Abstract

The symbiotic diazotrophs comprise with a very diverse group of Gram negative soil bacteria, collectively called as rhizobia found in nodule of legume plant. Rhizobia adopt themselves in different environment including soil, rhizosphere and grown within legume roots, where they fix nitrogen. The establishment of symbiosis is a very complicated process involving a coordinated exchange of signal between legume plants and the symbionts. The nodule development requires synthesis of signal molecules such as Nod factors that are important for induction of nodule development. There are different types of surface polysaccharides such as lipopolysaccharides, capsular polysaccharides, neutral and acidic polysaccharides found in rhizobia. The production of symbiotically active polysaccharides may allow rhizobial strains to adapt themselves to changing environmental conditions and interact efficiently with legume plants. Despite extensive research, the actual molecular function of the surface polysaccharides of rhizobia in symbiosis remains unclear. This review emphasized on the structural composition of extracellular polysaccharide of different rhizobia isolated from different legume plants. The compositions of extracellular polysaccharides are different in different rhizobia. The various compositions of extracellular polysaccharides produced by the symbionts are considered as the signaling molecules essential for determining host plant specificity. The present status of the biological functions of the exo-polysaccharide in symbiosis such as host specificity, successful invasion, formation of infection thread and induction of nodule formation in legume plants is also summarized here.

Abbreviations

EPS , extracellular polysaccharide ; CPS , capsular polysaccharide ; LPS , lipopolysaccharides ; CG , cyclic beta glucan ; KPS , K-antigen polysaccharide ; NP , neutral polysaccharide

Keywords

Rhizobium spp. ; Extracellular polysaccharide ; Production ; Composition ; Succinoglycan ; Galactoglucan

Introduction

Polysaccharide is the most abundant organic macromolecules in nature. The biosyntheses of polysaccharide are found in different organisms ranging from bacteria to eukarya, including plants. Gram negative soil bacteria belonging to (α and β-proteobacteria) have the ability to produce root nodule by symbiosis with legume plants (Skorupska et al., 2006 ). This interaction is initiated by the exchange of signal by diverse molecules between the two partners. Among them, plants liberate flavonoids into the rhizospheric region that upregulate rhizobial genes responsible for nodule formation (Spaink, 2000  ;  Schulze et al ., 1998 ). Recognition of the symbiont is made possible through the exchange of nod factor perception and Ca2 + /calmodulin-dependent protein signaling (Geurts and Bisseling, 2002  ;  Oldroyd and Downie, 2004 ). The establishment of successful symbiosis in legume plant was made by the production of nod factor signal and exposure of the correct surface and/or extracellular polysaccharide.

This signal exchange between the two partners seems to work at a distance in the rhizosphere and before binding of rhizobial symbiont to the host root hairs, to induce morphogenetic changes in plant roots. These signal molecules, the Nod factors, are sufficient for initiation of root hair changes, bacterial cell entry for infection, thread formation and activation of cortical cell division Schulze et al. (1998) to generate the nodule primordium (Nod) (Kijne, 1992 ). Rhizobia colonize with plant root hairs, develops infection, the bacteria multiply to form infection thread. In this thread the bacteria encircled by the peribacteroid membrane of plant origin that differentiate into bacteroids (Fisher and Long, 1992 ).

Bacteroids were found to fix nitrogen by synthesizing the nitrogenase enzyme and other proteins. In return, plant supplies carbohydrates to bacteria as a source of carbon and energy. The establishment of symbiosis is stringently controlled through a complex network of signaling cascades Schulze et al. (1998) . This process is partner specific and signifies that the rhizobial species can only nodulate a limited but defined range of legume plants.

The key factors for the interaction are a number of rhizobial genes which are responsible for production of different types of cell-surface polysaccharides such as capsular polysaccharide (CPS) that form as adherent cohesive layer on the cell surface. However, the term exopolysaccharides (EPS) is used for polysaccharides with little or no cell association (Becker and Pühler, 1998 ). Cyclic beta-(1-2)-glucan is concentrated in periplasmic space of rhizobia, which plays an important role in osmotic adaptation of bacteria Breedveld et al. (1993) . Lipopolysaccharides (LPS) are anchored in outer membrane and consist of lipid A, a core polysaccharide and repeating O-side antigen polysaccharides. Despite extensive research, the precise role of surface polysaccharides in symbiosis remains unclear. So the role of rhizobial polysaccharide has been the goal of many studies.

The present review describes the production and structure of different exopolysaccharides of rhizobia isolated from legume root nodule. Attempts were also made to discuss the possible role of the exopolysaccharide in legume — rhizobia symbiosis and nodule formation.

Structural Features of Rhizobial Exopolysaccharides

Rhizobial cell produces different types of surface polysaccharides into environment or retained at the cell surface. They comprise extracellular polysaccharide (EPS), lipopolysaccharide (LPS), capsular polysaccharide (CPS), cyclic beta glucan (CG), K-antigen polysaccharide (KPS), neutral polysaccharide (NP), gel-forming-polysaccharide (GPS), and cellulose fibrils. They are species as well as strain-specific heteropolymers and consisting of repeating units containing mainly common monosaccharides (d -glucose, d -mannose, d -galactose, l -rhamnose, d -glucuronic and d -galacturonic acids) (Table 1 ). A large diversity in EPS chemical structures can be found among rhizobia, concerning sugar composition, linkage of subunit, repeating unit size and degree of polymerization as well as non-carbohydrate decoration (Table 1 ) (Laus et al ., 2005  ; Skorupska et al ., 2006  ; Downie, 2010  ;  Janczarek, 2011 ). EPS are mainly two types, succinoglycan (EPS I) and galactoglucan (EPS II) produced by several rhizobial strains (Reinhold et al., 1994 ) (Fig. 1 ). EPS-I composed of octasaccharide repeating units containing one galactose and seven glucose residues (in molar ratio 1:7), joined by β-1,3; β-1,4 and β-1,6 glycosidic linkages whereas EPS II is a polymer of disaccharide repeating unit and joined by α-1,3 and β-1,3 glycosidic bonds (Her et al ., 1990  ;  Zevenhuizen, 1997 ).

Table 1. Different linkage and composition of monomers in EPS produced by Rhizobium spp.
Name of rhizobia EPS structure Monomer composition (%) Reference
R. leguminosarum 128c53 → 4Glc → α4GlcA → β4GlcA → β4Glc → β6Glc ← β4Glc ← βGlc ← βGlc(4–6)Pyr  ← β3Gla(4–6)Pyr Galactosyl, glucosyl, glucuronosyl and pyruvyl Robertson et al. (1981)
R. leguminosarum 128c63 → 4Glc → α4GlcA → β4GlcA → β4Glc → β6Glc ← β4Glc ← βGlc ← βGlc(4–6)Pyr  ← β3Gla(4–6)Pyr Galactosyl, glucosyl, glucuronosyl and pyruvyl
R. trifolii NA30 → 4Glc → α4GlcA → β4GlcA → β4Glc → β6Glc ← β4Glc ← βGlc ← βGlc(4–6)Pyr  ← β3Gla(4–6)Pyr Galactosyl, glucosyl, glucuronosyl and pyruvyl
R. trifolii 0403 → 4Glc → α4GlcA → β4GlcA → β4Glc → β6Glc ← β4Glc ← βGlc ← βGlc(4–6)Pyr ← β3Gla(4–6)Pyr Galactosyl, glucosyl, glucuronosyl and pyruvyl
R. leguminosarum bv. trifolii 4S β-Glc-(1 → 3)-β-Glc-(1 → 4)-β-Glc(1 → 6)β → (4,6)-C-CH3 -CO2 H Galactosyl, glucosyl, glucuronosyl and pyruvyl Amemura et al. (1983)
R. trifolii 0403 ND Glucose:galactose:glucuronic acid = 5:1:0.9 Mikini et al. (1984)
R. meliloti SU47 4,6-O-(1-carboxyethylidene)-α-d -Galp 1 → 3(X-O-Ac)-β-d -Glcp 1 → 3 1,3,5-tri-O-acetyl-2,4,6-tri-o-methylglucitol and penta-o-acetyl-2-mono-o-ethylgalactitol galactose pyruvate ketal group, Zhan et al. (1991)
R. trifolii TA-1 Cyclic β-(1,2)-glucans Glucans Breedveld et al. (1990)
Rhizobium sp. NGR234 β-Glc-(1-6)-β-Glc(1-6)-β-(1-4)-β-Glc(1-4)-β(1-3)-βGal(1)-β(1-4)-GlcA(1-3)α-GlcA(1-4)α-(4-6) PyrGal-2,3-o-actyl Galactosyl, glucosyl, glucuronosyl and pyruvyl
R. meliloti β-4Glc(1-4)-β-Glc(1-4)-β-Glc(1-3)-β–Gal(1-6)-β-Glc(1-6)-β-Glc(1-3)-β-Glc(1-3)-Glc-(4-6)Pyr Galactosyl, glucosyl, glucuronosyl and pyruvyl Zhan et al. (1990)
S. meliloti RM 1021 EPS II → 3Gal → α(1,3)Glc-β(1,6)OAc → (4,6)-C-CH3 -CO2 H Galactose and glucose Her et al. (1990)
R. leguminosarum bv. viciae 248 β-Gla-(1 → 3)-β-Glc-(1 → 3)-β-Glc(1 → 3)β-GlcA-(1 → 4)-β-Glc(1 → 6)-β → [(4,6)-C-CH3 -CO2 H]2 Galactose, glucose and glucuronosyl Canter-Cremers et al. (1991)
R. leguminosarum biovar trifoli TA-1 Cyclic β-(1,2)-glucans Glucans Breedveld et al. (1992)
S. fredii USDA205 [(→ 3)-α-d -Galp-(1 → 5)-α-d -Kdop-(2 →)]n, [− 2-O-MeManp → β-Kdo–]n Xylose, mannose, glucose and Kdo in a molar ratio of 1:1:1:5. Reuhs et al. (1993)
S. fredii USDA257 [(→ 3)-β-d -Manp-(1 → 5)-β-d -Kdop(2 →)]n, [(→ 3)-β-d -2-O-MeManp-(1 → 5)-β-d -Kdop-[2 →]]n Xylose, mannose, glucose and Kdo in a molar ratio of 1:1:1:5.
S. meliloti RM 1021 EPS I → 4Glcβ → 6GlcOAc → β(1,4)Glc → β(1,3)Gal-β → 4Glcβ(1,6) ← βGlc(1,3) ← βGlc6-OSucc ← β(1,3)Glc(4,6)c-CO2 H-CH3 Succinoglycan with glycosidic linkage Reinhold et al. (1994)
Rhizobium sp. ND Mannose:galactose:glucose 5.79:19.69:74.52 De and Basu (1996)
S. meliloti AK631 [− β-GlcA → Pse5N(β-OH-But)7NAc–]n Kdo(3-deoxy-d -manno-octulosonic acid) Campbell et al. (1998)
S. meliloti NGR185 [− β-GlcNAc → β-Kdo–]n Glucosyl and Kdo Reuhs et al. (1998)
S. fredii USDA208 [− α-Gal → β-Kdo–]n Galactosyl and Kdo
S. fredii USDA201 [− α-Gal → β-Kdo → α-2-O-MeHex → β-Kdo–]n Galactosyl and Kdo (2-metho-hexo)
Sinorhizobium sp. NGR234 [− β-Glc → α-Pse5NAc7NAc–]n Glucosyl
S. fredii HH303 [Rha, GalA]n Rhamnose with glucuronosyl
S. fredii HH103 [− 7(3OH Bu)-Pse–]n 5-acetamido-3,5,7,9-tetradeoxy-7-[(R )-and (S )-3-hydroxybutyramido]-l-glycero -l-manno -nonulosonic acid = 3:1 Gil-Serrano et al. (1999)
S. meliloti − 4Glc,β-1,4-Glcβ-1,4Glcβ-1,3Galβ-1Glcβ-1,3-Glcβ-1,3-Glcβ-1,6-Glcβ-1,6-(side chain) Galactose and reducing glucose Wang et al. (1999)
Rhizobium sp. ND Arabinose:xylose:rhamnose = 11.73:23.68:64.59 Datta and Basu (1999)
Rhizobium sp. ND Arabinose:xylose:rhamnose = 14.7:23.6:61.7
Rhizobium sp. ND Arabinose:xylose:rhamnose = 12.0:23.8:64.2
B. japonicum 2143 ND Man:Glu:Gal:GalA = 1: 2: 1: 1 Karr et al. (2000)
Rhizobium sp. TAL1145 ND Glucose:galactose = 2:1 Kaufusi et al. (2004)
Rhizobium sp. ND Arabinose:galactose:glucose:rhamnose:xylose 1.47:4.62:6.30:26.90:60.71 Ghosh et al. (2005)
Rhizobium sp. strain KYGT207 (→ 4)-β-ManAp- (1 → 4)-β-Glcp -(1 → 4)-βGalp -(1 → 3 → 1) β-Glcp Glucose:galactose:mannuronic acid = 2:1:1 Kaci et al. (2005)
S. meliloti RM1021 ND Galactose:Glucose = 1:7 Luciana et al. (2010)
R. leguminosarum bv. trifolii Rt24.2 ND Glucose:glucuronic acid:galactose = 4.8:1.8:1.0 Janczarek (2011)
Rhizobium sp. strain PM25 ND Xylose:arabinose:mannose 0.1:0.8:99.1 Ghosh et al. (2011)
Rhizobium sp. ND Glucose and galactose Mukherjee et al. (2011)
R. sullae Cyclic-(1, 2)-glucans Glucose, galactose and fucose Gharzouli et al. (2013)
R. undicola strain N37 ND Galactose:mannose = 94.17:5.83 Ghosh et al. (2015)


Fig. 1


Fig. 1.

Chemical structure of rhizobial exopolysaccharides (EPS) (based on Skorupska et al ., 2006  ; Downie, 2010  ;  Janczarek, 2011 and Janczarek et al., 2014 review works). Abbreviations: Glc = glucose, GlcA = glucuronic acid, Gal = galactose, Succ = succinate and Ac = acetyl.

Single repeating unit is decorated by different non-carbohydrate such as acetyl, pyruvyl and succinyl groups. Both EPS I and II are secreted in two major fractions — High Molecular Weight (HMW) consisting of hundreds to thousands of repeating units and Low Molecular Weight (LMW) that represents monomers, dimers and trimers in a case of EPS I and oligomers (15–20) in the case of EPS II (Gonzalez et al ., 1996  ; Gonzalez et al ., 1998  ;  Wang et al ., 1999 ). The pattern of non-carbohydrate modifications of EPS may be different in various strains of the same species and depend on the phase of bacterial growth and culture medium. Non-carbohydrate modifications located in the side chain of the EPS units proved to be very important for the signaling properties of EPS in the symbiosis (Ivashina and Ksenzenko, 2012  ;  Janczarek et al ., 2014 ).

Production of Exopolysaccharides in Culture by Rhizobia

Rhizobium spp. are able to produce large amount of EPS in culture rather than EPS produced in symbiotic condition ( Table 2 ). The growth environment was very important for maximum exopolysaccharide production (Sutherland, 1972 ). Utilization of different carbon sources for the growth and EPS production by Rhizobium sp. was reported earlier ( Stowers, 1985  ;  Breedveld et al ., 1993 ). However, carbon source in medium was a determining factor for the amount of EPS produced by R. tropici CIAT899 ( Staudt et al., 2012 ). Different carbon sources supplemented at 1% level promoted the bacterial growth and EPS production by a Rhizobium sp. to different extent and mannitol was the most effective promoter. Higher concentrations of polysaccharides were obtained when carbon:nitrogen ratio was higher in medium ( Breedveld et al., 1993 ). Sulfate was less preferred nitrogen source for most of nitrogen sources for some strain of Rhizobium , whereas nitrate, glycine and ammonium conjugate were most preferred as nitrogen source ( Ghosh et al., 2005 ). Mandal et al. (2007) have reported l -asparagine increased both growth and production by Rhizobium sp. VMA301 from V. mungo (L.) Hepper. Various studies have found that EPS production is favored under conditions of nitrogen limitation ( Doherty et al ., 1988  ;  Dudman, 1964 ). Under such nitrogen-limited conditions, any excess sugars remaining can be used specifically for polysaccharide synthesis (Kucuk and Kivanc, 2009 ). However, thiamine hydrochloride and nicotinic acid increased EPS production by different species of Rhizobium were observed Amemura et al ., 1983  ;  Ghosh et al ., 2011 . Varied degrees of promotion of growth by isolates in the presence of vitamins might be due to differential requirement of vitamins as cofactors. Watson et al. (2001) stated that biotin might be involved as metabolic regulator in rhizobial growth.

Table 2. EPS producing Rhizobium spp. strains reported in optimal condition by culture in different media.
Symbiont isolated from legume plants Max EPS (g/L) C-source (%) EPS/carbon (g/g) N-source C/N ratio Composition of EPS Reference
R. leguminosarum bv. Trifolii TA-1 2.7 Mannitol (1%) 1.13 Glutamic acid 5 Glucans Breedveld et al. (1993)
Rhizobium sp. 1.76 Mannitol (2%) 0.88 Potassium nitrate 20 Mannose, galactose and glucose De and Basu (1996)
Rhizobium sp. T1 1.5a Sucrose (1%) 1.5b Ammonium acetate 10 Glucose and glucuronic acid Guentas et al. (2000)
Rhizobium sp. D1 10 1.89 Mannitol (2%) 0.95 Potassium nitrate 20 Xylose, rhamnose, glucose, galactose and arabinose Ghosh et al. (2005)
Rhizobium sp. KYGT207 2.5a Sucrose (2%) 1.25b ND ND Glucose, galactose and mannuronic acid Kaci et al. (2005)
Rhizobium sp. VMA301 0.35 Mannitol (1%) + asparagine (0.3%) 0.27 l -asparagine 3.3 Ribose and mannose Mandal et al. (2007)
Rhizobium sp. 1.182 Mannitol (1%) 1.18 Sodium nitrate 11.8 ND Kucuk and Kivanc (2009)
Rhizobium sp. 0.966 Mannitol ND ND ND ND Kumari et al. (2009)
Rhizobium sp. PM25 0.596 Sucrose (1.5%) 0.39 Glycine 15 Xylose, arabinose and mannose Ghosh et al. (2011)
Rhizobium sp. 0.116 Glucose (2%) 0.058 Glycine 20 Glucose and galactose Mukherjee et al. (2011)
Rhizobium sp. 2.47 Sucrose (1%) 2.47 Ammonium sulfate 10 Glucose and maltose Sayyed et al. (2011)
R. tropici CIAT899 4.08 Sucrose (2%) 2.04 Ammonium nitrogen 20 Glucose, galactose, rhamnose and xylose Staudt et al. (2012)
R. sullae 2.92 ND ND ND ND Glucose, galactose and fructose Razika et al. (2012)
R. radiobacter S10 2.834 ND ND ND ND Galactose, glucose, glucosamine, mannose Zhou et al. (2014)
R. undicola strain N37 0.515 Mannitol (0.4%) 1.28 Potassium nitrate 2 Galacotse and mannose Ghosh et al. (2015)
R. tropici Semia 4077 7.45 ND ND ND ND Mannose, rhamnose, glucuronic acid, galacturonic acid, glucose, galactose Castellane et al. (2015)
Rhizobium sp. LBMP-C04 6.63 ND ND ND ND Rhamnose, glucose, galactose, mannose, glucuronic acid, galacturonic acid Moretto et al. (2015)
Rhizobium sp. PRIM-18 2.1 ND ND ND ND ND Priyanka et al. (2015)

a. Ethanol-precipitated material from supernatant.

b. Ethanol precipitated material/carbon, ND = not detected.

EPS production also varies with time, as a function of growth phase, for many bacteria. For many rhizobacterial species, growth and exopolysaccharide production occur simultaneously, because EPS biosynthesis being growth-associated (Datta and Basu, 1999  ;  Ghosh et al ., 2005 ). Several studies have indicated that the EPS yields vary with bacterial growth phase, while EPS composition remains constant through the batch cycle of growth (Breedveld et al ., 1993  ;  Ghosh et al ., 2015 ).

In regards to oxygen availability, the agitation rate controls both bacterial growth and EPS production. Bacterial growth (in biomass) tends to be increase with higher agitation rates, under conditions where oxygen limitation is not imposed. However, the impact of agitation on EPS production is unclear. Studies by Dudman (1964) and Kucuk and Kivanc (2009) indicate that EPS production is optimal under conditions of low agitation. However, others have indicated that polysaccharide production is maximized under conditions of high aeration, when oxygen limitation is not imposed (Duta et al., 2006 ).

Both bacterial growth and rates of EPS production are dependent upon the pH of the growth medium (Martinez-Romero et al ., 1991  ;  Staudt et al ., 2012 ). High level of pH resulted dramatic decrease in EPS production, particularly in the acidic range (Kucuk and Kivanc, 2009  ;  Staudt et al ., 2012 ) whereas optimum EPS production was reported at slight alkaline pH value of 8.0 (Sayyed et al., 2011 ). The role of bacterial growth temperature in EPS production is variable. EPS production is often favored by suboptimal temperature Sutherland (1972) . However, other studies found maximum EPS production occurring at optimal temperature conditions by rhizobia (Sayyed et al ., 2011  ;  Ghosh et al ., 2015 ).

Functions of Rhizobial Exopolysaccharide in Symbiosis

Several possible biological functions of rhizobial EPS are suggested by different workers (Fig. 2 ). These includes role in protecting bacteria against environmental stresses, initial attachment of bacteria to the roots, involvement in stage of infection, structural role in the infection thread formation, release of bacteria from the infection threads, bacteroid development, suppression of plant defense responses and protection against plant antimicrobial compounds (Becker and Pühler, 1998  ;  Fraysse et al ., 2003 ).


Fig. 2


Fig. 2.

Different types of function related to rhizobial EPS production.

The primary attachment is established by recognition of root-hair lectins by the surface carbohydrates of rhizobial cell Dazzo et al. (1984) . EPS may enhance the chance of adhesion of bacteria to the tip of growing root hairs. However, EPS-deficient mutants are not significantly affected in adhesion to the roots of several species such as clover (Rolfe et al., 1996 ), vetch (Van Workum et al., 1998 ) or alfalfa (Cheng and Walker, 1998 ). The surface proteins rhicadhesins could also play an important role in the initial attachment (Smit et al., 1992 ) and involvement of cellulose fibrils is suggested in this process (Laus et al., 2005 ). After initial attachment of R. leguminosarum to root hairs, bacteria aggregate around the root hair surface in a cap or a biofilm formation which requires cellulose fibrils ( Laus et al ., 2005  ;  Williams et al ., 2008 ). Rhizobial strain produce EPS in large amount were characterized by biofilm formation that enhanced bacterial cell to better adaptation inside the host roots (Fujishige et al., 2006 ).

The low molecular mass of EPS in Sinorhizobium meliloti Rm1021 has been studied to know the structural requirement of EPS for an effective nodulation ( Gonzalez et al., 1996 ). Normally, this strain requires the presence of a succinoglycan to efficiently infect Medicago sativa root hairs Reinhold et al. (1994) . The importance of this polysaccharide in the symbiosis was confirmed in several non-EPS producing strains of Sinorhizobium meliloti and Rhizobium leguminosarum bvs. trifolii and viciae , which were symbiotically defective due to induction of empty or almost uninfected nodules on the respective host plants, being a result of aborted infection thread elongation within the peripheral cells of the developing nodule ( Ivashina and Ksenzenko, 2012 ).

The most important among the suggested EPS functions is its role as a signaling molecule. Rhizobial lipochitin oligosaccharides (Nod factors), bacterial cell-surface components and low-molecular weight metabolites are engaged in the signaling. The EPS of Mesorhizobium loti played a signaling role in symbiosis with Lotus plants forming determinate type of nodules Kelly et al. (2013) . Although several studies about rhizobial EPS and its precise function as a signal molecule in the symbiosis have not yet been clearly established (Janczarek et al., 2014 ).

Moreover, EPS is especially important in symbioses with legumes that form indeterminate-type nodules, where long infection threads are formed, as a compound indispensable for initiation and propagation of infection threads, bacterial release from the infection threads and development of bacteroids (Brewin, 2004 ; Skorupska et al ., 2006  ;  Ivashina and Ksenzenko, 2012 ). The acidic EPS essential for the development of an indeterminate type of nodules: Sinorhizobium meliloti /alfalfa , Rhizobium leguminosarum bv. Viciae /Vicia sativa and bv. Trifoli /trifolium ssp. NGR234/Leucaena ( Breedveld et al ., 1993  ;  Djordjevic et al ., 1987 ).

Besides, there are several ways that plant pathogenic and symbiotic bacteria used to avoid plant defense system and to protect themselves (D'Haeze et al., 2004 ). The rhizobial surface polysaccharides and glucan play important roles in protection against the host defense (D'Haeze et al., 2004 ). It is suggested that EPS might be act by suppressing bacterial antigens at the stage of nodule cell infection (Wielbo et al., 2004 ). Recently Ciesla et al. (2016) reported that EPS plays an essential role in electrophoretic mobility of rhizobial cells and their higher amounts depend on mobility as well as its acidic nature of the bacterial cell surface.

Conclusion

Extracellular polysaccharides (EPS) are species-specific complex polymers of different carbohydrate unit secreted by bacterial cell. This subject has been a great interest for a long time because of their importance in successful development of symbiosis with legume hosts. The production of EPS by the rhizobia is considered to have important physiological implications and its critical constituents seemed to be only for the invasion process leading to indeterminate and determinate nodule types. Several putative roles have been considered for EPS synthesis such as specific signaling in the root invasion process, inhibition of plant defense response structural requirement for this process and electrophoretic mobility of rhizobial cells.

On the other hand, new development of molecular methods that advances our understanding of the biosynthesis, regulation and secretion of exopolysaccharides. The important goal for the future research should be the enlightenment of mechanisms of EPSs action as signaling molecules in the initiation and development of symbiosis and mechanisms of control of the plant defense systems which enable rhizobia to invade legume plants and their survival.

Acknowledgements

Authors gratefully acknowledged the financial support provided by the UGC , New Delhi, India, through CAS, Department of Botany, and The University of Burdwan , Burdwan, West Bengal, India. The authors also gratefully acknowledged DST (SERB), New Delhi, India (NPDF/2016/00323 dt. 05.07.2016) for providing National Post-Doctoral Fellowship to the first author.

References

  1. Amemura et al., 1983 A. Amemura, T. Harada, M. Abe, S. Higashi; Structural studies on the extracellular acidic polysaccharide from Rhizobium trifolii 4S  ; Carbohydr. Res., 115 (1983), pp. 165–174
  2. Becker and Pühler, 1998 A. Becker, A. Pühler; Production of exopolysaccharides; H.P. Spaink, A. Kondorosi, P.J.J. Hooykaas (Eds.), Rhizobiaceae, Kluwer Acad Publ., Dordrecht, Boston, London (1998), pp. 97–118
  3. Breedveld et al., 1990 M.W. Breedveld, L.P.T.M. Zevenhuizen, A.J.B. Zehnder; Excessive excretion of cyclic 3-(1, 2)-glucan by Rhizobium trifolii TA-1  ; Appl. Environ. Microbiol., 56 (1990), pp. 2080–2086
  4. Breedveld et al., 1992 M.W. Breedveld, L.P.T.M. Zevenhuizen, A.J.B. Zehnder; Synthesis of cyclic 1B-(1, 2)-glucans by Rhizobium leguminosarum biovar trifolii TA-1: factors influencing excretion  ; J. Bacteriol. (1992), pp. 6336–6342
  5. Breedveld et al., 1993 M.W. Breedveld, C.H.C.J. Canters, M. Batley, M.A. Posthumus, L.P.T.M. Zevenhuizen, C.A. Wijffelman, A.J.B. Zehnder; Polysaccharides synthesis in relation to nodulation behaviour of Rhizobium leguminosarum; J. Bacteriol., 175 (1993), pp. 750–757
  6. Brewin, 2004 N.J. Brewin; Plant cell wall remodelling in the Rhizobium -legume symbiosis  ; CRC Crit. Rev. Plant Sci., 23 (2004), pp. 293–316
  7. Campbell et al., 1998 G.O. Campbell, B.L. Reuhs, G.C. Walker; Different phenotypic classes of Sinorhizobium meliloti mutants defective in synthesis of K antigen  ; J. Bacteriol., 180 (1998), pp. 5432–5436
  8. Canter-Cremers et al., 1991 H.C.J. Canter-Cremers, K. Stevens, B.J.J. Lugtengberg, C.A. Wijffelman, M. Batley, J.W. Redmond, M. Breedveld, L.P.T.M. Zevenhuizen; Unusual structure of the exopolysaccharide of Rhizobium leguminosarum bv. viciae strain 248  ; Carbohydr. Res., 218 (1991), pp. 185–200
  9. Castellane et al., 2015 T.C.L. Castellane, M.R. Persona, J.C. Campanharo, E.G.M. Lemos; Production of exopolysaccharide from rhizobia with potential biotechnological and bioremediation applications; Int. J. Biol. Macromol., 74 (2015), pp. 515–522
  10. Cheng and Walker, 1998 H.P. Cheng, G.C. Walker; Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti; J. Bacteriol., 180 (1998), pp. 5183–5191
  11. Ciesla et al., 2016 J. Ciesla, M. Kopycinska, M. Lukowska, A. Bieganowski, M. Janczarek; Surface properties of wild type Rhizobium leguminosarum bv. trifolii strain 24.2 and its derivatives with different extracellular polysaccharide content  ; PLoS One, 11 (10) (2016), Article e0165080 http://dx.doi.org/10.137/journal.pone.0165080
  12. Datta and Basu, 1999 C. Datta, P.S. Basu; Production of extracellular polysaccharides by a Rhizobium species from root nodules of Cajanus cajan; Acta Biotechnol., 19 (1999), pp. 59–68
  13. Dazzo et al., 1984 F.B. Dazzo, G.L. Truchet, J.E. Sherwood, E.M. Hrabak, M. Abe, S.H. Pankratz; Specific phases of root hair attachment in the Rhizobium trifolii -clover symbiosis  ; Appl. Environ. Microbiol., 48 (1984), pp. 1140–1150
  14. De and Basu, 1996 P.S. De, P.S. Basu; Production of extracellular polysaccharides by a Rhizobium sp. from the root nodules of Tephrosia purpurea Pers  ; Acta Biotechnol., 16 (1996), pp. 155–162
  15. D'Haeze et al., 2004 W. D'Haeze, J. Glushka, R. De Rycke, M. Holsters, R.W. Carlson; Structural characterization of extracellular polysaccharides of Azorhizobium caulinodans and importance for nodule initiation on Sesbania rostrata; Mol. Microbiol., 52 (2004), pp. 485–500
  16. Djordjevic et al., 1987 S.P. Djordjevic, H. Chen, M. Batley, J.W. Redmond, B.G. Rolfe; Nitrogen fixation ability of exopolysaccharide synthesis mutants of Rhizobium sp. strain NGR234 and Rhizobium trifolii is restored by the addition of homologous exopolysaccharides  ; J. Bacteriol., 169 (1987), pp. 53–60
  17. Doherty et al., 1988 D. Doherty, J.A. Leigh, J. Glazebrook, G.C. Walker; Rhizobium meliloti mutants that over produce the R. meliloti acidic calcafluor-binding exopolysaccharide  ; J. Bacteriol., 170 (1988), pp. 4249–4256
  18. Downie, 2010 J.A. Downie; The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots; FEMS Microbiol. Rev., 34 (2010), pp. 150–170
  19. Dudman, 1964 W.F. Dudman; Growth and extracellular polysaccharide production by Rhizobium meliloti in defined medium  ; J. Bacteriol., 88 (1964), pp. 640–645
  20. Duta et al., 2006 F.P. Duta, F.P. Franca, L.L.M. Almeida; Optimization of culture conditions for exopolysaccharide production in Rhizobium sp. using the response surface method  ; Electron. J. Biotechnol., 9 (2006), pp. 391–399
  21. Fisher and Long, 1992 R.F. Fisher, S.R. Long; Rhizobium — plant signal exchange  ; Nature, 357 (1992), pp. 655–660
  22. Fraysse et al., 2003 N. Fraysse, F. Couderc, V. Poinsot; Surface polysaccharide involvement in establishing the Rhizobium -legume symbiosis  ; Eur. J. Biochem., 270 (2003), pp. 1365–1380
  23. Fujishige et al., 2006 N.A. Fujishige, N.N. Kapadia, P.L. De Hoff, A.M. Hirsch; Investigations of Rhizobium biofilm formation  ; FEMS Microbiol. Ecol., 56 (2006), pp. 195–206
  24. Geurts and Bisseling, 2002 R. Geurts, T. Bisseling; Rhizobium nod factor perception and signalling; Plant Cell (2002), pp. S239–S249
  25. Gharzouli et al., 2013 R. Gharzouli, M.A. Carpéné, F. Couderc, A. Benguedouar, V. Poinsot; Relevance of fucose-rich extracellular polysaccharides produced by Rhizobium sullae strains nodulating Hedysarum coronarium L. legumes  ; Appl. Environ. Microbiol., 79 (6) (2013), pp. 1764–1776
  26. Ghosh et al., 2005 A.C. Ghosh, S. Ghosh, P.S. Basu; Production of extracellular polysaccharide by a Rhizobium species from root nodules of leguminous tree Dalbergia lanceolaria; Eng. Life Sci., 5 (2005), pp. 378–382
  27. Ghosh et al., 2011 S. Ghosh, P. Ghosh, P. Saha, K.T. Maiti; The extracellular polysaccharide produced by Rhizobium sp. isolated from the root nodules of Phaseolus mungo; Symbiosis, 53 (2011), pp. 75–81
  28. Ghosh et al., 2015 P.K. Ghosh, J. Ganguly, P. Maji, T.K. Maiti; Production and composition of extracellular polysaccharide synthesized by Rhizobium undicola isolated from aquatic legume, Neptunia oleracea Lour  ; Proc. Natl. Acad. Sci. India B Biol. Sci., 85 (2015), pp. 581–590
  29. Gil-Serrano et al., 1999 A.M. Gil-Serrano, C.M.A. Rodriguez, M.P. Tejero, J.L. Espartero, M. Menendez, J. Corzo, J.E. Ruiz-Sainz, C.A. Buendia; Structural determination of a 5-acetamido-3,5,7,9-tetradeoxy-7-(3-hydroxy-butyramido)-l -glycero-l -manno-nonulosonicacid containing homopolysaccharide isolated from Sinorhizobium fredii HH103  ; Biochemist, 342 (1999), pp. 527–535
  30. Gonzalez et al., 1996 J.E. Gonzalez, G.M. York, G.C. Walker; Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function  ; Gene, 179 (1996), pp. 141–146
  31. Gonzalez et al., 1998 J.E. Gonzalez, C.E. Semino, L.X. Wang, L.E. Castellano-Torres, G.C. Walker; 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 (1998), pp. 13477–13482
  32. Guentas et al., 2000 L. Guentas, P. Pheulpin, A. Heyraud, C. Gey, B. Courtois, J. Courtois; Production of a glucoglucuronan by a rhizobia strain infecting alfalfa. Structure of the repeating unit; Int. J. Biol. Macromol., 27 (2000), pp. 269–277
  33. Her et al., 1990 G.R. Her, J. Glazebrook, G.C. Walker, V.N. Reinhold; Structural studies of a novel exopolysaccharide produced by a mutant of Rhizobium meliloti strain Rm 1021  ; Carbohydr. Res., 198 (1990), pp. 305–312
  34. Ivashina and Ksenzenko, 2012 T.N. Ivashina, V.N. Ksenzenko; Exopolysaccharide biosynthesis in Rhizobium leguminosarum from genes to functions  ; D.N. Karunaratne (Ed.), The Complex World of Polysaccharides, InTech, Rijeka, Croatia (2012), pp. 99–127
  35. Janczarek, 2011 M. Janczarek; Environmental signals and regulatory pathways that influence exopolysaccharide production in Rhizobia; Int. J. Mol. Sci., 12 (2011), pp. 7898–7933
  36. Janczarek et al., 2014 M. Janczarek, R. Kamila, M. Anna, G. Jarosław, P.S. Marta; Signal molecules and cell-surface components involved in early stages of the legume–Rhizobium interactions  ; Appl. Soil Ecol., 85 (2014), pp. 94–113
  37. Kaci et al., 2005 Y. Kaci, A.H.M. Barakat, T. Heulin; Isolation and identification of an EPS-producing Rhizobium strain from arid soil (Algeria): characterization of its EPS and the effect of inoculation on wheat rhizosphere soil structure  ; Res. Microbiol., 156 (2005), pp. 522–531
  38. Karr et al., 2000 D.B. Karr, R.T. Liang, B.L. Reuhs, D.W. Emerich; Altered exopolysaccharides of Bradyrhizobium japonicum mutants correlate with impaired soybean lectin binding, but not with effective nodule formation  ; Planta, 211 (2000), pp. 218–226
  39. Kaufusi et al., 2004 P.H. Kaufusi, L.S. Forsberg, P. Tittabutr, D. Borthakur; Regulation of exopolysaccharide synthesis in Rhizobium sp. strain TAL1145 involves an alternative sigma factor gene, rpoH2  ; Microbiology, 150 (2004), pp. 3473–3482
  40. Kelly et al., 2013 S.J. Kelly, A. Muszynski, Y. Kawaharada, A.M. Hubber, J.T. Sullivan, N. Sandal, R.W. Carlson, J. Stougaard, C.W. Ronson; Conditional requirement for exopolysaccharide in the MesorhizobiumLotus symbiosis  ; Mol. Plant Microbe Interact., 26 (2013), pp. 319–329
  41. Kijne, 1992 J.W. Kijne; The Rhizobium infection process  ; G. Stacey, R.H. Burris, H.J. Evans (Eds.), Biological Nitrogen Fixation, Chapman, New York, USA (1992), pp. 293–398
  42. Kucuk and Kivanc, 2009 C. Kucuk, M. Kivanc; Extracellular polysaccharide production by Rhizobium ciceri from Turky  ; Ann. Microbiol., 59 (2009), pp. 141–144
  43. Kumari et al., 2009 B.S. Kumari, M.R. Ram, K.V. Mallalah; Studies on exopolysaccharide and indole acetic acid production by Rhizobium strains from Indigofera sp.  ; Afr. J. Microbiol. Res., 3 (1) (2009), pp. 14–20
  44. Laus et al., 2005 M.C. Laus, A.A.N. Van Brussel, J.W. Kijne; Role of cellulose fibrils and exopolysaccharides of Rhizobium leguminosarum in attachment to and infection of Vicia sativa root hairs  ; Mol. Plant-Microbe Interact., 18 (2005), pp. 533–538
  45. Luciana et al., 2010 V.R. Luciana, F. Sorroche, A. Zorreguieta, W. Giordano; Analysis of the mucR gene regulating biosynthesis of exopolysaccharides: implications for biofilm formation in Sinorhizobium meliloti Rm1021  ; FEMS Microbiol. Lett., 302 (1) (2010), pp. 15–21
  46. Mandal et al., 2007 M.S. Mandal, B. Ray, S. Dey, B. Pati; Production and composition of extracellular polysaccharide synthesized by a Rhizobium isolate of Vigna mungo (L.) Hepper  ; Biotechnol. Lett., 29 (2007), pp. 1271–1275
  47. Martinez-Romero et al., 1991 E. Martinez-Romero, L. Segovia, F.M. Mercante, A.A. Franco, P. Graham, M.A. Pardo; Rhizobium tropici , a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees  ; Int. J. Syst. Bacteriol., 41 (1991), pp. 417–426
  48. Mikini et al., 1984 A.B.E. Mikini, J.E. Sherwood, R.I. Hollingworth, F.B. Dazzo; Stimulation of clover root hair infection by lectin-binding oligosaccharide from the capsular and extracellular polysaccharides of Rhizobium trifolii; J. Bacteriol., 160 (1984), pp. 517–520
  49. Moretto et al., 2015 C. Moretto, T.C.L. Castellane, E.M. Lopes, W.P. Omori, L.P. Sacco, E.G.M. Lemos; Chemical and rheological properties of exopolysaccharides produced by four isolates of rhizobia; Int. J. Biol. Macromol., 81 (2015), pp. 291–298
  50. Mukherjee et al., 2011 S. Mukherjee, S. Ghosh, S. Sadhu, P. Ghosh, T.K. Maiti; Extracellular polysaccharide production by a Rhizobium sp. isolated from legume herb Crotalaria saltiana Andr  ; Indian J. Biotechnol., 10 (2011), pp. 340–345
  51. Oldroyd and Downie, 2004 E.D.G. Oldroyd, J.A. Downie; Calcium, kinases and nodulation signalling in legumes; Nature, 5 (2004), pp. 566–576
  52. Priyanka et al., 2015 P. Priyanka, A.B. Arun, P. Ashwini, P.D. Rekha; Versatile properties of an exopolysaccharide R-PS18 produced by Rhizobium sp. PRIM-18  ; Carbohydr. Polym., 126 (2015), pp. 215–221
  53. Razika et al., 2012 G. Razika, B. Amira, B. Yacine, B. Ammar; Influence of carbon source on the production of exopolysaccharide by Rhizobium sullae and on the nodulation of Hedysarum coronarium L. legume  ; Afr. J. Microbiol. Res., 6 (2012), pp. 5940–5946
  54. Reinhold et al., 1994 B.B. Reinhold, S.Y. Chan, T.L. Reuber, A. Marra, G.C. Walker, V.N. Reinhold; Detailed structural characterization of succinoglycan, the major exopolysaccharide of Rhizobium meliloti Rm 1021  ; J. Bacteriol., 176 (1994), pp. 1997–2002
  55. Reuhs et al., 1993 B.L. Reuhs, R.W. Carlson, J.S. Kim; Rhizobium fredii and Rhizobium meliloti produce 3-deoxy-d -manno-2-octulosonic acid-containig polysaccharides that are structurally analogous to group II K antigens (capsular polysaccharides) found in Escherichia coli; J. Bacteriol., 175 (1993), pp. 3570–3580
  56. Reuhs et al., 1998 B.L. Reuhs, D.P. Geller, J.S. Kim, J.E. Fox, V.S.K. Kolli, S.G. Pueppke; Sinorhizobium fredii and Sinorhizobium meliloti produce structurally conserved lipopolysaccharide and strain specific kantigens  ; Appl. Environ. Microbiol., 64 (1998), pp. 4930–4938
  57. Robertson et al., 1981 B.K. Robertson, P. Aman, A.G. Darvill, M. McNeil, P. Albersheim; Host symbiont interactions. V. The structure of acidic extracellular polysaccharides secreted by Rhizobium leguminosarum and Rhizobium trifolii; Plant Physiol., 67 (1981), pp. 389–400
  58. Rolfe et al., 1996 B.G. Rolfe, R.W. Carlson, R.W. Ridge, F.B. Dazzo, P.F. Mateos, C.E. Pankhurst; Defective infection and nodulation of clovers by exopolysaccharide mutants of Rhizobium leguminosarum cf. trifolii; Aust. J. Plant Physiol., 23 (1996), pp. 285–303
  59. Sayyed et al., 2011 R.Z. Sayyed, D.D. Jamadar, P.R. Patel; Production of exo-polysaccharide by Rhizobium sp.  ; Indian J. Microbiol., 51 (3) (2011), pp. 294–300
  60. Schulze et al., 1998 M. Schulze, E. Kondorosi, P. Ratet, M. Buire, A. Kondorosi; Cell and molecular biology of Rhizobium –plant interaction  ; Int. Rev. Cytol., 156 (1998), pp. 1–75
  61. Skorupska et al., 2006 A. Skorupska, M. Janczarek, M. Marczak, A.M.J. Krol; Rhizobial exopolysaccharides: genetic control and symbiotic functions; Microb. Cell Factories, 5 (2006), p. 7
  62. Smit et al., 1992 G. Smit, S. Swart, B.J.J. Lugtenberg, J.W. Kijne; Molecular mechanisms of attachment of Rhizobium bacteria to plant roots  ; Mol. Microbiol., 6 (1992), pp. 2897–2903
  63. Spaink, 2000 H.P. Spaink; Root nodulation and infection factors produced by rhizobial bacteria; Annu. Rev. Microbiol., 54 (2000), pp. 257–288
  64. Staudt et al., 2012 A.K. Staudt, G.W. Lawrence, D.S. Joshua; Variations in exopolysaccharide production by Rhizobium tropici; Arch. Microbiol., 194 (2012), pp. 197–206
  65. Stowers, 1985 M.D. Stowers; Carbon metabolism in Rhizobium species  ; Annu. Rev. Microbiol., 39 (1985), pp. 89–108
  66. Sutherland, 1972 I.W. Sutherland; Bacterial exopolysaccharides; Microbial Physiology, Academic Press Inc., London (1972), pp. 143–213
  67. Van Workum et al., 1998 W.A.T. Van Workum, S. Van Slageron, A.A.N. Van Brussel, J.W. Kijne; Role of exopolysaccharide of Rhizobium leguminosarum bv. viciae as host plant-specific molecules required for infection thread formation during nodulation of Vicia sativa; Mol. Plant-Microbe Interact., 11 (1998), pp. 1233–1241
  68. Wang et al., 1999 L.X. Wang, Y. Wang, B.J. Pellock, G.C. Walker; Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti; J. Bacteriol., 181 (1999), pp. 6788–6796
  69. Watson et al., 2001 R.J. Watson, R. Heys, T. Martin, M. Savard; Sinorhizobium meliloti cells require biotin and either cobalt or methionine for growth  ; Appl. Environ. Microbiol., 67 (8) (2001), pp. 3767–3770
  70. Wielbo et al., 2004 J. Wielbo, A. Mazur, J. Krol, M. Marczak, J. Kutkowska, A. Skorupska; Complexity of phenotypes and symbiotic behaviour of Rhizobium leguminosarum biovar trifolii exopolysaccharide mutants  ; Arch. Microbiol., 182 (2004), pp. 331–336
  71. Williams et al., 2008 A. Williams, A. Wilkinson, M. Krehenbrink, D.M. Russo, A. Zorreguieta, J.A. Downie; Glucomannan-mediated attachment of Rhizobium leguminosarum to pea root hairs is required for competitive nodule infection  ; J. Bacteriol., 190 (2008), pp. 4706–4715
  72. Zevenhuizen, 1997 L.P.T.M. Zevenhuizen; Succinoglycan and galactoglucan; Carbohydr. Polym., 33 (1997), pp. 139–144
  73. Zhan et al., 1990 H. Zhan, X. Gray, B. Levery, B.G. Rolfe, J.A. Leigh; Functional and evolutionary relatedness of genes for exopolysaccharide synthesis in Rhizobium meliloti and Rhizobium sp. strain NGR234  ; J. Bacteriol., 172 (1990), pp. 5245–5253
  74. Zhan et al., 1991 H. Zhan, C.C. Lee, J.A. Leigh; Induction of second exopolysaccharide (EPSb) in Rhizobium meliloti SU47 by low phosphate concentrations  ; J. Bacteriol., 173 (1991), pp. 7391–7394
  75. Zhou et al., 2014 R. Zhou, Z. Wu, C. Chen, J. Han, L. Ai, B. Guo; Exopolysaccharides produced by Rhizobium radiobacter S10 in whey and their rheological properties  ; Food Hydrocoll., 36 (2014), pp. 362–368
Back to Top

Document information

Published on 27/03/17

Licence: Other

Document Score

0

Views 79
Recommendations 0

Share this document

claim authorship

Are you one of the authors of this document?