In agricultural soils, SO
42− used by crop plants comes mainly from the contribution of fertilizers with sulfates, such as ammonium sulfate, gypsum, potassium sulfate, magnesium sulfate, single superphosphate, ammonium phosphate sulfate, potassium magnesium sulfate, and sulfates of micronutrients
[8][14], as well as the oxidation of S
0, and of S
2− contained in organic fertilizers. Another part of the S of crops is obtained from SO
42− and aerosols coming from precipitation, as well as the absorption by soil and plants of aerosols and gases such as H
2S, COS, and DMS. When S is added to the soil in the form of SO
42−, plants and aerobic prokaryotes absorb it and incorporate it into a reductive metabolism that produces sulfide (S
2−). On the other hand, when S is supplied as S
0 or in the form of organic fertilizers (S
2−), it must be oxidized to SO
42− by the action of soil prokaryotes to be available to plants
[2][6][8].
2. Transformations of Elemental Sulfur in Soil
The S available for plants in agricultural ecosystems is in dynamic storage (
Figure 2). It comes from gaseous forms and aerosols of S from the atmosphere, from dissolved S (mostly SO
42−) in rain and snow precipitation, and from SO
42−, which is obtained from the oxidation of S of soil organic matter and S
0. Sulfates can be fixed in the soil exchange matrix or leached to the subsoil
[10]. In arid regions, SO
42− can be stored in large quantities as gypsum in the subsoil, but in areas with higher water availability, leached SO
42− is mobilized to lower horizons and to the subsoil
[15].
Figure 2. Schematic representation of the flow of sulfur in soil. APS = adenosine 5′-phosphosulfate. Oxidation states of sulfur in the different molecules are: SO42− (+6); S2O62− (+5 and −2); S4O62− (+5 and −2); S3O62− (+5 and −2); SO32− (+4); SO2 (+4); S2O32− (+6 and −2); COS (+2); S0 (0); SH− (−2); S2− (−2); DMS (−2); CS2 (−2).
In the anoxic zones of the soil, S
0 and SO
42− are transformed to H
2S that is volatilized or is reoxidized to S
0 y and sulfate in the oxic zone. Plants and microorganisms take the SO
42− and reduce it to S
2− to incorporate it into a huge variety of organic compounds. Subsequently, these same plants and microorganisms transform a part of the sulfur to H
2S, DMS, and CS
2 [8][16]. The above volatile molecules have been associated with detoxification metabolism, stress tolerance, and signaling in plants and prokaryotes
[17][18]. As with iodine
[19], soil organic matter can transform the S to volatile forms by means of abiotic reactions, but the rate of transformation is very low in comparison with biotic metabolism of S
[16].
Since there are several access ways by which S can enter the agricultural ecosystem, it is not possible to mark a specific starting point. Therefore, arbitrarily, the assumption of an application of S0 to the soil is taken, and the transformations that this material experiences up to SO42− are described. Once in the form of SO42−, it is assimilated into plant cells in the form of myriad organic compounds. The final part of the flow of S from soil to plants ends with the production of volatile compounds by plant cells, or in the transformation of the S contained in plant waste (Figure 2).
S atoms tend to avoid double bonds, therefore, in the S
0, instead of forming molecules of S
2 (S=S) the S atoms are grouped in the form of cyclic allotropes (cyclosulfur) or as long chains Sn (catena sulfur)
[20]. The S
0 used to apply to soil consists mainly of molecules of S
8 (cycloocta-S) that are grouped, forming polymers of variable size; S
8 is the most stable form from a thermodynamic point of view. S
8 is a very electrophilic Lewis acid, so it reacts with nucleophilic anions or Lewis bases such as OH
−, sulfides (S
2−), thiols (R-SH), thiolates (RS
−), I
−, CN
−, and SO
32− [21][22].
S
0 is applied to the soil or substrate in quantities ranging from 20 to 250 kg ha
−1 yr
−1, the last figure being equivalent to 200 mg S
0 kg
−1 soil. Once in the soil or substrate, S
0 begins to transform into other chemical forms, mainly through biotic processes, and, to a lesser extent, by abiotic processes. The transformation rate is inversely proportional to the particle size and directly proportional to the temperature (Q
10 = 4.0), humidity availability, and abundance of edaphic microorganisms
[8][23][24].
Any factor that decreases bacterial activity, such as temperatures <10 °C or >40 °C and lack of humidity in the soil, will reduce the transformation of S. Flooded or compact soils will have anoxic conditions that induce high rates of conversion of S
0 and SO
42− into gaseous forms of sulfur
[8][24]. The metabolism of S in soils can modify other processes, as in rice paddies, where the use of gypsum amendment has been shown to decrease greenhouse methane emissions
[25]. In alkaline soils, it has been observed that the use of S
0 induces acidification (by H
2SO
4), which increases the bioavailability of elements such as P
[26].
When it is desired that S
0 produces SO
42− rapidly available for crops, an S
0 source with a small particle size (<150 μm or 100 mesh) should be chosen. Contrarily, if a long-term impact (two or more consecutive crops) is sought, it is desirable to use S
0 sources with a larger particle diameter, or even granular forms such as S
0 prills or S
0-fortified N-P-K and DAP fertilizers
[27][28]. At a temperature of 14 °C, it was found that, in 51 weeks, 51% of S
0 with particle diameter 41 μm (300 mesh) was oxidized, compared to 18% of S
0 with 125 μm (120 mesh). In soils with low temperatures, S
0 sized 41 μm will oxidize at a rate equivalent to S
0 sized 125 μm in soils with higher temperatures
[23]. In another experiment, applying 50 kg ha
−1 of S
0, it was found that 80–90% of S
0 with particles <150 μm was oxidized over a period of 340 days
[29].
On the other hand, it has been found that repeated applications of S
0 to soil increase the population and the activity of oxidizing bacteria of S
0 [24]. Accompanying the increase in S
0 oxidant bacteria was a reduction in the number of fungi and protists, while bacterial and actinomycete populations remained stable
[30]. Other authors reported a decrease in biomass and bacterial metabolism by applying S
0 annually for five years
[31].
When S
0 is in micronized form (<177 μm, <80 mesh) it is used for the control of mites and some fungi
[32][33]. The reactivity of micronized S
0 is a consequence of the high quotient surface/volume of the particles, estimated to be 1300 to 1940 cm
2 g
−1 for S
0 of 125 and 41 μm, respectively
[23]. Micronized S
0 can be applied through the foliar route or even by using pressurized irrigation systems to incorporate it into the soil
[34][35]. When applied by irrigation system, the problems associated with the application of micronized S
0 (because it is a flammable and irritant material) by dusting machines are reduced
[24].
The use of S nanoparticles for the control of pathogens in plants has also been described
[36][37]. Taking into account the high value of the surface/volume ratio of S nanoparticles, furthermore being a source of S for rapid assimilation by plants and microorganisms, it is possible that they function as biostimulants
[38], and that they provide highly reactive S
0 that works as a tolerance-inducing factor against pathogenic fungi
[32][39].
To be available for plants, S
0 applied to the soil or substrate must be oxidized to SO
42−. The change in the oxidation state of sulfur from 0 to +6 allows reduction equivalents to be obtained (8H
+ + 6e
−). The oxidation is carried out by most soil microorganisms, highlighting
Thiobacillus,
Beggiatoa,
Desulfomicrobium, and
Desulfovibrio, as well as other heterotrophic aerobics S-oxidizing bacteria such as
Bacillus,
Pseudomonas, and
Arthrobacter [2][40]. Two metabolic pathways have been described that allow the oxidation of inorganic S to SO
42−: the Kelly–Friedrich pathway, which does not involve the production of intermediates such as polythionates, and the Kelly–Trudinger pathway, which includes as an intermediate output tetrathionate (S
4O
62−) and other polythionates
[16]. The existence of two different routes and the large number of taxa that carry out the oxidation of S
0 allow a high redundancy, and capacity to tolerate extensive changes in pH and salinity in soils
[41][42].
In
Figure 2, the oxidation activity from S
0 to SO
42− is presented on the right side, and shows the Kelly–Trudinger pathway with the production of polythionates such as S
4O
62− and S
3O
62− (as well as S
2O
32− and SO
32−), which serve as a source of reducing potential and possibly act as inducers of stress tolerance in plants, perhaps by containing a single sulfane sulfur not associated with oxygen
[16].
Under anoxic conditions, S
0 is produced as part of the dissimilatory reduction of SO
42−. Later, the S
0 can be assimilated into S
2− that will be part of the biomolecules, or it will be volatilized in the case of excess S (see the central section of
Figure 2). At the left and right ends of
Figure 2, in the central part, the SO
42− from fertilizers, precipitation, and mineralization of organic matter is represented. A portion of this SO
42− forms a soil adsorbed sulfate storage, which will be in dynamic equilibrium with SO
42− dissolved in the soil solution. Under oxic conditions, SO
42− is assimilated in S
2− by assimilatory reduction and then transformed back into SO
42− during the organic decay and mineralization of organic matter
[42].
As part of the processes of organic decay, mineralization of organic matter, and sulfate reduction, both the soil, through abiotic reactions, and micro-organisms and plants can be source or sink of volatile forms of S, such as H
2S, DMS, COS, CS
2, and SO
2 (
Figure 2). Generally, under anoxic conditions, the oxidized forms of S are reduced by the soil microbiome to H
2S, CS
2, COS, DMDS, methyl mercaptan, and COS
[8]. These gaseous molecules are believed to be part of a mechanism of dissipation of excess S, although participation in other processes is not ruled out
[16][43].
In terms of reductive and oxidative microbial reactions, the most abundant forms of sulfur in the soil and the edaphic microbiome are S
2−, R-SH, RSSH, polysulfides (RS
n2−), S
2O
32−, SO
32−, SO
42− and polythionates
[16]. SO
42− applied as fertilizer or obtained through the processes described above is the form of S that plants assimilate through their roots
[40].
At best growth conditions, a plant’s sulfur requirement ranges from 2 to 10 μmol g
−1 plant fresh weight day
−1 [1]. As the flow of S is a dynamic process where the ecosystem receives S from the atmosphere, precipitation, subsoil water, and fertilizers, and loses S through the process of volatilization of S by soil and plants and by leaching, it is difficult to estimate the actual amount of S that a plant surface absorbs, assimilates, leaches, and volatilizes. As an exercise, let us suppose a single sampling point for a field of maize, for example before the harvest. In one hectare, there may be 78,000 kg of fresh weight ha
−1, which would be equivalent to 25 kg of sulfur contained in the plants. However, the 25 kg ha
−1 accumulated in the plant tissues at that specific sampling time does not include the S volatilized by the plant itself, or that leached, assimilated, or volatilized in the soil and by the microorganisms.
The point to highlight with the data of the previous paragraph is that the S of the soil is in constant exchange and extraction by the crops, atmosphere, and soil water. Therefore, a continuous supply of S is required, which is recommended to be applied in the form of S0 (40–60 kg ha−1) every one or two years, to maintain the edaphic store.