Abstract
Agrobacterium is a genus of gram-negative bacteria that can produce several typical exopolysaccharides with commercial uses in the food and pharmaceutical fields. In particular, succinoglycan and curdlan, due to their good quality in high yield, have been employed on an industrial scale comparatively early. Exopolysaccharide biosynthesis is a multiple-step process controlled by different functional genes, and various environmental factors cause changes in exopolysaccharide biosynthesis through regulatory mechanisms. In this mini-review, we focus on the genetic control and regulatory mechanisms of succinoglycan and curdlan produced by Agrobacterium. Some key functional genes and regulatory mechanisms for exopolysaccharide biosynthesis are described, possessing a high potential for application in metabolic engineering to modify exopolysaccharide production and physicochemical properties. This review may contribute to the understanding of exopolysaccharide biosynthesis and exopolysaccharide modification by metabolic engineering methods in Agrobacterium.
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References
Aird ELH, Brightwell G, Jones MA, Johnston AWB (1991) Identification of the exo loci required for exopolysaccharide synthesis in Agrobacterium radiobacter NCIB 11883. Microbiology 137(10):2287–2297
Anguillesi A (2003) Molecular biology of curdlan biosynthesis by Agrobacterium sp. ATTC 31749. MSc thesis. La Trobe University, Melbourne
Bae SO, Sugano Y, Ohi K, Shoda M (2004) Features of bacterial cellulose synthesis in a mutant generated by disruption of the diguanylate cyclase 1 gene of Acetobacter xylinum BPR 2001. Appl Microbiol Biotechnol 65(3):315–322
Becker A (2015) Challenges and perspectives in combinatorial assembly of novel exopolysaccharide biosynthesis pathways. Front Microbiol 6
Becker A, Kleickmann A, Keller M, Arnold W, Pühler A (1993) Identification and analysis of the Rhizobium meliloti exoAMONP genes involved in exopolysaccharide biosynthesis and map** of promoters located on the exoHKLAMONP fragment. Mol Gen Genet 241(3–4):367–379
Bertram-Drogatz PA, Quester I, Becker A, Pühler A (1998) The Sinorhizobium meliloti MucR protein, which is essential for the production of high-molecular-weight succinoglycan exopolysaccharide, binds to short DNA regions upstream of exoH and exoY. Mol Gen Genet 257(4):433–441
Boels IC, van Kranenburg R, Hugenholtz J, Kleerebezem M, de Vos WM (2001) Sugar catabolism and its impact on the biosynthesis and engineering of exopolysaccharide production in lactic acid bacteria. Int Dairy J 11(9):723–732
Brightwell G, Hussain H, Tiburtius A, Yeoman KH, Johnston AWB (1995) Pleiotropic effects of regulatory ros mutants of Agrobacterium radiobacter and their interaction with Fe and glucose. Mol Plant-Microbe Interact 8(5):747–754
Cangelosi GA, Hung LYNN, Puvanesarajah V, Stacey G, Ozga DA, Leigh JA, Nester EW (1987) Common loci for Agrobacterium tumefaciens and Rhizobium meliloti exopolysaccharide synthesis and their roles in plant interactions. J Bacteriol 169(5):2086–2091
Close TJ, Tait RC, Kado CI (1985) Regulation of Ti plasmid virulence genes by a chromosomal locus of Agrobacterium tumefaciens. J Bacteriol 164(2):774–781
Donot F, Fontana A, Baccou JC, Schorr-Galindo S (2012) Microbial exopolysaccharides: main examples of synthesis, excretion, genetics and extraction. Carbohydr Polym 2:951–962
Farrand SK, van Berkum PB, Oger P (2003) Agrobacterium is a definable genus of the family Rhizobiaceae. Int J Syst Evol Microbiol 53(5):1681–1687
Freitas F, Alves VD, Reis MA (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol 29(8):388–398
Glucksmann MA, Reuber TL, Walker GC (1993) Genes needed for the modification, polimerization, export and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J Bacteriol 175(21):7045–7055
González JE, Semino CE, Wang LX, Castellano-Torres LE, Walker GC (1998) Biosynthetic control of molecular weight in the polymerization of the octasaccharide subunits of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Proc Natl Acad Sci U S A 95(23):13477–13482
González JE, Marketon MM (2003) Quorum sensing in nitrogen-fixing rhizobia. Microbiol Mol Biol Rev 67(4):574–592
Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, Qurollo B, Slater S (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294(5550):2323–2328
Janczarek M (2011) Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia. Int J Mol Sci 12(11):7898–7933
** LH, Um HJ, Yin CJ, Kim YH, Lee JH (2008) Proteomic analysis of curdlan-producing Agrobacterium sp. in response to pH downshift. J Biotechnol 138(3):80–87
Jofre E, Becker A (2009) Production of succinoglycan polymer in Sinorhizobium meliloti is affected by SMb21506 and requires the N-terminal domain of ExoP. Mol Plant-Microbe Interact 22(12):1656–1668
Hassler RA, Doherty DH (1990) Genetic engineering of polysaccharide structure: production of variants of xanthan gum in Xanthomonas campestris. Biotechnol Prog 6(3):182–187
Heckel BC, Tomlinson AD, Morton ER, Choi JH, Fuqua C (2014) Agrobacterium tumefaciens exoR controls acid response genes and impacts exopolysaccharide synthesis, horizontal gene transfer, and virulence gene expression. J Bacteriol 196(18):3221–3233
Hisamatsu M, Ott I, Amemura A, Harada T, Nakanishi I, Kimura K (1977) Change in ability of Agrobacterium to produce water-soluble and water-insoluble β-glucans. Microbiology 103(2):375–379
Hisamatsu M, Sano K, Amemura A, Harada T (1978) Acidic polysaccharides containing succinic acid in various strains of Agrobacterium. Carbohydr Res 61(1):89–96
Karnezis T, Karnezis T, Epa VC, Stone BA, Stanisich VA (2003) Topological characterization of an inner membrane (1 → 3)-β-D-glucan (curdlan) synthase from Agrobacterium sp. strain ATCC 31749. Glycobiology 13(10):693–706
Kim MK, Lee IY, Ko JH, Rhee YH, Park YH (1999) Higher intracellular levels of uridinemonophosphate under nitrogen-limited conditions enhance metabolic flux of curdlan synthesis in Agrobacterium species. Biotechnol Bioeng 62(3):317–323
Knipper M, Senechal A, Raffar M (1993) Composition deÂrivant d'un succinoglycane, son proceÂde de preÂparation et ses applications. EP 0 527 061 A1
Looijesteijn PJ, Boels IC, Kleerebezem M, Hugenholtz J (1999) Regulation of exopolysaccharide production by Lactococcus lactis subsp. cremoris by the sugar source. Appl Environ Microbiol 65(11):5003–5008
Li A, Geng J, Cui D, Shu C, Zhang S, Yang J, Hu S (2011) Genome sequence of Agrobacterium tumefaciens strain F2, a bioflocculant-producing bacterium. J Bacteriol 193(19):5531–5531
McIntosh M, Stone BA, Stanisich VA (2005) Curdlan and other bacterial (1 → 3)-β-D-glucans. Appl Microbiol Biotechnol 68(2):163–173
Müller P, Keller M, Weng WM, Quandt J, Arnold W, Pühler A (1992) Genetic analysis of the Rhizobium meliloti exoYFQ operon: ExoY is homologous to sugar transferases and ExoQ represents a transmembrane protein. Mol Plant-Microbe Interact 6(1):55–65
Nampoothiri KM, Singhania RR, Sabarinath C, Pandey A (2003) Fermentative production of gellan using Sphingomonas paucimobilis. Process Biochem 38(11):1513–1519
Ortiz Martinez C, Pereira Ruiz S, Carvalho Fenelon V, Rodrigues de Morais, G, Luciano Baesso, M, Matioli, G (2015) Characterization of curdlan produced by Agrobacterium sp. IFO 13140 cells immobilized in a loofa sponge matrix, and application of this biopolymer in the development of functional yogurt. J Sci Food Agric
Romling U, Gomelsky M, Galperin MY (2005) C-di-GMP: the dawning of a novel bacterial signaling system. Mol Microbiol 57(3):629–639
Ruffing AM, Castro-Melchor M, Hu WS, Chen RR (2011) Genome sequence of the curdlan-producing Agrobacterium sp. strain ATCC 31749. J Bacteriol 193(16):4294–4295
Ruffing AM, Chen RR (2012) Transcriptome profiling of a curdlan-producing Agrobacterium reveals conserved regulatory mechanisms of exopolysaccharide biosynthesis. Microb Cell Factories 11(1):1–13
Saxena IM, Brown RM Jr, Fevre M, Geremia RA, Henrissat B (1995) Multidomain architecture of β-glycosyl transferases: implications for mechanism of action. J Bacteriol 177(6):1419–1424
Schmid J, Sieber V, Rehm B (2015) Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol 6
Shrout JD, Nerenberg R (2012) Monitoring bacterial twitter: does quorum sensing determine the behavior of water and wastewater treatment biofilms? Environ Sci Technol 46(4):1995–2005
Skorupska A, Janczarek M, Marczak M, Mazur A, Król J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Factories 5(1):7
Stasinopoulos SJ, Fisher PR, Stone BA, Stanisich VA (1999) Detection of two loci involved in (1 → 3)-β-glucan (curdlan) biosynthesis by Agrobacterium sp. ATCC31749, and comparative sequence analysis of the putative curdlan synthase gene. Glycobiology 9(1):31–41
Stredansky M, Conti E, Bertocchi C, Navarini L, Matulova M, Zanetti F (1999) Fed-batch production and simple isolation of succinoglycan from Agrobacterium tumefaciens. Biotechnol Tech 13(1):7–10
Sutherland IW (1985) Biosynthesis and composition of gram-negative bacterial extracellular and wall polysaccharides. Annu Rev Microbiol 39(1):243–270
Tiburtius A, de Luca NG, Hussain H, Johnston AW (1996) Expression of the exoY gene, required for exopolysaccharide synthesis in Agrobacterium, is activated by the regulatory ros gene. Microbiology 142(9):2621–2629
Tomlinson AD, Ramey-Hartung B, Day TW, Merritt PM, Fuqua C (2010) Agrobacterium tumefaciens ExoR represses succinoglycan biosynthesis and is required for biofilm formation and motility. Microbiology 156(9):2670–2681
Uttaro AD, Cangelosi GA, Geremia RA, Nester EW, Ugalde RA (1990) Biochemical characterization of avirulent exoC mutants of Agrobacterium tumefaciens. J Bacteriol 172(3):1640–1646
Uttaro AD, Ielpi L, Ugalde RA (1993) Galactose metabolism in Rhizobiaceae: characterization of Agrobacterium tumefaciens exoB mutants. Microbiology 139(5):1055–1062
van Kranenburg R, Marugg JD, van Swam II, Willem NJ, de Vos WM (1997) Molecular characterization of the plasmid encoded eps gene cluster essential for exopolysaccharide biosynthesis in Lactococcus lactis. Mol Microbiol 24(2):387–397
van Kranenburg R, van Swam I, Marugg JD, Kleerebezem M, de Vos WM (1999a) Exopolysaccharide biosynthesis of the glycosyltransferase genes involved in synthesis of the polysaccharide backbone. J Bacteriol 181(1):338–340
Whitehead NA, Barnard AM, Slater H, Simpson N, Salmond GP (2001) Quorum-sensing in gram-negative bacteria. FEMS Microbiol Rev 25(4):365–404
Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, Okura VK, Olson MV (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294(5550):2317–2323
Wu D, Li A, Yang JX, Ma F, Chen H, Pi SS, Wei W (2015) N-3-oxo-octanoyl-homoserine lactone as a promotor to improve the microbial flocculant production by an exopolysaccharide bioflocculant-producing bacterium Agrobacterium tumefaciens F2. RSC Adv 5(109):89531–89538
Wu JR, Yu LJ, Zhan XB, Zheng ZY, Lu J, Lin CC (2012) NtrC-dependent regulatory network for curdlan biosynthesis in response to nitrogen limitation in Agrobacterium sp. ATCC 31749. Process Biochem 47(11):1552–1558
Yang JX, Wu D, Li A, Guo HJ, Chen H, Pi SS, Ma F (2016) The addition of N-hexanoyl-homoserine lactone to improve the microbial flocculant production of Agrobacterium tumefaciens strain F2, an exopolysaccharide bioflocculant-producing bacterium. Appl Biochem Biotechnol. doi:10.1007/s12010-016-2027-6
Young JM, Kuykendall LD, Martinez-Romero E, Kerr A, Sawada H (2003) Classification and nomenclature of Agrobacterium and Rhizobium—a reply to Farrand et al. (2003). Int J Syst Evol Microbiol 53(5):1689–1695
Yuan ZC, Liu P, Saenkham P, Kerr K, Nester EW (2008) Transcriptome profiling and functional analysis of Agrobacterium tumefaciens reveals a general conserved response to acidic conditions (pH 5.5) and a complex acid-mediated signaling involved in Agrobacterium-plant interactions. J Bacteriol 190(2):494–507
Yu L, Wu J, Liu J, Zhan X, Zheng Z, Lin CC (2011a) Enhanced curdlan production in Agrobacterium sp. ATCC 31749 by addition of low-polyphosphates. Biotechnol Bioprocess Eng 16(1):34–41
Yu LJ, Wu JR, Zheng ZZ, Lin CC, Zhan XB (2011b) Changes in gene transcription and protein expression involved in the response of Agrobacterium sp. ATCC 31749 to nitrogen availability during curdlan production. Appl Biochem Microbiol 47(5):487–493
Yu XQ, Zhang C, Yang LP, Zhao LM, Lin C, Liu ZJ, Mao ZC (2015) CrdR function in a curdlan-producing Agrobacterium sp. ATCC31749 strain. BMC Microbiol 15:25
Zhan XB, Lin CC, Zhang HT (2012) Recent advances in curdlan biosynthesis, biotechnological production, and applications. Appl Microbiol Biotechnol 93(2):525–531
Zhang HT, Zhan XB, Zheng ZY, Wu JR, Yu XB, Jiang Y, Lin CC (2011) Sequence and transcriptional analysis of the genes responsible for curdlan biosynthesis in Agrobacterium sp. ATCC31749 under simulated dissolved oxygen gradients conditions. Appl Microbiol Biotechnol 91(1):163–175
Zhang HT, Zhan XB, Zheng ZY, Wu JR, English N, Yu XB, Lin CC (2012) Improved curdlan fermentation process based on optimization of dissolved oxygen combined with pH control and metabolic characterization of Agrobacterium sp. ATCC 31749. Appl Microbiol Biotechnol 93(1):367–379
Zheng ZY, Lee JW, Zhan XB, Shi Z, Wang L, Zhu L, Wu JR, Lin CC (2007) Effect of metabolic structures and energy requirements on curdlan production by Alcaligenes faecalis. Biotechnol Bioprocess Eng 12(4):359–365
Zhu J, Beaber JW, More MI, Fuqua C, Eberhard A, Winans SC (1998) Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens. J Bacteriol 180(20):5398–5405
Acknowledgments
This work was supported by grants from the National Natural Science Foundation of China (No. 51578179), the Fundamental Research Funds for the Central Universities (No. HIT. NSRIF. 2015095) and the Postdoctoral Scientific Research Development Fund of Heilongjiang Province in 2014 (No. LBH-Q14076).
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Wu, D., Li, A., Ma, F. et al. Genetic control and regulatory mechanisms of succinoglycan and curdlan biosynthesis in genus Agrobacterium . Appl Microbiol Biotechnol 100, 6183–6192 (2016). https://doi.org/10.1007/s00253-016-7650-1
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DOI: https://doi.org/10.1007/s00253-016-7650-1