatics. 2012 Jun 15;28(12):1647-9
pubmed: 22543367
Nucleic Acids Res. 2016 Jul 8;44(W1):W339-43
pubmed: 27106060
EMBO J. 2007 Dec 12;26(24):5153-66
pubmed: 18034161
Cell. 2012 Jun 22;149(7):1607-21
pubmed: 22579045
Proteins. 2015 Jan;83(1):1-24
pubmed: 25355688
Nature. 2016 Mar 17;531(7594):329-34
pubmed: 26958837
Annu Rev Biochem. 2015;84:895-921
pubmed: 26034894
Biomacromolecules. 2008 Mar;9(3):783-8
pubmed: 18257529
Nature. 2013 Jan 10;493(7431):181-6
pubmed: 23222542
J Exp Bot. 2014 Dec;65(22):6645-53
pubmed: 25262226
Plant Physiol. 2016 Jan;170(1):123-35
pubmed: 26556795
Genome Res. 2004 Jun;14(6):1188-90
pubmed: 15173120
Bioinformatics. 2006 Jan 15;22(2):195-201
pubmed: 16301204
Ann Bot. 2014 Oct;114(6):1349-58
pubmed: 24984713
Nat Genet. 2005 Jan;37(1):73-6
pubmed: 15568024
Trends Microbiol. 2015 Sep;23(9):545-57
pubmed: 26077867
J Comput Chem. 2016 Aug 15;37(22):2098-105
pubmed: 27317625
Plant Physiol. 2007 Apr;143(4):1881-93
pubmed: 17307900
J Biol Chem. 2002 Oct 4;277(40):36931-9
pubmed: 12145282
Biophys J. 2006 Jun 15;90(12):4337-44
pubmed: 16581848
PLoS One. 2011;6(12):e28766
pubmed: 22163331
Proc Natl Acad Sci U S A. 2007 Mar 6;104(10):4112-7
pubmed: 17360486
Proc Natl Acad Sci U S A. 2016 Oct 4;113(40):11360-11365
pubmed: 27647898
J Phys Chem B. 2010 Jun 17;114(23):7830-43
pubmed: 20496934
Annu Rev Plant Biol. 2014;65:69-94
pubmed: 24579997
Sci Rep. 2016 Jun 27;6:28696
pubmed: 27345599
Biochemistry. 2016 Apr 5;55(13):2054-61
pubmed: 26967377
Curr Opin Plant Biol. 2009 Apr;12(2):140-7
pubmed: 19168383
J Mol Biol. 1997 Apr 25;268(1):209-25
pubmed: 9149153
Nat Methods. 2017 Jun;14(6):587-589
pubmed: 28481363
Mol Biol Evol. 2016 Jul;33(7):1870-4
pubmed: 27004904
Nat Protoc. 2012 Jul 19;7(8):1511-22
pubmed: 22814390
Nucleic Acids Res. 2018 Jul 2;46(W1):W368-W373
pubmed: 29718451
Chembiochem. 2015 Sep 7;16(13):1866-1869
pubmed: 26097079
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
J Integr Plant Biol. 2010 Feb;52(2):161-75
pubmed: 20377678
PLoS Biol. 2016 May 03;14(5):e1002452
pubmed: 27138088
Nucleic Acids Res. 2014 Jan;42(Database issue):D490-5
pubmed: 24270786