Exopolysaccharide Carbohydrate Structure and Biofilm Formation by Rhizobium leguminosarum bv. trifolii Strains Inhabiting Nodules of Trifoliumrepens Growing on an Old Zn–Pb–Cd-Polluted Waste Heap Area
Abstract
:1. Introduction
2. Results
2.1. Exopolysaccharide (EPS) Carbohydrates Analysis
2.1.1. Qualitative Determination of EPS Carbohydrates
2.1.2. Quantitative Analysis of EPS Carbohydrates
2.1.3. Quantitative and Qualitative Comparison of Carbohydrate Content between R. leguminosarum bv. trifolii of Waste Heap and Reference Grassland Origin
2.1.4. Quantitative and Qualitative Comparison of Carbohydrate Content between Strains of R. leguminosarum bv. trifolii Originating from a Waste Heap and a Non-Polluted Reference Area
2.2. Biofilms Structure Analysis Using CLSM
3. Discussion
4. Materials and Methods
4.1. Exopolysaccharide (EPS) Carbohydrates Analysis
4.1.1. EPS Extraction
4.1.2. EPS Monosaccharides Analysis by GC-MS
Qualitative Assessment of EPS Monosaccharides
Quantitative Assessment of EPS Monosaccharides
4.2. Biofilm Formation and Structure Analysis
4.2.1. Quantification of Biofilm Formation
4.2.2. Biofilms Structure Analysis
4.3. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Carbohydrate | Control | Cd 0.05 | Cd 1.0 | Zn 0.5 | Zn 2.5 | Pb 0.5 | Pb 2.5 | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
R | WH | R | WH | R | WH | R | WH | R | WH | R | WH | R | WH | |
α-D,L-lyxopyranose | - | 15.13 a | - | - | - | - | - | - | - | - | - | - | - | - |
α-D-arabinopyranose | - | - | - | - | 17.78 a | - | 21.70 ± 1.60 a | - | - | - | 51.50 ± 43.56 a | 18.78 ± 1.19 a | - | - |
D-rhamnose | - | - | - | - | - | - | - | - | - | - | - | 6.69 b | - | - |
L-rhamnose monohydrate | - | - | - | - | - | - | 6.41 b | - | - | - | 12.02 a | - | - | - |
levoglucosan | 18.84 ± 0.22 a | - | 18.90 ± 1.05 a | 17.92 ± 0.44 a | - | - | - | - | - | - | - | - | - | - |
6-deoxy-D-glucose | 55.00 ± 1.33 b | 40.47 ± 21.27 a | - | - | - | - | - | - | - | - | - | - | - | - |
methyl α-D-mannopyranoside | 19.72 ± 0.22 a | 20.00 ± 0.64 a | - | - | 47.09 ± 13.79 b# | 32.68 ± 3.24 a# | 31.36 ± 8.66 a | 36.61 ± 12.86 a | 25.29 ± 8.78 a | 18.21 ± 0.25 a | 76.63 ± 11.57 b# | 73.08 ± 27.78 c# | 47.42 ± 7.41 a# | 63.22 ± 17.38 a# |
galactofuranoside | 20.88 ± 1.24 a | 18.72 ± 0.11 a | 15.07 ± 3.48 a | - | - | - | 18.65 ± 0.17 a | - | - | - | 18.43 a | - | - | - |
α-D-mannopyranose | 19.41 ± 0.15 a | - | 20.73 ± 2.02 a | 18.55 a | 18.66 ± 0.49 a | 18.15 ± 0.13 b | 19.08 ± 0.74 a | 19.53 ± 1.56 b | - | - | 21.77 ± 0.82 a | 21.55 ± 3.75 a | 18.86 ± 0.16 b | 19.35 ± 0.73 b |
D-fructose | 32.72 ± 2.55 c | 40.13 ± 9.54 b | - | - | 15.10 ± 2.45 a | - | 13.78 ± 1.56 c# | 21.00 ± 6.66 b# | 13.58 a# | 11.88 ± 0.27 b# | 16.73 ± 3.51 a# | 20.38 ± 13.77 a# | 12.89 ± 0.80 b# | 13.56 ± 2.13 b# |
β-D-galactopyranoside | 19.43 ± 0.28 a | 16.81 ± 2.22 a | 13.75 ± 1.20 a | 19.79 a | 23.55 a | - | 87.08 ± 59.59 a# | 18.54 ± 0.85 b* | - | - | 69.51 ± 64.05 a# | 36.57 ± 23.88 ab# | - | 18.62 b |
α-D-galactofuranose | - | - | - | - | - | - | 18.80 a | - | - | - | 19.21 a | - | - | - |
α-D-mannofuranose | - | - | - | - | - | - | 14.74 ± 2.12 c | - | - | - | - | 13.65 a | - | - |
α-glucofuranose | 20.11 ± 2.28 a | 23.52 ± 1.15 a | 18.06 a | - | - | - | - | 18.33 ± 0.75 b | - | - | - | 18.86 a | - | - |
D-galactose | 235 ± 8.42 d | 172 ± 144 b | 18.52 a# | - | - | - | 25.11 ± 4.78 a# | - | - | - | 23.65 ± 7.38 a# | 22.73 ± 7.07 a# | - | - |
α-D-glucopyranoside | 23.09 ± 3.88 a | 21.89 ± 5.40 a | 24.64 ± 3.77 a | 23.78 ± 5.20 a | 20.84 ± 2.52 a | 21.27 ± 2.64 b | 40.15 ± 24.22 a | 39.19 ± 15.94 a | 19.95 ± 0.03 a | - | 84.63 ± 31.64 a# | 123.96 ± 131 abc# | 20.38 ± 0.73 b | 22.63 ± 3.24 b |
α-D-glucopyranose | 66.42 ± 14.6 b | 75.29 ± 15.54 c | - | - | - | - | - | - | - | - | - | - | - | - |
D-glucose | 58.33 ± 30.1 b | 69.23 ± 16.04 c | 18.12 a# | 18.16 a# | - | - | 21.26 ± 3.49 a# | 19.20 ± 1.61 b# | - | - | 19.70 ± 0.82 a | 54.73 ± 6.74 c* | - | - |
β-D-galactopyranose | 18.88 ± 3.15 a | 16.64 ± 0.00 a | - | - | 19.00 ± 1.04 a | 18.76 ± 0.77 b | 25.14 ± 7.54 a | 23.72 ± 5.21 b | - | - | 42.86 ± 12.49 a# | 60.80 ± 53.75 abc | 18.48 ± 0.16 b | 19.19 ± 1.03 b |
β-D-mannopyranose | - | - | - | - | - | - | 18.32 ± 0.35 a | 19.48 ± 1.38 b | - | - | 19.56 ± 0.46 a | 24.57 ± 7.45 ab | - | - |
β-talopyranose | - | - | - | - | - | 20.54 b | 41.17 ± 21.08 a | 47.71 ± 15.27 a | - | - | 174.68 ± 55.58 b | 56.45 ± 22.51 ac | - | 18.69 b |
sedoheptulose | 20.26 ± 3.40 a | 24.12 ± 3.58 a | - | - | 134 ± 106 b# | 187 ± 2.57 c# | - | 11.18 b | - | 17.43 a | 21.30 a | - | 28.58 ab | - |
β-D-glucopyranose | 24.90 ± 4.98 a | 24.23 ± 9.10 a | 25.82 ± 2.86 a | 24.64 ± 4.58 a | - | - | - | - | - | - | - | - | - | - |
gluconic acid | 47.47 ± 2.99 b | - | 53.40 ± 3.15 b | 48.37 b | - | - | 71.37 d | 50.34 ± 4.33 a | - | - | 46.54 a | - | - | - |
glucuronic acid | - | - | - | - | - | - | 64.31 ± 31.74 a | 70.10 ± 25.83 a | - | - | 92.74 ± 36.33 b | 65.60 ± 27.40 bc | - | - |
D-glucuronic acid | - | - | - | - | - | - | 41.91 a | - | - | - | - | - | - | - |
myo-inositol | - | - | - | - | - | - | - | - | - | - | 26.93 a | - | - | - |
N-acetyl-D-glucosamine | - | - | - | - | - | - | 17.52a | - | - | - | 19.85 a | - | - | - |
glucitol | 250 ± 233 d | 327 ± 322 b | 84.58 ± 35.73 b# | 86.37 ± 20.44 b# | 1145 ± 240 c# | 717 ± 99 d*# | 575.05 ± 186.7 c# | 761.54 ± 67.24 c# | 654.79 ± 93.12 b# | 633.23 ± 53.83 c# | 1562 ± 234 c# | 948.12 ± 451 d | 868.81 ± 135 c# | 1181 ± 157.83 c# |
galactonic acid | - | 179 ± 175 b | - | - | - | - | 177.29 ± 112 a | 112.90 ± 76.86 d | - | - | 133.11 ± 34.75 b | 1532 ± 244 d* | - | - |
Rhizobial Strain | C | Cd 0.05 | Cd 1.0 | Zn 0.5 | Zn 2.5 | Pb 0.5 | Pb 2.5 |
---|---|---|---|---|---|---|---|
8.8K | 42.66 ± 7.51 a | 27.88 ± 1.81 a | 17.28 ± 1.10 a | 18.40 ± 2.07 a | 19.33 ± 2.10 a | 39.53 ± 0.00 a | 11.86 ± 0.06 a |
4.4K | 76.26 ± 7.90 b | 36.09 ± 2.70 b | 19.12 ± 1.08 b | 20.63 ± 0.98 a | 22.62 ± 2.97 a | 39.43 ± 2.09 a | 12.44 ± 0.01 a |
3.9K | 61.99 ± 1.01 a | 33.80 ± 2.80 a | 16.36 ± 0.60 a | 19.41 ± 0.45 a | 21.28 ± 2.58 a | 38.63 ± 2.08 a | 12.98 ± 0.25 a |
5.10K | 43.68 ± 6.45 a | 29.75 ± 3.35 a | 17.31 ± 1.21 a | 18.22 ± 3.08 a | 20.45 ± 2.18 a | 37.59 ± 1.18 a | 11.19 ± 0.09 a |
K | 59.46 ± 17.65 | 31.99 ± 3.94 # | 18.20 ± 1.40 ## | 19.52 ± 1.90 # | 20.98 ± 2.92 # | 39.46 ± 1.71 # | 12.09 ± 0.30 ## |
5.2H | 47.82 ± 6.26 a | 27.39 ± 6.58 a | 16.45 ± 1.68 a | 37.86 ± 2.87 a | 15.07 ± 1.12 a | 19.03 ± 1.33 a | 10.94 ± 0.81 a |
7.2H | 27.44 ± 2.60 b | 26.25 ± 2.30 a | 17.22 ± 0.25 a | 25.00 ± 4.44 b | 17.62 ± 0.66 a | 28.64 ± 4.60 b | 14.96 ± 1.11 a |
4.1H | 35.54 ± 11.22 b | 24.06 ± 2.97 a | 17.17 ± 1.01 a | 19.73 ± 0.14 c | 16.27 ± 0.67 a | 41.95 ± 15.95 b | 14.15 ± 0.25 a |
H | 32.40 ± 5.04 * | 23.62 ± 4.06 *# | 16.30 ± 1.09 ## | 23.00 ± 8.50 # | 15.81 ± 1.33 *# | 27.06 ± 12.98 # | 12.76 ± 1.97 ## |
Rhizobial Strain | C | Cd 0.05 | Cd 1.0 | Zn 0.5 | Zn 2.5 | Pb 0.5 | Pb 2.5 |
---|---|---|---|---|---|---|---|
8.8K | 3.19 ± 0.29 a | 2.00 ± 0.20 a | 0.37 ± 0.09 a | 0.32 ± 0.03 a | 0.53 ± 0.11 a | 2.18 ± 0.33 a | 0.48 ± 0.12 a |
4.4K | 2.94 ± 0.34 a | 2.58 ± 0.31 a | 0.96 ± 0.04 b | 0.78 ± 0.30 b | 1.33 ± 0.09 b | 3.75 ± 0.35 b | 0.80 ± 0.05 b |
3.9K | 2.52 ± 0.06 a | 1.45 ± 0.03 b | 0.23 ± 0.01 c | 0.38 ± 0.06 a | 0.28 ± 0.08 a | 1.63 ± 0.24 a | 0.36 ± 0.07 a |
5.10K | 3.25 ± 0.16 a | 2.23 ± 0.12 a | 0.35 ± 0.08 a | 0.32 ± 0.08 a | 0.52 ± 0.09 a | 2.18 ± 0.21 a | 0.48 ± 0.11 a |
K | 3.43 ± 0.51 | 2.07 ± 0.15 # | 0.34 ± 0.10 ## | 0.32 ± 0.07 # | 0.36 ± 0.17 # | 2,75 ± 0.21 # | 0.42 ± 0.05 ## |
5.2H | 2.94 ± 1.21 a | 4.69 ± 1.18 a | 1.59 ± 0.17 a | 4.26 ± 0.54 a | 0.52 ± 0.06 a | 4.80 ± 0.84 a | 0.56 ± 0.02 a |
7.2H | 3.01 ± 0.60 a | 2.72 ± 0.57 b | 1.19 ± 0.06 b | 2.67 ± 0.44 b | 1.34 ± 0.12 b | 3.62 ± 0.63 a | 0.73 ± 0.05 b |
4.1H | 3.06 ± 0.72 a | 2.15 ± 0.07 b | 0.43 ± 0.02 c | 0.41 ± 0.07 c | 0.41 ± 0.03 c | 5.58 a | 0.50 ± 0.01 c |
H | 3.00 ± 0.69 | 3.14 ± 0.87 * | 1.21 ± 0.27 *# | 3.10 ± 0.85 * | 0.89 ± 0.27 *# | 4.01 ± 0.71 * | 0.57 ± 0.04 *# |
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Oleńska, E.; Małek, W.; Kotowska, U.; Wydrych, J.; Polińska, W.; Swiecicka, I.; Thijs, S.; Vangronsveld, J. Exopolysaccharide Carbohydrate Structure and Biofilm Formation by Rhizobium leguminosarum bv. trifolii Strains Inhabiting Nodules of Trifoliumrepens Growing on an Old Zn–Pb–Cd-Polluted Waste Heap Area. Int. J. Mol. Sci. 2021, 22, 2808. https://doi.org/10.3390/ijms22062808
Oleńska E, Małek W, Kotowska U, Wydrych J, Polińska W, Swiecicka I, Thijs S, Vangronsveld J. Exopolysaccharide Carbohydrate Structure and Biofilm Formation by Rhizobium leguminosarum bv. trifolii Strains Inhabiting Nodules of Trifoliumrepens Growing on an Old Zn–Pb–Cd-Polluted Waste Heap Area. International Journal of Molecular Sciences. 2021; 22(6):2808. https://doi.org/10.3390/ijms22062808
Chicago/Turabian StyleOleńska, Ewa, Wanda Małek, Urszula Kotowska, Jerzy Wydrych, Weronika Polińska, Izabela Swiecicka, Sofie Thijs, and Jaco Vangronsveld. 2021. "Exopolysaccharide Carbohydrate Structure and Biofilm Formation by Rhizobium leguminosarum bv. trifolii Strains Inhabiting Nodules of Trifoliumrepens Growing on an Old Zn–Pb–Cd-Polluted Waste Heap Area" International Journal of Molecular Sciences 22, no. 6: 2808. https://doi.org/10.3390/ijms22062808