Progress on the amendment in biochars and its effects on the soil-plant-micro-organism-biochar system

Loissi Kalakodio 1 , Moussa Bakayoko 2 , Adiara Kalagodio 3 , Bodjui Olivier Abo 2 , Jean Pierre Muhoza 2  and El Moctar Ismaila 4
  • 1 University of Science and Technology, School of Energy and Environmental Engineering, Beijing Key Laboratory of Resource-Oriented Treatment of Industrial Pollutants, Xueyuan 30, Beijing 100083, China
  • 2 University of Science and Technology, School of Energy and Environmental Engineering, Beijing Key Laboratory of Resource-Oriented Treatment of Industrial Pollutants, Beijing, China
  • 3 School of Natural Science, Wuhan University Technology, Wuhan, Hubei, China
  • 4 Beijing Institute of Technology, Energy of Environment Materials, Beijing, China
Loissi Kalakodio
  • Corresponding author
  • University of Science and Technology, School of Energy and Environmental Engineering, Beijing Key Laboratory of Resource-Oriented Treatment of Industrial Pollutants, Xueyuan 30, Beijing 100083, China
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, Moussa Bakayoko
  • University of Science and Technology, School of Energy and Environmental Engineering, Beijing Key Laboratory of Resource-Oriented Treatment of Industrial Pollutants, Beijing, China
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, Adiara Kalagodio, Bodjui Olivier Abo
  • University of Science and Technology, School of Energy and Environmental Engineering, Beijing Key Laboratory of Resource-Oriented Treatment of Industrial Pollutants, Beijing, China
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, Jean Pierre Muhoza
  • University of Science and Technology, School of Energy and Environmental Engineering, Beijing Key Laboratory of Resource-Oriented Treatment of Industrial Pollutants, Beijing, China
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and El Moctar Ismaila

Abstract

Biochar, coal produced by pyrolysis and used as an amendment, has several advantages and has proven to be a promising avenue for sustainable agriculture. However, the current manufacturing methods, the conditions of pyrolysis and the biomasses used produce biochars of very variable qualities which can differently affect the productivity of the ground and the outputs of plants. Currently, no study makes it possible to elucidate the influence of the physicochemical properties of the biochars on the structure and the microbial diversity of the soil. The aim of this review was to understand how the physicochemical properties of a biochar affect its capacity: to reduce the emissions of greenhouse gases; to improve the growth of hothouse plants; to improve the effectiveness of the use of manures and water; and to modify the structure and the diversity of the bacterial communities in a horticultural substrate and a mineral soil. These biochars were produced under various conditions. The analyses show that the addition of biochar can stimulate certain groups of bacteria involved in carbon and nitrogen cycles and possibly those involved in the development of plants. This review identifies the important physicochemical properties of the biochars, which will be able to better guide agricultural producers and industries manufacturing substrates containing peat, in the choice of a biochar favorable to the growth of plants and a more durable agriculture.

Introduction

In the center of Amazonia where one finds jejune lands there are localized areas where the soil has an exceptional fertility and where there is much microbiological activity. These are called black cotton soils “Terra Preta” (Indigo C) and they are particularly rich in carbonic compounds and minerals. They have three times more organic matter (nitrogen, phosphorus and calcium) and 70 times more carbon than the soils of the neighboring areas (1), (2). These soils would have been formed several 1000 of years ago starting from carbonized residues (coal), and from excrement, bone and organic residues resulting from semi-intensive breeding of livestock (1), (2). After several decades, this kind of ground, which was very poor in the beginning evolved and became very interesting for the agriculture of today due to the stability of carbon present (1). The aromatic groupings of the poly-digests found in the structure of the coal in the ground of Terra Preta would mostly explain this biochemical stability and consequently the weak release out of CO2 (3). Recent studies show that very fertile soils, following the application of pyrolyzed coal (biochar), were structurally comparable with those of the soil of Terra Preta (4). The stability of carbon in Amazonian soil, the negative assessments of the CO2 emissions and the positive effect of carbon on the growth of plants attracted the interest of many researchers. Several studies show that biochar has properties which make it possible to increase the health and the growth of the plants, and the productivity of the soli, but which are also essential tools allowing the sequestration of lasting carbon in soil for many years (2), (5), (6), (7), (8). Moreover, many studies carried out during the last decade on the use of the biochar as an amendment show that it has several biological and physicochemical advantages and that it has proven to be a promising avenue for sustainable agriculture. However, the current manufacturing methods, the conditions of pyrolysis and the biomasses which have been used to produce biochars of very different qualities, have following their use, affected in variable ways the productivity of the soil and the outputs of plants (9), (10), (11), (12). This article thus aims to understand how the physicochemical properties of a biochar affect the productivity of the soil, the activity and the composition of the microbial communities and the growth of plants. Finally, this study will provide useful information for the development of industrial methods for producting biochars of good quality, while varying the temperature of pyrolysis and by employing various biomasses. We analyzed the factors influencing the properties of a biochar on the physicochemical and biological properties of the soil, on the emissions of greenhouse gases and on the growth of plants. This allows for the development of general knowledge and hypotheses and objectives to highlight some of the essential physicochemical properties of biochar to improve soil productivity, mitigate greenhouse gas emissions and promote plant growth and microbial diversity.

Formation of the biochar

Description

Biochar is the solid part produced by pyrolysis, the process of degradation of an organic biomass by heat in the absence of oxygen. Different biochars exist, and depend on the equipment used and the temperature of pyrolysis (13). The organic biomasses used to form the biochar are from vegetables or animals and are as rich in carbon as wood; crop waste products; the excrements of animals and organic waste. During the degradation of the biomass, three phases are generated by pyrolysis; a solid part (biochar), an organic liquid part (bio-oil) and a gas part. The quantity of each component (gas, liquid and biochar) is different according to the method of pyrolysis used. Several systems of pyrolysis exist. The most used systems are fast and slow pyrolyzers (14), (15). A system of rapid pyrolysis will very quickly heat (above 1000°C s−1) the dry biomass in the absence of oxygen and the time in the system is very short (approximately 2 s). The aim of a rapid pyrolysis is to maximize the production of the bio-oil. For this reason, the heating is very fast and of short duration. With regard to the traditional system (slow pyrolysis), the dry biomass is heated very slowly (1°C with 20°C min−1) in the absence of oxygen and with a time in the system varying from a few hours to a few days (16) (Figure 1).

Figure 1:
Figure 1:

Waste recycling and soil remediation.

Citation: Reviews on Environmental Health 33, 3; 10.1515/reveh-2018-0007

Biochar as an input

Biochar results from the pyrolysis of organic residues. Pyrolysis consists in transforming, under conditions very low in oxygen and under temperatures varying between 350 and 700°C, the organic matter in a porous matter of low density and rich in carbon. Most biochars are alkaline (pH >7). Their characteristics are determined by the nature of the matter and the temperature of pyrolysis (17), (18), (19), (20). The pyrolyzed materials can come from biomass forest, agricultural, urban or even industrial sources (5).

Several studies have indicated that there are many advantages to incorporating biochar in the soil. Among these advantages, one can enumerate the improvement of the structure and several parameters which result from this; the reduction in the apparent bulk density, the increase in the availability of the nutrients, the cation exchange capacity (CEC) of the water holding capacity and pH (21). The improvement of the structure could be due to the interaction between the biochar, the organic matter, the minerals and the micro-organisms. This interaction would stimulate the formation of microphone-aggregates. These microphone-aggregates influence, in their turn, other parameters of the substrate such as the infiltration, the retention of water and ventilation. Hydrous erosion and the loss of nutrients are decreased in the structured soils, i.e. having a stronger infiltration (22), (23).

These physical improvements of the medium have a significant impact on the growth of the plants as the root penetration, the availability of air and water in the root zone depends on it (24). Also, several biochars have the capacity to adsorb nutrients (exchangeable cations) by the increase in the pH of the substrate, coupled with the increase in the heat-transferring surface. The biochar could also reduce the biodisponibility of metals by chemically binding them because of their loads and their specific surface, but also because of their effect on the pH (21), (22), (24). Indeed, the majority of heavy metals are toxic when they are in a soluble form and this solubility depends on the pH. Generally, the lower the pH is the greater the concentration of heavy metals is, this is greater when the pH of the ground goes down to 5.5 (25), (26), (27). At this stage, the vegetable growth is affected by the toxicity of metals and the fixing of nitrogen by the bacteria is reduced (28). This aspect is very interesting for contaminated sites on which it can be detrimental to see the contaminants accumulating in the vegetable biomass (29), (30).

Except for its indirect role on the availability of the nutrients and metals played by its capacity for sorption, the biochar could also constitute a direct contribution of nutrients (C, P, K and micronutrients) according to the nature of the transformed organic matter and the method of pyrolysis.

However, the effects of the incorporation of biochar on the ground on the vegetable growth remains very variable, inter alia because of the nature of the receiving grounds and the climate (31), (32). Despite everything, Ding et al. (10) concluded that there exists a significant benefit with the application of biochar and that the best results were observed in the acid and neutral grounds with pH and in coarse or average soil. This suggests that, in addition to the named properties, several important mechanisms for vegetable growth would be improved by the introduction of the biochar, that is to say, the liming effect and the retention of water.

By its influence on the environment in which it is incorporated, the biochar could thus be an extremely interesting material in the restoration of mining sites, in particular, by its effect on the pH and the retention of water. Wardle et al. (29) characterized four substrates obtained after mixing mining residues with biochar at a rate of 0, 1.5 and 10% of biochar and affirm that the pH, the CEC and the water holding capacity increased with the rate of biochar. Bagreev et al. (33) for their part, used a mixture of biochar and compost which they incorporated in waste from a copper mine at a rate of 20, 40, 80 and 100%. They conclude that this mixture increases the pH, the concentration of C and N total, but decreases the biodisponibility of Co, Cu and Ni. In addition, the maintenance and the follow-up of the mining sites after their closing represent a large amount of work. It is thus desirable that the materials used in the restoration have a long-term effect. As the biochar is a material which include a large amount of highly recalcitrant material with microbial degradation (34), its effect is prolonged in time.

The ratio to which the biochar must be built-in on the ground varies from one study to another. In the scientific literature, one finds studies whose treatments go from 1% to 40% volume (18), (19). As biochar is expensive in comparison with of MRF which is often free, various amounts, up to volume 40% should be tested in order to determine the best growth rate of vegetation according to the cost generated by the purchase of biochar.

Physicochemical properties of a biochar

The raw material, the temperature, the speed of rise in the temperature, the warming-up time and the size of the particles can affect the physicochemical properties and the quality of a biochar (5), (13), (35) Table 1. Among the physicochemical properties which distinguish a biochar, there are porosity, specific surface, water holding capacity, contents in biogenic salts and organic materials, the CEC and the pH.

Table 1:

Adsorption characteristics of various pollutants with biomass.

FeedstockPyrolytic T°Residence time, hPyrolysis techniquepHBiochar size, mmElemental compositionCECBET surface area, m21Microspore volume, cm3 g−1Absorbed pollutantsqmax, mg g−1References
CHON
Coffee husk3501Slow pyrolysis6914.8192Phenol (94)3.88(36)
Sugarcane bagasse450Slow pyrolysis80.281.81.615.11.5186.00.342Sulfamethoxazole Hg(II)13(37)
Miscanthus sacchari-florus4002Slow pyrolysis11.6–12.32.068.4–74.84.8–1.619.8–13.42.0–1.7428.00.403Purple methyl11.99±1.02(38)
Sugar beet tailing6002Slow pyrolysis80.2756.415.61.3Cr(VI)123(39)
Soybean stover3003Slow pyrolysis7.31.068.84.325.01.95.60.010Trichloroethylene12.48(40)
Wastewater sludges5501Slow pyrolysis871.18Fluoroquinolone antibiotics19.8(37)
Hardwood450<5 sFast pyrolysis5<1.585.61.37.80.4Copper and zinc6.79(41)
Cattle manure100–7006Slow pyrolysis90.235.3–20.61.4–0.529.1–5.41.5–1.2Aluminum(42)
Chicken litter6001Slow pyrolysis37.155.3334.673.130.1Dimethyl sulfide(43)
Apple branch400–80010.07.0–100.570.2–84.84.1–0.620.6–5.80.8–0.311.9–545.4−0.512Pb17.7–19.2(44)
Corncob3001Slow pyrolysis8.10.267.2127.630.67100.014Methylene blue dye(45)
Cacao shell3501Slow pyrolysis10.42701.437Al(46)
Paddy straw500Slow pyrolysis10.50.386.283.2595.5Methylene blue9.8(47)
Wheat straw500Slow pyrolysis10.274.402.8314.260.4714.20.02Cr(VI)23.6(44)

Physical properties

Porosity

During the formation of the biochar, the temperature of selected pyrolysis influences porosity (16). It has been observed that the biochars produced between 350°C and 400°C have a higher total porosity than those produced at 300°C. Also, (33) showed that a temperature of pyrolysis between 400°C and 600°C the porosity of the biochar was considerably increased. The increase in the pores would be created by an increase in water molecules slackened following the action of the hydroxylation at high temperatures (33). Also, the residence time of the biomass in the pyrolyzer could have an impact on the porosity of the biochar (48).

Surface specific

The specific surface of an adsorbent is by definition, a surface per unit of mass (m2 g−1). This surface is created primarily by the microphone and mesopores. The greater the specific surface area the higher the contact surface and the greater the amount of adsorbed material. This parameter is obtained by applying the theory of Brunauer, Emmett and Teller (7). According to the literature, the specific surface of the biochars varies a lot according to the temperature and the conditions of pyrolysis. It was shown that a biochar of wheat straw produced beginning with a slow pyrolysis (6°C min−1, final temperature, 525°C and maintained during 2 h) had a weaker surface specific (0.6 m2 g−1) compared to the production of this biochar starting from a rapid pyrolysis (250 with 1000°C s−1, final temperature, 525°C and maintained during a few seconds, 1.6 m2 g−1) (15). Novak et al. (48) determined that the more the temperature increases, the more the specific surface rises and the great the increase in the ash content. Also, specific surface is influenced by the nature of the biomass used. For a given temperature (between 400°C and 450°C), of the biochars manufactured from pine wood, the manure of poultry and corn stems had a specific surface lower than 50 m2 g−1, while a wood biochar of alder had a specific surface ranging between 350 m2 g−1 and 400 m2 g−1 and that of hazelnut shells had a specific surface higher than 500 m2 g−1. In general, the biochars from wood products have a specific surface higher than 400 m2 g−1 (24). According to the study of Schimmelpfennig and Glaser (7), a biochar having a specific surface higher than 100 m2 g−1 would be beneficial in the improvement of the fertility of the soil and would allow the sequestration of carbon.

Water holding capacity

The O:C report of a biochar would be a potential indicator to determine its absorbent character and its polarity. Normally, when the temperature of pyrolysis increases, the biochar has a low oxygen content and thus a very weak O:C. According to a study of (49) the increase in the temperature of pyrolysis can decrease the polarity on the surface of the biochar resulting in a reductio n in its water holding capacity. However, (50) observed a weak difference in the hydrophobicity of three biochars pyrolyzed between 400°C with 600°C.

Chemical properties

Mineral composition

According to the literature, the composition and the availability of the biogenic salts of the biochars varies greatly. The raw material and the conditions of pyrolysis would be the source of this variation (10). Chan and Xu (51) observed a great variation in the phosphorus contents according to the biomass and the conditions of pyrolysis used. As regards the nitrogen contents, this one tends to be weaker in the biochar when the temperature of the pyrolysis increases. Moreover, it was reported that when the temperature of pyrolysis reached 500°C, more than half of the contents of the nitrogen and sulfur of the biomass can be lost (33), (52). The reduction of nitrogen could be caused by a loss of volatile organic compounds during pyrolysis. The increase in the temperature of pyrolysis can support the larger matter release trapped in the biochar (16), (33). The biomass used during pyrolysis can have an effect on the concentration of biogenic salts found in the biochar (53). Generally, the contents in biogenic salts seem to be higher in the biochars of animal origin, food waste and corn than in the biochars of forest products (pine, oak and walnut) (54). Moreover, Chan and Xu (51) noted that the concentrations cogitate some and that nitrogen was higher in the biochars produced starting from litters of animals than in the biochars of vegetable biomasses. As regards carbon, Antal and Grønli (55) mention that the carbon contents in the biochar vary according to the type of biomass. A biochar whose raw material comes from hardwood has more carbon compared to the residues of cultures or poultry manure.

Production of toxic compounds

The type of biomass and the temperature of pyrolysis affect the concentration of polycyclic aromatic hydrocarbons (HAPs) and of dioxin in the biochar (7). Moreover, the conditions of pyrolysis can also influence the concentration of HAPs (56). During pyrolysis, the organic compounds contained in the biomass are partially fragmented into smaller unstable compounds. These fragments are composed of highly reactive free radicals which combine to form a new more stable compound by recombination reactions and form HAPs (57).

According to (58) the dioxin would be primarily formed when the temperature of pyrolysis is between 200°C and 400°C. In the case of HAPs (19), reports that a biomass pyrolyzed at temperatures higher than 700°C generates a strong concentration of HAP. Concerning the study of (57), a weak concentration of HAP was observed in the biochars produced at temperatures of pyrolysis varying between 500°C and 600°C. Given variability, (7) recommend a content of HAPs weaker than that found normally in the ground.

Cation exchange capacity (CEC)

It has been established that the lower the temperature of pyrolysis the lower the CEC and vice versa (59). Moreover, the amendment with a biochar having a high specific surface can support more the CEC of the soil (60).

The CEC of the biochar is allotted partly to an increase in the oxygenation of the functional groupings found on the surface of the biochar (61). These various functional groups which interact with the medium are the groupings: pyrans, phenolic, carboxylic, lactones and the amines (62). These groups can act on the aggregation of the particles of the soil, on the dissolved organic matter and the transport of gases and water (63). According to certain research, the oxidation of the surface of the biochar would lead to a larger CEC per unit of carbon in the ground (4), (60). However, the addition of biochar can also have a null effect on the CEC of the ground and that could depend on the type of biomass used. For example, Novak et al. (64) report that the amendment with a biochar of pecan shells pyrolyzed with 700°C did not have any effect on the CEC of soil incubated over 67 days.

Mineralization and sequestration of carbon

With high temperatures during pyrolysis, aliphatic carbon is converted into aromatic carbon. For example, when the temperature of pyrolysis increases 150°C with 550°C, the groupings OH and CH3 of the organic matter decrease and double linking C=C increases. Moreover, the ratios H:C and O:C of the biochar decrease when the temperature of pyrolysis increases. In general, biochars produced with high temperatures, between 500°C with 700°C, are well carbonized and stable. These biochars have a small ratio H:C (<0.1) and a specific large surface. On the contrary, biochars produced at low temperatures (300°C and 400°C) are partially carbonized and less stable. In this case, the ratio H:C and the concentration of oxygen are high and the biochar has a weak specific surface. The presence of aromatic groupings generates a reduction in the rate of mineralization of carbon and consequently, a reduction of the availability of the nutrients such as nitrogen, phosphorus and sulfur (34), (51), (65).

Some biochars can be very recalcitrant, such as those having a strong proportion of carbon with condensed aromatic structures. The recalcitrant nature of the biochar can be interesting if the main aim is to sequester carbon. On the other hand, if the objective is to improve the fertility of the soil and to also increase the sequestration of carbon, the structure of the biochar must be more oxidizable and have a small ratio of C:NR (64). If the biochar is used as amendment, Schimmelpfennig and Glaser (7) recommend having a biochar with a ratio O:C<0.4, a ratio H:C<0.6 and one contents out of C total >15%.

pH and electric conductivity

The temperature of pyrolysis can influence the pH of the biochar. For example, Novak et al. (48), observed that a biochar produced with a high temperature (700°C) had a more raised pH compared to a biochar produced at a low temperature (250°C). Another study showed an increase of 2 units of pH between the biochars produced at temperatures of 300°C and 600°C (54). The increase in the temperature of pyrolysis can support the production of ash and an increase in the contents of basic cations (Na+, K+, Mg2+ and Ca2+) which are directly correlated with the pH of the biochar (66). The selected raw material can also vary the pH of the biochar; energy of pH=4 with pH=12 (59), (61), (67). A biochar produced from wood, has a pH higher in general than a biochar produced from residues of cultures, because its contents of Ca2+ are higher (66). However, a recent review literature report showed no effect of the lignin contents on the pH of the biochar (10). Rather, the pH of the biochar is proportional with the temperature of pyrolysis suitable for each vegetable biomass. In addition, the method of pyrolysis (fast or slow) can influence the pH of the biochar. Bruun et al. (15), observed that a biochar produced from wheat straw and slowly pyrolyzed (speed of 6°C min−1; maximum temperature of 525°C maintained during 2 h) had a higher pH (pH=10.1) than a quickly pyrolyzed biochar (pH=6.8; pyrolysis uninterrupted with a time of residence of a few seconds; speed of 250 with 1000°C s−1).

Compared to electric conductivity (EC), this seems to vary more according to type of biomass than temperature of the pyrolysis (54). For example, the EC in biochars of animal origin (cattle and poultry) and corn presented in the study of Rajkovich et al. (54), were not influenced with the increase in the temperature of pyrolysis, going from 300 to 600°C. By excluding the food residues and pulp and paper residues, the EC of the biochars in the study of Rajkovich et al. (54), are generally higher in the biochars of animal origin (200–500 ms · m−1) that those of vegetable origin (3.8–203 ms · m−1). Singh et al. (66) mention that the salt contents of original equipment influence the CEC of the biochar.

Effects of the biochar on the physicochemical properties of the soil

According to the literature, an amendment in the biochar can improve the physics of the properties of the soil, such as the apparent bulk density, porosity, the water holding capacity, the stability and the formation of aggregates (10). However, divergent effects have been reported. For example, Watts et al. (68) did not observe any improvement of the aggregation of their clay soil amended in biochar, without additional organic matter contribution. According to (69), it is possible that aggregation is only possible when there is interaction between the organic matter and the activity of the micro-organisms. In addition, Cheng et al. (61) mention that the effect of the biochar on the aggregation of the soil is related to its CEC and the pH of the ground. As it is the case with clays, a high CEC can support the aggregation of the ground.

As regards the chemical properties, a meta-analysis of 371 independent studies reports that the addition of biochar to the soil allows for an increase in the nitrogen content, phosphorus, potassium and that of total carbon (70), (71). Moreover, the contribution of a biochar in an acid ground tends to increase the pH, the EC and the CEC (72). The liming potential of the biochar can be allotted to its high basic cations content which can improve the availability of the nutrients essential for the plant to grow in acid ground. However, that will depend on the amount applied and the chemical composition of the biochar (72).

The soil type could influence the beneficial effects of the biochar (73). The results achieved after the application of 10 T ha−1 of a biochar manufactured from the waste of pastes and papers on a ferrous ground made it possible to improve the quality of the soil and the output of the cultures. On the other hand, the application of this biochar on calcareous soil presented negative effects, in particular, in the presence of manure. The liming power of the biochar coming from the waste pastes and papers would be very beneficial in acid soils, where the very high aluminum concentration limits the growth of the plant. On the other hand, the liming power of the biochar would be less beneficial for limestone soil (74). Some alkaline biochars can contain a strong salt concentration and influence the salinity of the limestone soil are are able to harm the growth of plants and the microbial activity (74), (75).

Effects of a biochar on the emissions of greenhouse gases

The principal physicochemical properties of the biochar implied in the attenuation of the CO2 emissions of the ground are: its water holding capacity and carbon retention capacity, its porosity, the stability of carbon and its contents in compounds toxic (32), (76), (77), (78), (79). For example, the increase in the contents of the easily degradable carbon soil (unstable carbon), following the addition of a biochar, can support the microbial activity and contribute to the CO2 emissions (34).

There exists three fractions of unstable carbon: mineral carbon (soluble with water); organic carbon (soluble with water and quickly mineralized by micro-organisms); and the hardly oxidizable form of carbon from the amorphous or microcrystalline part of the biochar structure. The unstable carbon of the biochar is defined as being the fraction mineralized out of CO2 during one short period. This mineralization would be caused by abiotic or biotic effects. The mineralization of the biochar generally comprises two phases: the fast mineralization followed by a slow mineralization.

According to a test of incubation, the fast phase of mineralization appears in the 1st week or the first months, following the application of a biochar in the soil (63). The exhaustion of unstable carbon generates, thereafter, a reduction in the CO2 emissions in the soil amended by the biochar (79), (80).

As regards the emissions in CH4, it has been observed in the literature that soil amended with biochar emitted concentrations that were very varied according to the type of biochar and the soil type (12), (19), (80). The emissions in CH4 will depend on the presence of easily decomposable organic matter, the water content of the ground and the redox potential. Moreover, a high concentration of potassium in the biochar can promote the activity of methanotrophic microorganisms and inhibit those involved in methanogenesis (5), (81), (82). According to the literature, the emissions in N2O appear to be decreased following the amendment in the biochar. Several biotic mechanisms implied in the attenuation of the N2O in soil amended by biochars have been proposed (83), (84), (85). Among these mechanisms, if there is: (I) an increase in the ventilation of the soil by inhibiting the process of denitrification by the presence of oxygen; (II) an unstable carbon content of the biochar supporting the complete denitrification of nitrogen (N2 formation); (iii) an increase in the pH by the biochar creating an optimal environment for the activity of the N2O reductase where this contributes to the formation of N2; (iv) a reduction of the availability of inorganic nitrogen to the micro-organisms implied in nitrification and/or the denitrification which produces the N2O; and (v) a relaxation of toxic compounds inhibiting the biological activity of the soil. Abiotic mechanisms were also proposed in the attenuation of the emissions of N2O in the soil amended by the biochar (84). There is the chemical denitrification which refers to abiotic chemical reactions which lead to the nitric oxide formation (NO), N2O and of N2. Among these reactions, there is the chemical decomposition of: (I) hydroxylamine (NH2OH); (II) of the NO2; and (III) of ammonium nitrate (NH4NO3) in the presence of light, of moisture and a reactive surface. Another plausible abiotic mechanism is the adsorption of the N2O on the surface of the biochar due to the presence of manganese and copper, iron hydroquinone. In addition, Cayuela et al. (86) mention that a biochar could possibly act as an electron shuttle transporter promoting the transport of electrons to microorganisms competing with the denitrating microorganisms, thus reducing N2O emissions.

Effects of a biochar on the growth of plants

The amendment in biochar can have a beneficial effect on the growth of plants (70). For example, Graber et al. (87) studied the contribution of a biochar made from lemon trees (1, 3 and 5% m/m) on the growth of tomato and sweet pepper in coconut fibre. According to their results, the growth of tomato and sweet pepper were significantly higher in the substrates amended by the biochar than in the substrate without amendment. Another study showed a beneficial effect on the growth of tomato and sweet pepper following an amendment in biochar in a sandy soil (88). On the other hand, no significant effect on the growth of the plant between the two amounts of applications of biochar (1 and 3% m/m) was observed. With regard to the study Vaughn et al. (89), divergent effects were observed on the growth of the seedlings of tomato and marigold amended with an amount of 5.10 or 15% (v/v) of biochar of wood or straw.

Although an amendment of biochar can have positive effects, this can also cause neutral effects and even vermin with the growth of the plant. This can to depend on the physicochemical properties of the biochar (19). This occurs in the case of the biochars manufactured from poultry manure. These biochars generally have a strong sodium concentration. According to a study carried out by Revell et al. (6), the application of 2.5% (m/m) of biochar, manufactured from poultry manure, had a soluble salt concentration (1.2 DS M−1) very high. They note that the salt concentration was too high for the growth of sweet pepper. Rajkovich et al. (54) also measured the concentration of sodium in the biochars of poultry manure, but also in those of cattle and waste pastes and papers.

This raised concentration of salts would also explain the reduction of the growth of corn in their study. Lastly, Rajkovich et al. (54) mentioned that an application higher than 2% (m/m) (≈26 T ha−1) of biochar the growth did not improve the growth of corn. They mentioned that the effect of the biochar varies a lot with the soil type and the type of culture and that an interaction between the plant, the soil and the type of biochar is possible.

In addition, a recent study reports that the addition of 5% (m/m) of biochar (mixture of cotton and rice barks) in a sandy loam made it possible to reduce the contribution of water without affecting the outputs of a culture of the tomato (90). According to the authors of this study, the increase in soil retention capacity amended in biochar may have contributed to reducing the number of irrigations. However, divergent effects can appear and that will depend on the nutritional requirements, the type of cultivar and the stage of development of the plant (91).

Effects of a biochar on the biology of the soil

In most studies, it was shown that the microbial biomass had increased following the addition of biochar in the soil (11). Moreover, the contribution of the biochar would have created material changes in the composition of the microbial communities including the mycorrhizae and the activity of the enzymes (9), (11), (69). According to Anderson et al. (9), the addition of a biochar could potentially influence the growth of certain groups of micro-organisms implied in the cycle of nitrogen, carbon and phosphorus in the soil. Moreover, the biochar could have a positive impact on the composition of the microbial communities of the soil and could support certain species implied in the complete denitrification of the nitrogen (92), (93). However, few studies exist to date on the relations between the type of biochar and the diversity of the microbial populations in the ground (10), (11), (93).

Studies report that the amendment of a biochar can support the growth of certain groups of beneficial organizations in the growth of the plant (87), (94). For example, Graber et al. (87) observed an increase in Pseudomonas spp., Trichoderma spp. and of Bacillus spp. in the rhizosphere of a culture of sweet pepper amended in biochar compared to the substrate without an amendment. With regard to the study Kolton et al. (94), they observed divergent effects on the bacterial populations. According to their results, there was an increase of 12–30% of the bacteroidetes and a reduction of 71–47% of proteobacteria following the amendment in the biochar. For their part (88), noted an increase in the total bacterial population and Bacillus spp. following the increase from 1 to 3% (m/m) of biochar. On the other hand, there was no apparent effect on the development of the bacteria, such as Pseudomonas spp., and mushrooms, such as Actinomycetes spp. observed. Within the framework of another study, the amendment of biochar seems to have had a significant role in the induction of a systemic answer of the plant against pathogenic micro-organisms. Elad et al. (95) noted that the addition of biochar from wood of the lemon tree (1, 3 and 5% m/m) in a horticultural mixture of substrate and a sandy soil allowed a better resistance against two foliar pathogenic mushrooms (Botrytis cinerea and Leveillula taurica) for tomatoes and sweet peppers. However, a recent study reports that the addition of 50% (v/v) of biochar of pyrolyzed pine at475°C in an organic substrate supported the development of Pythium ultimum, a disease-causing agent, in various cultures of greenhouse plants (geranium, basil, lettuce and sweet pepper) (96). However, no visible negative effect on the plants was observed in their study. According to a recent review of the literature, the biochar could deteriorate the signals between the plant and the micro-organisms of the soil and modify the balance of the trophic micro chain of the soil supporting certain microbial species to the detriment of other organizations (10).

According to (97), the biochar can increase the effectiveness of the mushrooms Mycorhiziens arbusculaires to protect the roots of their plant host against the infections transmitted by pathogenic organisms. In certain cases, it was shown that the pores of the biochar could be used as a refuge for the bacteria and mushrooms in the ground. Through the size of its pores, the biochar can be used as a habitat for the micro-organisms (0.3–3.0 μm for the bacteria; 2–80 μm for mushrooms; and 7–30 μm for the protozoa) which protect them from the microarthropod predators of the soil (11), (69). However, the biodisponibility of certain biogenic salts such as carbon, nitrogen, phosphorus and sodium in the soil amended in biochar can negatively influence the microbial populations. Moreover, the release of toxic products found in the biochar could also play a significant role in the inhibition of the development of the micro-organisms in the soil (11), (69). Recently, the International Biochar Initiative (IBI) (98) established standards so that a biochar can be used as an amendment. The IBI (98) proposes limiting concentrations of hydrocarbon (HAPs, dioxin and ethylene) and in heavy metals so as not to harm the growth of the plant and the microflora of soils.

It is now known that the physicochemical properties of the biochars, such as sorption, the structure of the pores, specific surface, the pH and the mineral matter play a significant role in the biology of soil. However, few studies exist in the literature on the interactions between the biochar, the soil, the micro-organisms and the plant, simultaneously (10), (11). According to Lehmann et al. (99), this gap blocks the knowledge of the mechanisms by which the biochar influence micro-organisms of the soil, fauna and the rhizosphere. The recent arrival of new tools for sequencing at high-speed, has made it possible to more precisely analyze the composition of these microbial communities and the interactions between the various populations. These new tools represent an opportunity for better understanding the key actors of the biogeochemical cycles of micro-organisms, in order to answer the challenges posed in agriculture (100).

All in all, seeing the great variability of the results in the literature relating to the physicochemical properties of the biochars, more research is necessary to look more into our knowledge of the mechanisms and the interactions of the biochar with the soil, the micro-organisms and the plant. This research will make it possible to find biochars with qualities favorable to the productivity of the soil and the growth of plants. Moreover, this research will allow knowledge for companies and the farmers so that they can take part in more durable agriculture.

Conclusion

This review enables us to understand how the physicochemical properties of a biochar affect the productivity of the soil, the activity and the composition of the microbial communities and the growth of plants, as the nature of the biomass and the temperature of pyrolysis influence the physic chemical properties of the biochar.

In general, the addition of biochar makes it possible to attenuate the gas emissions for the greenhouse effect at the time of the study of incubation in absence of plants. However, we restate that the type of biochar can interact differently in the production of CO2, CH4 and of N2O according to the physicochemical properties of the soil. Moreover, the addition of a nitrogenized source or a carbonaceous source (compost) can influence the effectiveness of some biochars to attenuate the emissions out of CO2 and N2O in the ground. The high pH of the maple biochar pyrolyzed at 550°C limits the breathing of the ground and makes it possible to effectively reduce the N2, N2O. With regard to a biochar pyrolyzed at 700°C, its high power of water retention and the weak diffusion of gases towards the atmosphere in the clay soil support favorable conditions with the attenuation of the emission of CO2 and N2O.

The presence of a plant however, supports the mineralization of carbon and the production of CO2 (directly via root respiration or indirectly through root exudates), amended biochar, and indicates an interaction between the ground, the plant and the biochar.

An extremely interesting result observed in this review is that the addition of biochar in a substrate containing peat made it possible to maintain and to even increase the output of the plant, fertilized with only 50% of the recommended amount of nitrogen.

The analysis diverges however, according to the amount in the biochar, the type of biochar and the species of the plant. The medium richer in carbon in the amended substrates of maple biochars allows a positive interaction between the global development of the plant and the heterotrophic micro-organisms.

In addition, the analysis confirms that the amendment in a biochar has a divergent effect on the bacterial communities of the substrate and the clay soil.

The changes specific to the biochars at the level of the physicochemical properties of the ground carries out modifications distinct from the bacterial communities. The very alkaline pH of the biochars is a significant component in the modification of the bacterial populations. This modification seems to have beneficial effects on the development of plants and the attenuation of the emissions in N2O.

This review is thus very promising for the producers in who use greenhouses, because they will make it possible to reduce the manufacturing costs by minimizing the contributions of water and nutrients without affecting the output of the cultures in the presence of biochar. Moreover, this is very encouraging for them, because the results show that the addition of biochar limits not only the contributions by the nutrients, but also the losses in biogenic salts by scrubbing.

However, additional research is necessary to better understand the complexity of the interactions between the type of biochar and the microbial communities of the soil which are implied in the greenhouse gas attenuation, the increase in the outputs of the plant and the biogeochemical cycles of carbon and nitrogen, under various environmental conditions.

Moreover, the study of the capacity of biochars to adsorb carbon according to their porosity and the microbial activity of the soil would be fundamental when looking to improve our knowledge on the attenuation of CO2. In addition, the study of the carbonaceous compounds released in the amended soils of biochar would be required to have a better comprehension of the composition of carbon and microbial breathing.

Although the pH of the biochar plays a significant role in the attenuation of the emissions in N2O in the soil, its interaction with the micro-organisms which are implied in the cycle of nitrogen is still little understood. The analysis of the form of genes, the growth and the activity of the bacteria supporting the complete denitrification of nitrogen in the soil amended with biocharis essential. Moreover, the study of the abiotic and biotic mechanisms that the bacteria implied in the reduction of the N2O in soil amended in biochar is important. Lastly, other research, including long-term tests on various grounds amended with various biochars, are crucial to look further into our comprehension of the effect of the biochar on the microbial communities which are implied in the cycle of nitrogen and the emissions in N2O of soil. The amendment in biochar can support certain groups of bacteria which are implied in the stimulation of the growth and the development of the plant and act like biological fighting agents. However, the effect of the biochar on bacterial communities which are beneficial and pathogenic is still little known. Additional studies are therefore needed to determine the mechanisms associated with biochars such as the biochar’s ability to alter and to alter signals between the plant and soil microorganisms and biochar’s ability to alter the trophic soil micro chain balance.

In addition, the effect of biochar on the intimate tripartite association between certain beneficial bacteria, arbuscular mycorrhizal fungi, and the plant was not studied.

Additional studies are thus necessary to better understand the impact of the biochar on its organizations associated with the development with the plant. Moreover, studies are essential to establish a consortium of beneficial micro-organisms reducing the demands for mineral fertilizers and to contribute to a more durable agriculture.

The inoculation of various beneficial micro-organisms in various soils amended or not, in biochar and in the presence of various plants could bring about fundamental knowledge on the association between these micro-organisms and optimize the soil-plant-micro-organism-biochar system.

Therefore, it is essential to study the impact of the biochars on various stocks of micronizes and microbial diversity associated with influencing the growth of plants in agricultural soil with a weak phosphorus concentration.

In addition, a thorough study of the life cycle of the biochar is essential to evaluate its ecological footprint. Lastly, it would be interesting to evaluate the potential of various mixtures of biochars for the production of biological and conventional cultures in greenhouses and fields on the outputs of the plants, the improvement of diversity and abundance of the microbial communities and on the greenhouse gas attenuation. As the physicochemical properties of the biochars are very different, each one could bring beneficial effects to the growth of plants and the micro-organisms.

Acknowledgments

The authors gratefully acknowledge all laboratory and schools involved in this review.

Research funding: Authors state no funding involved.

Conflict of interest: Authors state no conflict of interest.

Informed consent: Informed consent is not applicable.

Ethical approval: The conducted research is not related to either human or animal use.

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