r): [A] sodium lactate 60% (12 ml), K2HPO4 (0.35 g), KH2P04 (0.25 g), Na2S04 (4.00 g), MgS04, 7H2O (2.00 g), NaCl (0.5 g), NH4Cl (2.00 g), yeast extract (1.00 g), resazurin solution 0.1% (1 ml), 1 ml of trace elements solution [29] ; [B] Na2S, 9H2O (2.5 g), Chlorhydrate of cysteine (1.25 g), NaHCO3 (4.00 g). The heat-stable salts [A] solution was autoclaved and cooled under an atmosphere of N2. Then, the medium was supplemented with components [B] solution, to final concentration of 2%. The pH was adjusted to 7.2 by addition of NaOH 1N solution. Tubes were incubated at 37˚C for two weeks. Formation of colloidal CuS from total sulfides (H2S, S2 and HS) according to Cor-Ruchwich [30] was used for detection of positive tubes after incubation period. The most probable numbers of SRB were calculated from a table of MPN for three tubes.

2.6. Determination of Sulfides Content in Soil

From the soil sampled for bacterial enumeration and at the same periods during the rice cultural cycle, the sulfides were extracted using extraction medium, according to the method adapted from Chaudhry and Cornfield [31] . The extraction medium composition was as follows (per litter of distilled water): CH3 (COO)2 Zn, 2H2O (50 g), CH3COONa, 3H20 (12.5 g). Cor-Ruschwich [30] method was then used to measure the content of sulfides in the soil solution. The extracted sulfides solution (2 ml) was removed by syringe and rapidly injected

Figure 3. Microplots design for the experiments [25] [26] .

into tubes containing 2 ml of a copper reagent. Immediately after mixing (for 5s), the absorbance is measured at 480 nm using a Spectronic 61 photometer.

2.7. Statistical Analysis

Data obtained were analyzed for SRB populations’ development and activity, drainage mode, rice growth stage and rice yield variations using the Student’s t-test and XLSTAT 7.5.2 statistical software. Mean parameters were compared according to the Newman Keuls’ test at 5% probability level.

3. Results and Discussion

3.1. Effect of Soil Moisture on SRB Populations Dynamic and Activity

In the present study, densities of SRB enumerated on soil before flooding, when the soil was dried and at transplanting day after soil flooding, are shown in Figure 4 and expressed as log 10 (most probable population number g1 dry soil).

Sulfides content in soil before flooding when the soil was dried and at transplanting day after one week of soil flooding, are shown in Figure 5 and expressed as log 10 (µg/g dry soil). The concentration of sulfides increased after one week of flooding in the soil for all the microplots.

Rice paddy fields represent a freshwater environment from which sulfate reducers have been isolated and in which sulfate reduction occurs [1] [6] [16] [19] [31] . Many studies showed that sulfate-reducers are common in flooded soils and they are also found near rice roots [8] [32] .

Thus ours results are in agreement with those obtained by Dianou et al. [33] , who reported a population increase of 200%, 139%, 119%, 66%, 40%, 59%, 42% and 22% in the soils of Burkina Faso, after flooding. Garcia et al. [33] reported that SRB populations quantified in the paddy soils of Senegal were influenced by the redox potential related to flooding [34] . Indeed, soon after the flooding of the rice fields, O2 is removed from the bulk soil via respiratory processes, and large amounts of minerals and nutrients available for bacterial growth were released in the soil solution [16] [35] . In these anaerobiosis conditions the strictly anaerobic bacteria, including sulfate reducers, become active. Thus, significant reduction of sulfate occurs in a wide range of rice fields [16] .

Figure 4. Densities of Sulfate-Reducing Bacteria in soil before flooding, at transplanting day, and in soil near rice roots during the cultural cycle of FKR 19 rice in microplots without drainage (T), and drained for 7 days (P1), 14 days (P2) and 21 days (P3), respectively (means of 3 replicates).

Figure 5. Evolution of the soil sulfides content during the cultural cycle of FKR 19 rice in micro- plots not drained (T), and drained for 7 days (P1), 14 days (P2) and 21 days (P3), respectively (means of 3 replicates).

3.2. Effects of Rice Plant on SRB Populations’ Dynamic and Activity

The number of SRB in the soil near rice roots increased after one week of flooding for all microplots (Figure 4). An increase in SRB population number of 95.32%, 93.03%, 86.62% and 88.7% was recorded in the soil of the control (T), P1, P2 and P3 microplots, respectively. Our study also revealed that the number of SRB in soil near rice roots increased gradually with fluctuations from the transplanting day to rice flowering and maturity stages in all the paddy microplots (Figure 4). In most microplots, the highest densities of SRB were recorded from rice tillering and flowering to maturity stages, at which bacterial population number could reach 107 to 108/g dry soil (Figure 4).

The sulfides content in soil near rice roots also increased gradually with fluctuations during the rice cultural cycle and the highest levels were recorded from rice tillering and flowering to maturity stages at which it could reach 102 to 103 µg/g dry soil (Figure 5).

Thus, SRB population density and sulfides concentration in soil near rice roots appeared particularly high at the tillering flowering and maturity stages of rice growth (Figure 4 & Figure 5).

Wind et al. [36] who reported that the number of Sulfate-Reducing Bacteria were higher in planted than in unplanted rice microcosms support our findings. Many studies reported also that sulfate reduction rates and sulfate concentration were high at the root surface and near the rice roots [36] [37] .

Our results are also in agreement with those of Ouattara [18] and Dianou and Traoré [19] who reported that after rice transplanting the numbers of SRB increased significantly in the plant rhizosphere. Dianou and Traoré [19] reported also that populations increased gradually with fluctuations from transplanting day to rice flowering and maturity stages in the soil near rice roots during paddy plots experiments. Dianou and Traoré [19] and Jacq et al. [38] showed that bacterial population number could reach values of 107 to 109/g dry soil in most of paddy plot soils of Senegal and Burkina Faso, from rice tilling and flowering to maturity stages, respectively. The rice heading and repining periods which correspond to the highest level of reduced soil conditions in paddy flooded soil, may be conducive to the growth of SRB as underlined Dianou and Traoré [19] . Thus, the high physiological activity of rice plant at these stages may result in the production of more substrates available for bacterial growth [19] [20] [38] .

3.3. Impact of Drainage on SRB Populations’ Development and Activity

The variance of the SRB density in soil near rice roots, in relation to drainage and sampling period during rice growth is presented in Table 1. The Newman Keuls’ test revealed that the density of SRB in the paddy soil near rice roots was not significantly related to drainage (P = 0.187) (Table 1). Moreover, no significant difference was observed between the average numbers of SRB population in the soil of all the microplots (drained or not) (Table 2). However, the number of bacteria in the paddy soil near rice roots was significantly related to sampling period (P < 0.0001) and to combined both factors (P = 0.000, Table 1). These contrasted results could be partially explained by the MPN method used. Indeed, the analysis of bacterial communities by culturing methods, although valuable to characterize metabolic activities of their members, allows the characterization of only 1% to 3% of the microscopically-detectable cells in soils [39] [40] . Thus, molecular methods could be an indispensable tool to provide a more comprehensive description of the SRB community evolution in relation to drainage [3] [5] [40] [41] .

The variance of the soil sulfides content in relation to drainage and sampling period during rice growth is presented in Table 2. It appeared that sulfides content in the soil near rice roots was significantly related to drainage (P = 0.032) and to the sampling period (P < 0.0001). SRB have been traditionally considered as strict anaerobes [16] [42] . However, in the present study, the SRB population number in the soil of P1, P2 and P3 drained microplots increased slightly as compared to the control (18.45%, 1.06%, 8.76%, respectively) indicating that some among the SRB can survive and grow in aerobic compartments in the presence of low pressure of oxygen where a surplus of oxygen is released by drainage and by healthy roots [38] [43] .

These results are in agreement with the ones of Johnson et al. [44] and Dolla et al. [45] who found that some species of SRB were capable of slow linear aerobic growth in sulfate-containing medium in the presence of very low concentrations of oxygen. Thus, the abundance and metabolic activity of SRB in oxic zones of numerous biotopes are frequently evaluated as higher than those in neighboring anoxic zones [46] [47] . The high number of SRB found in these oxic environments indicates that these organisms are able to deal with temporarily exposures to elevated oxygen concentration [16] [48] . Wind et al. [36] show also that sulfate reduction also takes place on the roots of intact rice plants when O2 is allowed to diffuse to the roots through the aerenchyma system of the plants.

The density of SRB populations and the sulfides concentration in drained microplots could also be explained by heterogeneous distribution of oxygen through the drainage system leading to the formation of anoxic compartments [25] . A lack of oxygenation of such microsites in drained microplots may promote the SRB population survival [49] and the sulfides production [50] . Therefore, an efficient oxygenation of soil by water drainage would significantly reduce anaerobic SRB population’s development and activity.

Table 1. Variance of SRB number and sulfides content in soil near rice roots in relation to drainage and sampling period during the cultural cycle of FKR19 rice.

DF = degree of freedom; F = Fisher F; *significant P < 0.05; **significant P < 0.01; ns not significant P < 0.05.

Table 2. Effect of drainage on SRB population number in soil near rice roots during the cultural cycle of FKR19 rice in microplots not drained (T), and drained for 7 days (P1), 14 days (P2) and 21 days (P3) (means of 3 replicates).

Means with a same letter within a column are not significantly different according to Newman Keuls’ test P > 0.05.

3.4. Impact of Drainage on FKR 19 Rice Yield

In our study, symptoms of sulfides toxicity for rice based on IRRI standard evaluation system [51] weren’t evidenced during the microplot experiments. Although no significant difference (P = 0.209) was found for rice yield among treatments, drained microplots, in particular P2 ones showed the highest yield. Dobermann and Fairhurst [21] reported that an excessive concentration of hydrogen sulfide in the soil results in reduced nutrient uptake due to a decrease of root respiration. The typical symptoms linked to sulfide toxicity involves: rotting of roots, bronzing of leaves, poor growth at the reproductive phase, reduced ability to oxidize iron in the rhizosphere and poor yield [52] - [60] . The symptoms of sulfide toxicity can occur throughout the growth cycle of the rice [21] ; however no critical levels have been established to test sulfide toxicity. Our result can be explained by the chemical fertilizers (NPK and urea) applied in all the microplots. Indeed, according to Dobermann and Fairhurst [21] and Fageria et al. [61] , sulfides toxicity is generally associated with iron toxicity, which is defined as a multiple nutritive disorder further through excesses of H2S [61] . Deficiencies in minerals may enlarge the root permeability that enhances exudation, oxygen consumption and sulfate reduction, finally leading to severe sulfide toxicity [21] [61] - [63] . Many studies reported that sulfides toxicity for rice depends on nutrient supply; thus, amendment of paddy soil in mineral elements may reduce symptoms of sulfide toxicity for rice [64] [65] .

One raison of our results may be that the FKR 19 rice variety is not susceptible to sulfides toxicity as reported some studies [26] .

Rice plants can develop also physiological avoidance mechanisms to survive under toxic-sulfide condition [36] [49] . Indeed, sulfide toxicity depends on the strength of rice root oxidizing power, H2S concentration in the soil solution and root health [21] [38] .

Soil oxygenation by water drainage can affect sulfides profiles [49] [66] . The release of oxygen from the roots of rice causes radial redox gradients around the roots, leading to various chemical and microbial oxidation processes in the rhizosphere along with the oxidation of sulfide to sulfate [67] .

4. Conclusion

The study revealed important populations of cultivable Sulfate-Reducing Bacteria in soil near roots. The SRB populations and the production of sulfides appeared also impacted mainly by the soil flooding and by the physiological activity of rice plant at tillering, flowering and maturity stages. The effect of subsurface drainage on the above microbial dynamics and activity and the related consequence on rice production highlighted the highest rice yields for drained microplots. Although important concentrations of sulfides were recorded in the drained microplots, no deleterious effect was observed for rice development and rice yield. These findings suggested that the soil oxygenation through subsurface drainage might lead to chemical and microbial oxidation of toxic-sulfides to sulfate. Thus, an efficient oxygenation of soil by subsurface drainage may be a key factor of sulfides toxicity control in rice paddy field.

Acknowledgements

The authors would like to express profound gratitude to International Institute for Water and Environmental Engineering (2iE), CNRST/IRSS, General Direction Meteorology-Burkina Faso, International Foundation for Science, PACER-UEMOA/RABIOTECH, ISP-SUEDE/RABIOTECH, FCN-WAAPP and CNS-FL/WAAPP, for financial and technical supports.

Cite this paper

Cécile HarmonieOtoidobiga,AmadouKeita,HammaYacouba,Alfred S.Traore,DayériDianou, (2015) Dynamics and Activity of Sulfate-Reducing Bacterial Populations in Paddy Soil under Subsurface Drainage: Case Study of Kamboinse in Burkina Faso. Agricultural Sciences,06,1393-1403. doi: 10.4236/as.2015.611135

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NOTES

*Corresponding author.

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