Skip to main content

Exopolysaccharides of Agrobacterium tumefaciens

  • Chapter
  • First Online:
Agrobacterium Biology

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 418))

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.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amikam D, Benziman M (1989) Cyclic diguanylic acid and cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 171:6649–6655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breedveld MW, Miller KJ (1994) Cyclic beta-glucans of members of the family Rhizobiaceae. Microbiol Rev 58:145–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–422

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douglas CJ, Halperin W, Nester EW (1982) Agrobacterium tumefaciens mutants affected in attachment to plant cells. J Bacteriol 152:1265–1275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans LR, Linker A, Impallomeni G (2000) Structure of succinoglycan from an infectious strain of Agrobacterium radiobacter. Int J Biol Macromol 27:319–326

    Article  CAS  PubMed  Google Scholar 

  • Feirer N, Kim D, Xu J, Fernandez et al (2017) The Agrobacterium tumefaciens CheY-like protein ClaR regulates biofilm formation. Microbiol 163:1680–1691

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez JE, York GM, Walker GC (1996) Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function. Gene 179:141–146

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hussain H, Johnston AW (1997) Iron-dependent transcription of the regulatory gene ros of Agrobacterium radiobacter. Mol Plant Microbe Interact 10:1087–1093

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matthysse AG (1983) Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection. J Bacteriol 15:906–915

    Article  Google Scholar 

  • Matthysse AG (1994) Conditioned medium promotes the attachment of Agrobacterium tumefaciens strain NT1 to carrot cells. Protoplasma 183:131–136

    Article  Google Scholar 

  • Matthysse AG (2014) Attachment of Agrobacterium to plant surfaces. Front Plant Sci 5:252

    Article  PubMed  PubMed Central  Google Scholar 

  • Matthysse AG, Holmes KV, Gurlitz RH (1981) Elaboration of cellulose fibrils by Agrobacterium tumefaciens during attachment to carrot cells. J Bacteriol 145:583–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matthysse AG, White S, Lightfoot R (1995) Genes required for cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 177:1069–1075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McIntosh M, Stone BA, Stanisich VA (2005) Curdlan and other bacterial (1→3)-beta-D-glucans. Appl Microbiol Biotechnol 68:163–173

    Article  CAS  PubMed  Google Scholar 

  • Miller KJ, Kennedy EP, Reinhold VN (1986) Osmotic adaptation by Gram-negative bacteria: possible role for periplasmic oligosaccharides. Science 231:48–51

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Morgan JL, McNamara JT, Fischer M et al (2016) Observing cellulose biosynthesis and membrane translocation in crystallo. Nature 531:329–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reuber TL, Walker GC (1993) Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell 74:269–280

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romling U (2002) Molecular biology of cellulose production in bacteria. Res Microbiol 153:205–212

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruffing AM, Chen RR (2012) Transcriptome profiling of a curdlan-producing Agrobacterium reveals conserved regulatory mechanisms of exopolysaccharide biosynthesis. Microb Cell Fact 11:17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slabaugh E, Davis JK, Haigler CH et al (2014) Cellulose synthases: new insights from crystallography and modeling. Trends Plant Sci 19:99–106

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Srivatsan A, Wang JD (2008) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11:100–105

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sykes LC, Matthysse AG (1986) Time required for tumor induction by Agrobacterium tumefaciens. Appl Environ Microbiol 52:597–598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Uttaro AD, Cangelosi GA, Geremia RA et al (1990) Biochemical characterization of avirulent exoC mutants of Agrobacterium tumefaciens. J Bacteriol 172:1640–1646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiner R, Langille S, Quintero E (1995) Structure, function and immunochemistry of bacterial exopolysaccharides. J Ind Microbiol 15:339–346

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zorreguieta A, Ugalde RA, Leloir LF (1985) An intermediate in cyclic beta 1-2 glucan biosynthesis. Biochem Biophys Res Commun 126:352–357

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ann G. Matthysse .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

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

Download citation

Publish with us

Policies and ethics