Abstract
Agrobacterium exopolysaccharides play a major role in the life of the cell. Exopolysaccharides are required for bacterial growth as a biofilm and they protect the bacteria against environmental stresses. Five of the exopolysaccharides made by A. tumefaciens have been characterized extensively with respect to their structure, synthesis, regulation, and role in the life of the bacteria. These are cyclic-β-(1, 2)-glucan, cellulose, curdlan, succinoglycan, and the unipolar polysaccharide (UPP). This chapter describes the structure, synthesis, regulation, and function of these five exopolysaccharides.
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References
Abe K, Nakajima M, Yamashita T et al (2017) Biochemical and structural analyses of a bacterial endo-beta-1,2-glucanase reveal a new glycoside hydrolase family. J Biol Chem 292:7487–7506
Amikam D, Benziman M (1989) Cyclic diguanylic acid and cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 171:6649–6655
Ausmees N, Mayer R, Weinhouse H et al (2001) Genetic data indicate that proteins containing the GGDEF domain possess diguanylate cyclase activity. FEMS Microbiol Lett 204:163–167
Baba T, Ara T, Hasegawa M et al (2006) Construction of Escherichia coli K–12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2:2006
Barnhart DM, Su S, Baccaro BE et al (2013) CelR, an ortholog of the diguanylate cyclase PleD of Caulobacter, regulates cellulose synthesis in Agrobacterium tumefaciens. Appl Environ Microbiol 79:7188–7202
Bash R, Matthysse AG (2002) Attachment to roots and virulence of a chvB mutant of Agrobacterium tumefaciens are temperature sensitive. Mol Plant Microbe Interact 15:160–163
Breedveld MW, Benesi AJ, Marco ML et al (1995) Effect of phosphate limitation on synthesis of periplasmic cyclic (beta)-(1,2)-glucans. Appl Environ Microbiol 61:1045–1053
Breedveld MW, Miller KJ (1994) Cyclic beta-glucans of members of the family Rhizobiaceae. Microbiol Rev 58:145–161
Brightwell G, Hussain H, Tiburtius A et al (1995) Pleiotropic effects of regulatory ros mutants of Agrobacterium radiobacter and their interaction with Fe and glucose. Mol Plant-Microbe Interact 8:747–754
Brown RM Jr, Willison JHM, Richardson CL (1976) Cellulose biosynthesis in Acetobacter xylinum: visualization of the site of synthesis and direct measurement of the in vivo process. Proc Natl Acad Sci USA 73:4565–4569
Cangelosi GA, Hung L, Puvanesarajah V et al (1987) Common loci for Agrobacterium tumefaciens and Rhizobium meliloti exopolysaccharide synthesis and their roles in plant interactions. J Bacteriol 169:2086–2091
Cangelosi GA, Martinetti G, Leigh JA et al (1989) Role for Agrobacterium tumefaciens ChvA protein in export of beta-1,2-glucan. J Bacteriol 171:1609–1615
Castro OA, Zorreguieta A, Ielmini V et al (1996) Cyclic beta-(1,2)-glucan synthesis in Rhizobiaceae: roles of the 319-kilodalton protein intermediate. J Bacteriol 178:6043–6048
Cheng HP, Walker GC (1998) Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI two-component regulatory system. J Bacteriol 180:20–26
Chou AY, Archdeacon J, Kado CI (1998) Agrobacterium transcriptional regulator Ros is a prokaryotic zinc finger protein that regulates the plant oncogene ipt. Proc Natl Acad Sci USA 95:5293–5298
Chouly C, Colquhoun IJ, Jodelet A et al (1995) NMR studies of succinoglycan repeating-unit octasaccharides from Rhizobium meliloti and Agrobacterium radiobacter. Int J Biol Macromol 17:357–363
Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–422
Danhorn T, Hentzer M, Givskov M et al (2004) Phosphorus limitation enhances biofilm formation of the plant pathogen Agrobacterium tumefaciens through the PhoR-PhoB regulatory system. J Bacteriol 186:4492–4501
Douglas CJ, Halperin W, Nester EW (1982) Agrobacterium tumefaciens mutants affected in attachment to plant cells. J Bacteriol 152:1265–1275
Evans LR, Linker A, Impallomeni G (2000) Structure of succinoglycan from an infectious strain of Agrobacterium radiobacter. Int J Biol Macromol 27:319–326
Feirer N, Kim D, Xu J, Fernandez et al (2017) The Agrobacterium tumefaciens CheY-like protein ClaR regulates biofilm formation. Microbiol 163:1680–1691
Feirer N, Xu J, Allen KD et al (2015) A pterin-dependent signaling pathway regulates a dual-function diguanylate cyclase-phosphodiesterase controlling surface attachment in Agrobacterium tumefaciens. MBio 6:e00156
Glucksmann MA, Reuber TL, Walker GC (1993) Genes needed for the modification, polymerization, export, and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J Bacteriol 175:7045–7055
Gonzalez JE, York GM, Walker GC (1996) Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function. Gene 179:141–146
Halder U, Banerjee A, Bandopadhyay R (2017) Structural and functional properties, biosynthesis, and patenting trends of bacterial succinoglycan: a review. Indian J Microbiol 57:278–284
Hawes MC, Pueppke SG (1987) Correlation between binding of Agrobacterium-tumefaciens by root cap cells and susceptibility of plants to crown gall. Plant Cell Rep 6:287–290
Hawes MC, Pueppke SG (1989) Variation in binding and virulence of Agrobacterium tumefaciens chromosomal virulence (Chv) mutant bacteria on different plant-species. Plant Physiol 91:113–118
Heckel BC, Tomlinson AD, Morton ER et al (2014) Agrobacterium tumefaciens exoR controls acid response genes and impacts exopolysaccharide synthesis, horizontal gene transfer, and virulence gene expression. J Bacteriol 196:3221–3233
Heindl JE, Wang Y, Heckel BC et al (2014) Mechanisms and regulation of surface interactions and biofilm formation in Agrobacterium. Front Plant Sci 5:176
Hou CT, Ahlgren JA, Brown W et al (1996) Production of an extracellular polysaccharide by Agrobacterium sp DS3 NRRL B-14297 isolated from soil. J Ind Microbiol 16:129–133
Hussain H, Johnston AW (1997) Iron-dependent transcription of the regulatory gene ros of Agrobacterium radiobacter. Mol Plant Microbe Interact 10:1087–1093
Ingram-Smith C, Miller KJ (1998) Effects of ionic and osmotic strength on the glucosyltransferase of Rhizobium meliloti responsible for cyclic beta-(1,2)-glucan biosynthesis. Appl Environ Microbiol 64:1290–1297
Kamoun S, Cooley MB, Rogowsky PM et al (1989) Two chromosomal loci involved in production of exopolysaccharide in Agrobacterium tumefaciens. J Bacteriol 171:1755–1759
Karnezis T, Epa VC, Stone BA et al (2003) Topological characterization of an inner membrane (1→3)-{beta}-d-glucan (curdlan) synthase from Agrobacterium sp. strain ATCC31749. Glycobiology 13:693–706
Keiski CL, Harwich M, Jain S, Neculai AM et al (2010) AlgK is a TPR-containing protein and the periplasmic component of a novel exopolysaccharide secretin. Structure 18:265–273
Kim MK, Lee IY, Kim KT et al (2000) Residual phosphate concentration under nitrogen-limiting conditions regulates curdlan production in Agrobacterium species. J Ind Microbiol Biotechnol 25:180–183
Kuroda A, Murphy H, Cashel M et al (1997) Guanosine tetra- and pentaphosphate promote accumulation of inorganic polyphosphate in Escherichia coli. J BiolChem 27:21240–21243
Laus MC, Logman TJ, Lamers GE et al (2006) A novel polar surface polysaccharide from Rhizobium leguminosarum binds host plant lectin. Mol Microbiol 59:1704–1713
Li G, Brown PJ, Tang JX et al (2012) Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol Microbiol 83:41–51
Liu Y, Gu Q, Ofosu FK et al (2016) Production, structural characterization and gel forming property of a new exopolysaccharide produced by Agrobacterium HX1126 using glycerol or d-mannitol as substrate. Carbohydr Polym 136:917–922
Marks JR, Lynch TJ, Karlinsey JE et al (1987) Agrobacterium tumefaciens virulence locus pscA is related to the Rhizobium meliloti exoC locus. J Bacteriol 169:5835–5837
Matthysse AG (1983) Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection. J Bacteriol 15:906–915
Matthysse AG (1994) Conditioned medium promotes the attachment of Agrobacterium tumefaciens strain NT1 to carrot cells. Protoplasma 183:131–136
Matthysse AG (2014) Attachment of Agrobacterium to plant surfaces. Front Plant Sci 5:252
Matthysse AG, Holmes KV, Gurlitz RH (1981) Elaboration of cellulose fibrils by Agrobacterium tumefaciens during attachment to carrot cells. J Bacteriol 145:583–595
Matthysse AG, Marry M, Krall L et al (2005) The effect of cellulose overproduction on binding and biofilm formation on roots by Agrobacterium tumefaciens. Mol Plant-Microbe Interact 18:1002–1010
Matthysse AG, McMahan S (1998) Root colonization by Agrobacterium tumefaciens is reduced in cel, attB, attD, and attR mutants. Appl Environ Microbiol 64:2341–2345
Matthysse AG, White S, Lightfoot R (1995) Genes required for cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 177:1069–1075
McIntosh M, Stone BA, Stanisich VA (2005) Curdlan and other bacterial (1→3)-beta-D-glucans. Appl Microbiol Biotechnol 68:163–173
Miller KJ, Kennedy EP, Reinhold VN (1986) Osmotic adaptation by Gram-negative bacteria: possible role for periplasmic oligosaccharides. Science 231:48–51
Molhoj M, Pagant S, Hofte H (2002) Towards understanding the role of membrane-bound endo-{beta}-1,4-glucanases in cellulose biosynthesis. Plant Cell Physiol 43:1399–1406
Morgan JL, McNamara JT, Fischer M et al (2016) Observing cellulose biosynthesis and membrane translocation in crystallo. Nature 531:329–334
Morgan JL, McNamara JT, Zimmer J (2014) Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP. Nat Struct Mol Biol 21:489–496
O’Connell KP, Handelsman J (1989) chvA locus may be involved in export of neutral cyclic beta-1,2-linked d-glucan from Agrobacterium tumefaciens. Mol Plant-Microbe Interact 2:11–16
O’Neill MA, Robison PD, Chou KJ et al (1992) Evidence that the acidic polysaccharide secreted by Agrobacterium radiobacter (ATCC 53271) has a seventeen glycosyl-residue repeating unit. Carbohydr Res 226:131–154
Puvanesarajah V, Schell FM, Stacey G et al (1985) Role for 2-linked-beta-D-glucan in the virulence of Agrobacterium tumefaciens. J Bacteriol 164:102–106
Reuber TL, Walker GC (1993) Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell 74:269–280
Reuhs BL, Kim JS, Matthysse AG (1997) Attachment of Agrobacterium tumefaciens to carrot cells and Arabidopsis wound sites is correlated with the presence of a cell-associated, acidic polysaccharide. J Bacteriol 179:5372–5379
Romling U (2002) Molecular biology of cellulose production in bacteria. Res Microbiol 153:205–212
Ruffing AM, Castro-Melchor M, Hu WS et al (2011) Genome sequence of the curdlan-producing Agrobacterium sp. strain ATCC 31749. J Bacteriol 193:4294–4295
Ruffing AM, Chen RR (2012) Transcriptome profiling of a curdlan-producing Agrobacterium reveals conserved regulatory mechanisms of exopolysaccharide biosynthesis. Microb Cell Fact 11:17
Slabaugh E, Davis JK, Haigler CH et al (2014) Cellulose synthases: new insights from crystallography and modeling. Trends Plant Sci 19:99–106
Spiers AJ, Bohannon J, Gehrig SM et al (2003) Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 50:15–27
Srivatsan A, Wang JD (2008) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11:100–105
Stanisich VA, Stone BA (2009) Enzymology and molecular genetics of biosynthetic enzymes for (1,3)-beta-glucans: prokaryotes. In: Bacic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry, and biology of (1-3)-beta-glucans and related polysaccharides. Elsevier, Amsterdam, pp 201–232
Stasinopoulos SJ, Fisher PR, Stone BA et al (1999) Detection of two loci involved in (1→3)-beta-glucan (curdlan) biosynthesis by Agrobacterium sp. ATCC31749, and comparative sequence analysis of the putative curdlan synthase gene. Glycob 9:31–41
Swart S, Lugtenberg B, Smit G et al (1994) Rhicadhesin-mediated attachment and virulence of an Agrobacterium tumefaciens chvB mutant can be restored by growth in a highly osmotic medium. J Bacteriol 176:3816–3819
Sykes LC, Matthysse AG (1986) Time required for tumor induction by Agrobacterium tumefaciens. Appl Environ Microbiol 52:597–598
Thomashow MF, Karlinsey JE, Marks JR et al (1987) Identification of a new virulence locus in Agrobacterium tumefaciens that affects polysaccharide composition and plant cell attachment. J Bacteriol 169:3209–3216
Tiburtius A, de Luca NG, Hussain H et al (1996) Expression of the exoY gene, required for exopolysaccharide synthesis in Agrobacterium, is activated by the regulatory ros gene. Microbiol 142:2621–2629
Tomlinson AD, Ramey-Hartung B, Day TW et al (2010) Agrobacterium tumefaciens ExoR represses succinoglycan biosynthesis and is required for biofilm formation and motility. Microbiol 156:2670–2681
Uttaro AD, Cangelosi GA, Geremia RA et al (1990) Biochemical characterization of avirulent exoC mutants of Agrobacterium tumefaciens. J Bacteriol 172:1640–1646
Wang D, Xue H, Wang Y et al (2013) The Sinorhizobium meliloti ntrX gene is involved in succinoglycan production, motility, and symbiotic nodulation on alfalfa. Appl Environ Microbiol 79:7150–7159
Wang Y, Kim SH, Natarajan R et al (2016) Spermidine Inversely Influences Surface Interactions and Planktonic Growth in Agrobacterium tumefaciens. J Bacteriol 198:2682–2691
Weiner R, Langille S, Quintero E (1995) Structure, function and immunochemistry of bacterial exopolysaccharides. J Ind Microbiol 15:339–346
Whitney JC, Hay ID, Li C et al (2011) Structural basis for alginate secretion across the bacterial outer membrane. Proc Natl Acad Sci USA 108:13083–13088
Wong HC, Fear AL, Calhoon RD et al (1990) Genetic organization of the cellulose synthase operon in Acetobacter xylinum. Proc Natl Acad Sci USA 87:8130–8134
Wu CF, Lin JS, Shaw GC et al (2012) Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLoS Pathog 8:e1002938
Wu D, Li A, Ma F et al (2016) Genetic control and regulatory mechanisms of succinoglycan and curdlan biosynthesis in genus Agrobacterium. Appl Microbiol Biotechnol 100:6183–6192
Xu J, Kim J, Danhorn T et al (2012) Phosphorus limitation increases attachment in Agrobacterium tumefaciens and reveals a conditional functional redundancy in adhesin biosynthesis. Res Microbiol 163:674–684
Xu J, Kim J, Koestler BJ et al (2013) Genetic analysis of Agrobacterium tumefaciens unipolar polysaccharide production reveals complex integrated control of the motile-to-sessile switch. Mol Microbiol 89:929–948
York GM, Walker GC (1998) The Rhizobium meliloti ExoK and ExsH glycanases specifically depolymerize nascent succinoglycan chains. Proc Natl Acad Sci USA 95:4912–4917
Yu LJ, Wu JR, Zheng ZY et al (2011a) Changes of curdlan biosynthesis and nitrogenous compounds utilization characterized in ntrC mutant of Agrobacterium sp. ATCC 31749. Curr Microbiol 63:60–67
Yu LJ, Wu JR, Zheng ZZ et al (2011b) Changes in gene transcription and protein expression involved in the response of Agrobacterium sp. ATCC 31749 to nitrogen availability during curdlan production. Prikl Biokhim Mikrobiol 47:537–543
Zorreguieta A, Geremia RA, Cavaignac S et al (1988) Identification of the product of an Agrobacterium tumefaciens chromosomal virulence gene. Mol Plant-Microbe Interact 1:121–127
Zorreguieta A, Ugalde RA, Leloir LF (1985) An intermediate in cyclic beta 1-2 glucan biosynthesis. Biochem Biophys Res Commun 126:352–357
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Matthysse, A.G. (2018). Exopolysaccharides of Agrobacterium tumefaciens. In: Gelvin, S. (eds) Agrobacterium Biology. Current Topics in Microbiology and Immunology, vol 418. Springer, Cham. https://doi.org/10.1007/82_2018_100
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DOI: https://doi.org/10.1007/82_2018_100
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