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The combined application of nitrogen and biochar reduced microbial carbon limitation in irrigated soils of West African urban horticulture



Intensive wastewater irrigated urban horticulture in sub-Saharan West Africa receives high nutrient inputs, which lead to large gaseous and leaching losses. The addition of biochar to the usually sandy soils may reduce these losses and improve the habitat conditions for soil microorganisms. Two similar experiments focused on crop yields and nutrient balances have been carried out over a 2-year period in semi-arid Ouagadougou, Burkina Faso, and in sub-humid Tamale, Ghana, representing to some extent different but typical locations in West Africa.


Biochar and N fertilization effects were measured on soil microbial biomass carbon (MBC), fungal ergosterol, and functional diversity, estimated by multi-substrate-induced respiration. It was additionally possible to study the effects of clean water irrigation on the respective microbial properties in Tamale soil.


Sole biochar addition did not affect any soil chemical or soil biological properties analyzed. In contrast, biochar application with N fertilization increased the mean respiratory response of the 11 substrates added by 23% in the Ouagadougou soil and by 13% in the Tamale soil. N fertilization decreased soil pH in both cities by 1.1 units. However, a pH-H2O of 4.7 led to reduced MBC and ergosterol contents at Tamale. Also, the Shannon index of the respiratory response was positively correlated with the soil pH. Clean water irrigation decreased the ergosterol content and increased the respiratory response to organic acids.


Biochar addition with N fertilization improved habitat conditions for soil microorganisms. An N fertilizer-induced decline in soil pH < 5 should be avoided, as it decreased MBC and microbial functional diversity.

Graphical Abstract


Sub-Saharan West African countries, such as Burkina Faso and Ghana, are exposed to increasing urbanization, accompanied by the expansion of urban agriculture [1, 2]. In contrast to rural agriculture, urban horticulture in sub-Saharan West African countries receives considerable organic inputs by mulching of harvest residues, fertilization with organic manures, and irrigation with wastewater [3,4,5]. Such intensively used systems lead to large gaseous and leaching losses of nutrients [4, 6]. The addition of biochar to soil may reduce these losses and the cultivation of square meters instead of hectares makes it possible to add biochar in a meaningful quantity to improve soil fertility [7].

Biochar is produced by pyrolysis of harvest residues with restricted O2 supply [8]. Biochar properties strongly depend on the substrates and pyrolysis conditions [9]. Carbonized biochar usually consists of a polycyclic aromatic structure, which is highly stable in soil [9, 10] and, thus, more resistant against microbial decomposition than soil organic C (SOC) [11]. However, biochar effects on soils properties strongly depend on soil type, especially clay content and soil pH [12], but may also be affected by climate [13]. Biochar has been reported to increase the water holding capacity and, thus, water storage for crop use in highly acidic Ferralsols of humid tropical regions [14, 15]. In this context, Steiner et al. [16] observed a linear relationship between increased microbial biomass carbon (MBC) contents and biochar application rates in Amazonia.

Biochar effects might be different in sandy soil under the semi-arid to sub-humid climate of sub-Saharan West Africa. This is characterized by an 8-month dry period that requires irrigation for year-round production in urban horticultural systems, which is usually supplied as domestic wastewater [17]. This wastewater use for irrigation has the advantages of reducing the demand for sewage plants [18], of supplying nutrients to vegetables [17, 19], and of saving scarce freshwater resources [20]. However, wastewater contains not only fecal pathogens [21,22,23], but also heavy metals, [24], organic pollutants [25], and NaCl [18], which cause problems for food safety, human health, and soil fertility [26]. Biochar application to soil may reduce the negative effects of wastewater application on the environment by absorbing these pollutants [9, 12], which most likely increases the functional diversity of the soil microbial community.

The effectts of biochar and N fertilization were investigated in two wastewater irrigated field experiments at semi-arid Ouagadougou (Burkina Faso) and sub-humid Tamale (Northern Ghana) [4, 5]. These experiments were focused on yields and nutrient balances in vegetable production systems over a 2-year period comprising 11 and 13 crops, respectively. Effects of N fertilization according to farmers’ practices, addition of biochar made from rice husks and corn cobs as well as wastewater and clean water irrigation on dry and fresh matter yields were extensively studied [4, 5]. Also, the effects of these treatments on changes in chemical soil properties such as soil pH, cation exchange capacity, SOC, and total N as well as extractable phosphorus have been carefully monitored at Ouagadougou and Tamale [3]. However, soil microorganisms as drivers of plant residue decomposition as well as C and N mineralization have been completely neglected in these experiments.

The biomass of soil microorganisms is an important indicator for soil fertility in tropical and sub-tropical soils [27], because MBC draws a relationship between plant C input, SOC stocks, and microbial mobilization–immobilization turnover of nutrients [28, 29]. MBC is usually combined with basal respiration rate, i.e., SOC mineralization in the absence of fresh substrates [30,31,32]. The membrane component ergosterol [33] gives additional important information on the contribution of saprotrophic fungi to the microbial community of agricultural soils [34, 35]. However, MBC often failed to indicate the rather subtle biochar effects [36, 37]. Multi-substrate-induced respiration (MSIR) is an interesting additional approach [38, 39]. MSIR is a potential activity of whole microbial communities in the period immediately after adding low molecular weight organic substances to soil before microorganisms start to grow [40]. Consequently, more of these substances will generally be anabolized by a C-limited microbial community, whereas an N-limited community is specifically characterized by the anabolization of N-containing substrates, such as amino acids or amino sugars. Consequently, MSIR may be able to create a link between functional diversity and a mechanistic understanding of soil processes.

The objective of the current study was to fill the current knowledge gap in two extensively studied experiments by measuring MBC, MSIR, and ergosterol. The study was designed to investigate the following hypotheses: (1) the sole application of biochar has no effects on soil microorganisms, because the effects on crop yield are negligible [4]. (2) The combined application of biochar and N fertilization increases MBC, fungal biomass, and functional diversity, because the negative effects of the nitrification-induced pH decline are reduced [3]. (3) Relative to clean water, wastewater irrigation may not have any impact on microbial biomass and functional diversity, as positive and negative impacts counterbalance each other. Effects of water quality on soil microorganisms were only studied in the Tamale soil, due to the strong differences in nutrient concentration between clean and wastewater in this city [3, 4], leading to marked differences in crop yield.

Material und methods

Study sites

The study was carried out in two West African cities, Ouagadougou (12°24′16 N, 1°28′40 W; approx. 1,500,000 inhabitants), the capital city of Burkina Faso, and Tamale (9°28′29 N, 0°50′53 W; approx. 300,000 inhabitants), the capital city of the Northern Region of Ghana, which are both characterized by a climate with a unimodal rainy season. The long-term average annual rainfall is 788 mm at Ouagadougou and 1111 mm at Tamale. In both cities, rainfall is lowest in January and highest in August and September. During the study period (2014–2016), the mean annual temperature was 28.2 °C in Ouagadougou and 27.5 °C in Tamale, measured by a watchdog weather station (Spectrum Technologies, Aurora, USA). The soil at semi-arid Ouagadougu was characterized as Cutanic Haplic Lixisol [41] with 60% sand, 35% silt and 5% clay. The soil at sub-humid Tamale was a Petroplinthic Cambisol with 46% sand, 48% silt and 6% clay.

Until the start of the experiment, the Ouagadougou site had been used for intensive vegetable horticulture, while the Tamale site had been used for rainfed maize (Zea mays L.) production. The cropping pattern in the two cities was similar during the experimental period for 11 and 13 harvest events (Table 1). The Ouagadougou site was cultivated with lettuce (Lactuca sativa L.), cabbage (Brassica oleracea L.), amaranth (Amaranthus cruentus L.), jute mallow (Corchorus olitorius L.), roselle (Hibiscus sabdariffa L.), and carrots (Daucus carota subsp. sativus (Hoffm.) Schübl. & G. Martens). The Tamale site was cultivated similarly, except for a start with maize (Zea mays L.) and a repeat of jute mallow after its first cultivation. All plots were irrigated with watering cans once or twice a day with a predefined quantity of water, which reflected farmers’ perception of the weather-related water demand of the current crops. Precipitation was considered for irrigation in the rainy seasons.

Table 1 Mean yield, N-input, P-input at the experimental sites in Ouagadougou (Burkina Faso) and Tamale (Northern Ghana) over the experimental years 2014 to 2016 taken from Akoto-Danso et al. [4]

Experimental design, setup, and treatments

The two experiments were carried out with four treatments as described in detail [3,4,5, 17] on plots of 2 × 4 m, which were replicated four times in a split-block design: (1) unfertilized control, (2) only biochar (BC), (3) fertilizer application according to local farmers’ practice (FP), and (4) FP + biochar. Generally, in Ouagadougou a combination of urea (46% N: 70–375 kg ha−1 per crop) and cattle manure (9 to 20 t ha−1 per crop with 17% C and 1.3% N) was used (Table 1). The fertilization in Tamale comprised only NPK (15-15-15: 200–563 kg ha−1 per crop). All treatments were also irrigated according to local farmers’ practice with wastewater (WW), obtained from a large open channel at Ouagadougou and from an untreated sewage channel at Tamale. Wastewater contained more N and P in Tamale: 31.9 mg N, 8.9 mg P, and 8.4 mg K l−1 than in Ouagadougou: 3.9 mg N, 0.8 mg P, and 44 mg K l−1 [3]. In Tamale, untreated wastewater (WW) was compared with clean water (CW), obtained from a tap: 0.4 mg N, 0.1 mg P, and 1.7 mg K l−1 [3].

Biochar was produced by slow pyrolysis using a local kiln at a temperature of about 500 °C [7]. Biochar was made from rice husks in Tamale and from corn cobs at Ouagadougou. Biochar from corn cobs had a pH-CaCl2 of 10.3, with concentrations of 68% C, 0.9% total N, and 19% ash. Biochar from rice husks had a pH-CaCl2 of 9.1, with concentrations of 42% C, 0.6% total N, and 45% ash [3]. A single biochar application in May 2014 at a rate of 20 t ha−1 was used in a 2-year study [17] and incorporated at 0–20 cm depth in both cities. After incorporation, the soil of all plots was thoroughly tilled.

Soil analysis

One soil sample was taken with an auger (7 cm diameter) after harvest of lettuce in June 2016 at 0–20 cm, sieved (< 2 mm), and stored at 4 °C in polyethylene bags until analysis. Soil pH was measured in water at a 1:2.5 soil to H2O ratio. Soil was dried at 80 °C and ground with a ball mill before measuring total C and N, using a Vario MAX CN analyser (Elementar, Hanau, Germany), ergosterol was extracted from 2 g moist soil with 100 ml ethanol for 30 min by oscillating shaking at 250 rev min−1 [42]. Then, ergosterol was measured by reversed phase HPLC (Gynkotek M 480 pump, UVD 340 S detector, and Gina 50 autosampler, Germering, Germany), using 100% methanol as the mobile phase and detected at a wavelength of 282 nm.

Microbial functional diversity

Functional diversity of soil microorganisms was determined by the MSIR approach using the MicroResp™ method [38]. The soil was adjusted to a water holding capacity of 45%, before weighing 300 mg into each deep well (1.1 ml) of a microtiter plate (Nunc, Thermo Electron LED, Langenselbold, Germany) and stored for 3 days in the dark at 25 °C prior to MSIR analysis. The physiological profiles were determined by applying distilled water (for basal respiration), three amino acids [L-alanine (Ala), L-glutamine (GluN), and L-serine (Ser)], one amino sugar [N-acetyl-glucosamine (NAG)], two carbohydrates [(D-glucose (Glc), D-fructose (Fruc)], four carboxylic acids [malic acid (Mal), quinic acid (Qui), oxalic acid (Oxa), and tartaric acid (Tat)], and one phenolic organic acid [protocatechuic acid (ProC)]. These substrates were chosen to present a cross section of root exudates [38] and microbial components and products [43, 44]. A substrate concentration of 8 mg g−1 dry soil was used by placing 20 μl of solution in the deep well plate, before incubating the soil for 6 h at 25 °C. Only 1 mg g−1 soil of L-glutamine and 0.3 mg g−1 soil of protocatechuic acid were used, due to their low solubility at higher concentrations. An excess of substrate was always added to the soil to saturate the microbial community, as tested in previous studies [38, 39].

A colorimetric CO2 trap [38] was stored for 72 h in a closed PVC bag, containing soda lime and wet tissue paper. The color of the CO2 trap was measured immediately before sealing and after 6 h of incubation (25 °C) at 572 nm (FLUOstar, BMG, Offenburg, Germany). The CO2 trap was calculated as μl CO2 = 51 × (0.2 + ABS)3 [40], where ABS is the difference in absorption of T1 and T0. The Shannon diversity index was calculated using the formula H =  − Σ pi (ln pi), where pi is the particular activity of the sum of all activities [45]. In addition, basal respiration was calculated from aqua dest. addition and MBC from Glc addition (30 × µl CO2 g−1 h−1) [46].

Statistical analysis

Data are presented as arithmetic means on a dry weight basis. Statistical analyses were carried out using SigmaPlot 13.0 (Systat, San José, USA). Data were tested for normality of residuals using Shapiro–Wilk test. In case of non-normality, data were ln-transformed. The significance of treatment main effects was analyzed by a two-way ANOVA for the samples from Ouagadougou and a three-way ANOVA for the samples from Tamale. Biochar and N-fertilization on the mean substrate-specific respiration were assessed using a paired t-test. Discriminant function analysis was conducted on the combined MSIR data for all samples from Ouagadougou (n = 16) and Tamale (n = 24) to investigate fertilizer effects on the substrate utilization patterns, with SPSS 16.0 statistical software (SPSS 16.0). To describe discrimination, substrate-specific respiration was correlated to the canonical scores of the significant (P < 0.05) discriminant functions (DF). Pearson correlation coefficients were used to express significance. The canonical DF scores were correlated with the soil parameters to identify their contribution to discrimination.


Biochar addition increased SOC contents in both cities and total N contents at Tamale (Table 2), but no other soil chemical or soil biological property analyzed (Table 3). Nitrogen fertilization decreased soil pH in both cities by 1.1 units (Table 2), so that a pH-H2O of 4.7 was reached at Tamale. This strong acidification was combined with a significant reduction in MBC and ergosterol contents, whereas basal respiration was not affected. This led to increased qCO2 values in comparison with the unfertilized control treatments.

Table 2 Mean soil pH and mean contents of SOC, total N, MBC, and ergosterol, mean basal respiration rate and metabolic quotients qCO2 in soil from the experimental sites at Ouagadougou (Burkina Faso) and Tamale (Northern Ghana); probability values for the two-way ANOVA at Ouagadougou and the three-way ANOVA at Tamale, interactions were all not significant with one exception at Tamale

Without N fertilization, Mal, Qui, Oxa, and Tat exhibited on average a 90% (P < 0.01, paired t-test) stronger respiratory response in the Tamale soil than in the Ouagadougou soil (Table 3), whereas all other substrates led to similar respiration rates in both soils. With N fertilization, Ala (Fig. 1) and Mal-induced respiration was significantly increased by 29% and 19%, respectively, in Ouagadougou soil, whereas Ser, GluN, NAG, Qui, Oxa, Tat, Pro, and Fruc-induced respiration remained largely unaffected (Table 3). In contrast, Ala (Fig. 1), Ser, GluN, NAG, Pro, and Fruc-induced soil respiration was significantly decreased with N fertilization in Tamale soil (Table 3), whereas the four organic acids Mal, Qui, Oxa, and Tat again remained unaffected.

Fig. 1
figure 1

Mean alanine-induced respiration rates in soil from the experimental sites in Ouagadougou (Burkina Faso) and Tamale (Northern Ghana); probability values for the two-way ANOVA at Ouagadougou: Biochar (not significant) and Fertilizer (P < 0.04); probability values for the three-way ANOVA at Tamale: Biochar (not significant), Fertilizer (P < 0.01), and Irrigation (not significant); interactions were all not significant; bars on top of each column indicate one standard deviation

Biochar application increased the mean respiratory response of the 11 substrates added by 23% (P < 0.01, paired t-test) in Ouagadougou soil and by 13% (P < 0.02, paired t-test) in Tamale soil only in combination with N fertilization. Clean water irrigation in Tamale decreased basal respiration of soils without N fertilization, whereas the reverse effect was observed with N fertilization, leading to the only significant second-order interaction. Clean water irrigation decreased the ergosterol content at Tamale (Table 2), but increased organic acid-induced respiration (Fig. 2).

Fig. 2
figure 2

Boxplots of respiration rates, induced by malic acid, quinic acid, tartaric acid and oxalic acid in soil from the experimental site in Tamale (Northern Ghana)

The Shannon index of the respiratory response to water and the 11 substrates added was generally positively correlated with soil pH (Fig. 3). This index varied in a small range around 2.42 at Ouagadougou and a much larger range between 2.05 and 2.41 at Tamale. There, biochar addition increased the range of the Shannon index without N fertilization and reduced the range with N fertilization. This different behavior was partly reflected by the DF2 (Fig. 4), where the pure BC treatment produced negative scores and the FP + BC treatment yielded positive scores. However, N fertilization effects were much more clearly separated by DF1, which explained 81% of the variance.

Fig. 3
figure 3

Relationship between Shannon diversity index and pH in soil from the experimental sites in Ouagadougou (Burkina Faso) and Tamale (Northern Ghana)

Fig. 4
figure 4

Discriminant function analysis of catabolic response of 11 substrates plus aqua dest. for the four fertilizer treatments in soil from the experimental sites in Ouagadougou (Burkina Faso) and Tamale (Northern Ghana)

Mal, Qui, Oxa, and Tat were the only substrates that were negatively correlated with soil pH and the Shannon index (Table 4), whereas Ser, GluN, NAG, Pro, and Fruc were positively correlated. The four organic acids Mal, Qui, Oxa, and Tat remained unaffected by SOC content, whereas all other substrates showed highly significant correlations. N effects explaining DF1 were positively correlated with GluN, Pro, Fruc, and Glc (Fig. 4), whereas biochar effects explaining DF2 were significantly correlated with aqua dest., Ala, Ser, NAG, Mal, Pro and Glc.

Table 3 Mean multi-substrate-induced respiration rates in soil from the experimental sites in Ouagadougou (Burkina Faso) and Tamale (Northern Ghana); probability values for the two-way ANOVA at Ouagadougou and the three-way ANOVA at Tamale, interactions were all not significant
Table 4 Pearson correlation coefficient between substrate utilization and discriminant functions DF1 and DF2, Shannon index, soil pH, and SOC in soil from the experimental sites in Ouagadougou (Burkina Faso) and Tamale (Northern Ghana)


Sole biochar addition to soil did not affect biomass or functional diversity of soil microorganisms in either of the cities. Also, the effects on crop yield were generally negligible and only transient for short times if some increases occurred [4, 5, 17]. Consequently, the sole biochar treatment was not considered in a publication summarizing treatment effects on dry matter yields in Ouagadougou and Tamale (Table 1; [4]).

In contrast, biochar addition in combination with N fertilization increased the mean respiratory response of soil microorganisms to virtually all substrates added to soil in both cities in comparison with the sole N fertilization treatment, despite the absence of significant effects on a single substrate. A higher respiratory response indicates a reduction in microbial C limitation [40], e.g., due to an increased C input into soil by harvest and root residues of the crops cultivated, assuming a relationship between crop yield and belowground biomass [47]. However, the reduction in microbial C limitation was not strong enough to increase MBC contents. The increase in respiratory response was markedly stronger in the alkaline Ouagadougou, due to the strong fertilizer-induced increase in MBC, than in the acidic Tamale soil, where fertilization further reduced soil pH accompanied by a strong decline in MBC. This contradicts the view that biochar especially improves microbial habitat conditions in acidic low fertility soils, such as a Ferralsol in Brasilia [48]. Fertilization with inorganic N and organic manure increased total N by 88% and SOC by 52% in the alkaline Ouagadougou soil in comparison with the control and sole BC treatment. These increases were accompanied by a significantly higher respiratory response to alanine, which indicates a strong reduction in N limitation [40], as otherwise alanine should have been anabolized to microbial metabolites and not catabolized to CO2.

Inorganic N fertilization with ammonium generally decreased soil pH in both cities, which is most likely due to nitrification [3]. This was of little relevance in the alkaline Ouagadougou soil, but it is a serious threat to soil fertility in the acidic Tamale soil, where inorganic fertilization reduced the pH to below the critical value of pH 5. At this pH, soluble and exchangeable Al3+ is a serious threat to crops [49] and soil microorganisms, leading to a strong decline in MBC, respiratory response, and functional diversity. The negative pH effects on MBC and microbial functional diversity override the positive effects of increased crop yields, probably accompanied by increased input of harvest and root residues. This is in line with the view that soil pH is the dominating factor that controls microorganisms in soil [28, 50, 51]. The significantly increased qCO2 values indicate the higher demand for maintenance energy in acidic soil [31, 52], strongly impeding SOC accumulation and, thus, soil fertility [28]. Care should be taken to avoid such N fertilizer-induced acidification, not only in West African urban horticulture, but also elsewhere.

Irrigation with wastewater had no general negative effects on MBC in the acidic Tamale soil, but a strong positive effect on ergosterol, an important indicator for saprotrophic fungi in agricultural soils [34, 35]. The positive biochar effect on fungi might be due to their stronger ability to break down the recalcitrant C components in wastewater compared with bacteria [53,54,55]. A striking feature of the current results is the response of the malic acid, quinic acid, oxalic acid, and tartaric acid to differences in soil properties between Ouagadougou and Tamale as well as to differences between clean water and wastewater. This is even more remarkable as these four organic acids were the only ones that did not respond to N fertilization and that were not correlated with discriminant functions. The strong response of the four organic acids is probably due to their extremely high respiratory quotient (mol CO2/mol O2), which results in higher CO2 evolution rates during catabolization in comparison with other substrates [56, 57].

In the acidic Tamale soil, the respiratory response to the addition of organic acids is nearly twice that in the alkaline Ouagadougou soil. One reason might be a stronger adsorption of organic acids at high pH [58]. However, the respiratory responses to organic acid addition were like the other substrates in all treatments, i.e., also in the N fertilization treatments with neutral pH. Another reason might be a stronger adaptation of the microbial community to mineralize organic acids in their presence [59]. However, the catabolic use of organic acids probably requires less adaptation than the anabolic use, which seems to be higher in the Ouagadougou soil, as indicated by the lower respiratory responses to organic acid addition. In this alkaline soil, crop roots, especially those of non-mycorrhizal cabbage and lettuce [60], might excrete more organic acids for mobilizing phosphate. Consequently, these acidic organic components are more common for microbial anabolism, as indicated by the lower respiratory response to organic acid addition in the alkaline Ouagadougou soil.

The higher respiratory response of soil microorganisms to organic acid addition in the clean water treatment at Tamale might also be due to the lower presence of organic acids in comparison with wastewater. Another reason might be differences in microbial community structure, as the soil of the clean water treatments contained fewer saprotrophic fungi, which seem to have a higher ability to excrete and to anabolize organic acids than bacteria [61]. This would be an appropriate objective for a follow-up experiment.


Sole biochar addition to field plots in Ouagadougou and Tamale did not affect soil microbial biomass carbon (MBC) or functional diversity, estimated by multi-substrate-induced respiration. Biochar addition with N fertilization generally increased the microbial respiratory response to most substrates added, indicating a reduction in C limitation for soil microorganisms and, thus, improved habitat conditions. However, the N fertilizer-induced decline in soil pH < 5 should be avoided, as it decreased MBC and microbial functional diversity in the Tamale soil. Only the respiratory response to organic acids added remained unaffected by biochar and N fertilizer addition but was significantly increased by clean water compared with wastewater irrigation. This is an interesting feature of the current results, which was accompanied by a reduction in saprotrophic soil fungi. However, the long-term effects of this shift in microbial biomass and functional diversity in soil needs further evaluation to promote best management practices of biochar application and wastewater use.

Availability of data and materials

The data are available on request.



Soil organic carbon


Microbial biomass carbon


Multi-substrate-induced respiration






L-Serine (Ser)


One N-acetyl-glucosamine






Malic acid


Quinic acid


Oxalic acid


Tartaric acid


Protocatechuic acid


  1. Bellwood-Howard I, Häring V, Karg H, Roessler R, Schlesinger J, Shakya M. Characteristics of urban and peri-urban agriculture in West Africa: results of an exploratory survey conducted at Tamale, Ghana, and Ouagadougou, Burkina Faso. IWMI Working Papers 163; 2015.

  2. Neina D, Faust S, Joergensen RG. Charcoal and firewood ash waste from urban kitchens differ in their chemical and mineralogical properties. Chem Biol Technol Agric. 2020;7:5.

    Article  CAS  Google Scholar 

  3. Häring V, Manka’abusi D, Akoto-Danso EK, Werner S, Atiah K, Steiner C, Lompo DJP, Adiku S, Buerkert A, Marschner B. Effects of biochar, waste water irrigation and fertilization on soil properties in West African urban agriculture. Sci Rep. 2017;7:10738.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Akoto-Danso EK, Manka’abusi D, Steiner C, Werner S, Hearing V, Lompo DJP, Nyarko G, Marschner B, Drechsel P, Buerkert A. Nutrient flows and balances in intensively managed vegetable production of two West African cities. J Plant Nutr Soil Sci. 2019;182:229–43.

    Article  CAS  Google Scholar 

  5. Manka’abusi D, Steiner C, Akoto-Danso EK, Lompo DJP, Hearing V, Werner S, Marschner B, Buerkert A. Biochar application and wastewater irrigation in urban vegetable production of Ouagadougou, Burkina Faso. Nutr Cycl Agroecosyst. 2019;115:263–79.

    Article  CAS  Google Scholar 

  6. Werner S, Akoto-Danso EK, Manka’abusi D, Steiner C, Haering V, Nyarko G, Buerkert A, Marschner B. Nutrient balances with wastewater irrigation and biochar application in urban agriculture of Northern Ghana. Nutr Cycl Agroecosyst. 2019;115:249–62.

    Article  CAS  Google Scholar 

  7. Steiner C, Bellwood-Howard I, Häring V, Tonkudor K, Addai F, Atiah K, Abubakari AH, Kranjac-Berisavljevic G, Marschner B, Buerkert A. Participatory trials of on-farm biochar production and use in Tamale, Ghana. Agron Sustain Develop. 2018;38:12.

    Article  CAS  Google Scholar 

  8. Lehmann J, Joseph S. Biochar for environmental management: science and technology. London: Earthscan; 2009.

    Google Scholar 

  9. Jindo K, Audette Y, Higashikawa FS, Silva CA, Akashi K, Mastrolonardo G, Sanchez-Monedero MA, Mondini C. Role of biochar in promoting circular economy in the agriculture sector. Part 1: A review of the biochar roles in soil N, P and K Cycles. Chem Biol Technol Agric. 2020;7:15.

    Article  Google Scholar 

  10. Schimmelpfennig S, Glaser B. One step forward toward characterization. Some important material properties to distinguish biochars. J Environ Qual. 2012;41:1001–13.

    Article  CAS  PubMed  Google Scholar 

  11. Baldock JA, Smernik RJ. Chemical composition and of thermally altered Pinus resinosa (Red pine) wood. Org Geochem. 2002;33:1093–109.

    Article  CAS  Google Scholar 

  12. Ding Y, Liu Y, Liu S, Li Z, Tan X, Huang X, Zeng G, Zhou L, Zheng B. Biochar to improve soil fertility. A review. Agron Sustain Dev. 2016;36:36.

    Article  CAS  Google Scholar 

  13. Ye L, Camps-Arbestain M, Shen Q, Lehmann J, Singh B. Biochar effects on crop yields with and without fertilizer: a meta-analysis of field studies using separate controls. Soil Use Manag. 2020;36:2–18.

    Article  Google Scholar 

  14. Steiner C, Teixeira WG, Lehmann J, Nehls T, Vasconcelos de Macêdo JL, Blum WEH, Zech W. Long term effects of manure, charcoal and mineral fertilization on crop production and fertility on a highly weathered Central Amazonian upland soil. Plant Soil. 2007;291:275–90.

    Article  CAS  Google Scholar 

  15. Dakoure MYS, Mermoud A, Yacouba H, Boivin P. Impacts of irrigation with industrial treated wastewater on soil properties. Geoderma. 2013;200–201:31–9.

    Article  CAS  Google Scholar 

  16. Steiner C, Das KC, Garcia M, Förster B, Zech W. Charcoal and smoke extract stimulate the soil microbial community in a highly weathered xanthic Ferralsol. Pedobiologia. 2008;51:359–66.

    Article  CAS  Google Scholar 

  17. Akoto-Danso EK, Manka’abusi D, Steiner C, Werner S, Häring V, Nyarko G, Marschner B, Drechsel P, Buerkert A. Agronomic effects of biochar and wastewater irrigation in urban crop production of Tamale, northern Ghana. Nutr Cycl Agroecosyst. 2019;15:231–47.

    Article  CAS  Google Scholar 

  18. Musazura W, Odindo AO, Tesfamariam EH, Hughes JC, Buckley CA. Nitrogen and phosphorus dynamics in plants and soil fertigated with decentralised wastewater treatment effluent. Agric Water Manag. 2019;215:55–62.

    Article  Google Scholar 

  19. Singh PK, Deshbhratar PB, Ramteke DS. Effects of sewage wastewater irrigation on soil properties, crop yield and environment. Agric Water Manag. 2012;103:100–4.

    Article  Google Scholar 

  20. Scott CA, Faruqui NI, Raschid-Sally L. Wastewater use in irrigated agriculture: management challenges in developing countries. In: Wastewater use in irrigated agriculture: confronting the livelihood and environmental realities. CABI Wallingford; 2004. P. 1–10

  21. Akponikpè PBI, Wima K, Yacouba H, Mermoud A. Reuse of domestic wastewater treated in macrophyte ponds to irrigate tomato and eggplant in semi-arid West-Africa: benefits and risks. Agric Water Manag. 2011;98:834–40.

    Article  Google Scholar 

  22. Faour-Klingbeil D, Todd ECD. The impact of climate change on raw and untreated wastewater use for agriculture, especially in arid regions: a review. Foodborne Path Dis. 2018;15:61–72.

    Article  PubMed  Google Scholar 

  23. Bougnom BP, Zongo C, McNally A, Ricci V, Etoa FX, Thiele-Bruhn S, Piddock LJV. Wastewater used for urban agriculture in West Africa as a reservoir for antibacterial resistance dissemination. Environ Res. 2019;168:14–24.

    Article  CAS  PubMed  Google Scholar 

  24. Diogo RVC, Buerkert A, Schlecht E. Horizontal nutrient fluxes and food safety in urban and peri-urban vegetable and millet cultivation of Niamey, Niger. Nutr Cycl Agroecosyst. 2010;87:81–102.

    Article  Google Scholar 

  25. Amoah P, Drechsel P, Abaidoo RC, Ntow WJ. Pesticide and pathogen contamination of vegetables in Ghana’s urban markets. Arch Environ Contamin Toxicol. 2006;50:1–6.

    Article  CAS  Google Scholar 

  26. Esmaili E, Kapourchal SA, Malakouti MJ, Homaee M. Interactive effect of salinity and nitrogen fertilizers on growth and composition of sorghum. Plant Soil Environ. 2008;54:537–46.

    Article  CAS  Google Scholar 

  27. Joergensen RG. Organic matter and micro-organisms in tropical soils. In: Dion P, editor. Soil biology and agriculture in the tropics. Berlin: Springer; 2010. p. 17–44.

    Chapter  Google Scholar 

  28. Khan KS, Mack R, Castillo X, Kaiser M, Joergensen RG. Microbial biomass, fungal and bacterial residues, and their relationships to the soil organic matter C/N/P/S ratios. Geoderma. 2016;271:115–23.

    Article  CAS  Google Scholar 

  29. Joergensen RG, Wichern F. Alive and kicking: Why dormant soil microorganisms matter. Soil Biol Biochem. 2018;116:419–30.

    Article  CAS  Google Scholar 

  30. Anderson TH, Domsch KH. Application of ecophysiological quotients (qCO2 and qD) on microbial biomasses from soils of different cropping histories. Soil Biol Biochem. 1990;22:251–5.

    Article  Google Scholar 

  31. Anderson TH, Domsch KH. The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol Biochem. 1993;25:393–5.

    Article  Google Scholar 

  32. Anderson TH, Domsch KH. Soil microbial biomass: the eco-physiological approach. Soil Biol Biochem. 2010;42:2039–43.

    Article  CAS  Google Scholar 

  33. Weete JD, Abril M, Blackwell M. Phylogenetic distribution of fungal sterols. PLoS ONE. 2010;5:e10899.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Joergensen RG, Wichern F. Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem. 2008;40:2977–91.

    Article  CAS  Google Scholar 

  35. Faust S, Heinze S, Ngosong C, Sradnick A, Oltmanns M, Raupp J, Geisseler D, Joergensen RG. Effect of biodynamic soil amendments on microbial communities in comparison with inorganic fertilization. Appl Soil Ecol. 2017;114:82–9.

    Article  Google Scholar 

  36. Fernández JM, Nieto MA, López de Sá EG, Gascó G, Méndez A, Plaza C. Carbon dioxide emissions from semi-arid soils amended with biochar alone or combined with mineral and organic fertilizers. Sci Total Environ. 2014;482–483:1–7.

    Article  CAS  PubMed  Google Scholar 

  37. Elzobair KA, Stromberger ME, Ippolito JA, Lentz RD. Contrasting effects of biochar versus manure on soil microbial communities and enzyme activities in an Aridisol. Chemosphere. 2016;142:145–52.

    Article  CAS  PubMed  Google Scholar 

  38. Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM. A rapid microtiter plate method to measure carbon dioxide evolved from C substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol. 2003;69:3593–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sradnick A, Murugan R, Oltmanns M, Raupp J, Joergensen RG. Changed in functional diversity of the soil microbial community in a heterogeneous sandy soil after long-term fertilisation with cattle manure and mineral fertilizer. Appl Soil Ecol. 2013;63:23–8.

    Article  Google Scholar 

  40. Struecker J, Joergensen RG. Microorganisms and their substrate utilization patterns in topsoil and subsoil layers of two silt loams, differing in soil organic C accumulation due to colluvial processes. Soil Biol Biochem. 2015;91:310–7.

    Article  CAS  Google Scholar 

  41. IUSS Working Group WRB. World Reference Base for Soil Resources 2014, update 2015 International soil classification system for naming soils and creating legends for soil maps. Rome: FAO; 2015.

    Google Scholar 

  42. Djajakirana G, Joergensen RG, Meyer B. Ergosterol and microbial biomass relationship in soil. Biol Fertil Soils. 1996;22:299–304.

    Article  CAS  Google Scholar 

  43. Amelung W, Miltner A, Zhang X, Zech W. Fate of microbial residues during litter decomposition as affected by minerals. Soil Sci. 2001;166:598–606.

    Article  CAS  Google Scholar 

  44. Meyer A, Fischer H, Kuzyakov Y, Fischer K. Improved RP-HPLC and anion exchange chromatography methods for the determination of amino acids and carbohydrates in soil solutions. J Plant Nutr Soil Sci. 2008;171:917–26.

    Article  CAS  Google Scholar 

  45. Zak J, Willig M, Moorhead D, Wildman H. Functional diversity of microbial communities. A quantitative approach. Soil Biol Biochem. 1994;26:1101–8.

    Article  Google Scholar 

  46. Kaiser EA, Mueller T, Joergensen RG, Insam H, Heinemeyer O. Evaluation of methods to estimate the soil microbial biomass and the relationship with soil texture and organic matter. Soil Biol Biochem. 1992;24:675–83.

    Article  CAS  Google Scholar 

  47. Ludwig B, Schulz E, Merbach I, Rethemeyer J, Flessa H. Predictive modelling of the C dynamics for eight variants of the long-term static fertilization experiment in Bad Lauchstädt using the Rothamsted Carbon Model. Eur J Soil Sci. 2007;58:1155–63.

    Article  CAS  Google Scholar 

  48. Steiner C, de Arruda MR, Teixeira WG, Zech W. Soil respiration curves as soil fertility indicators in perennial central Amazonian plantations treated with charcoal, and mineral or organic fertilisers. Tropic Sci. 2007;47:218–30.

    Article  Google Scholar 

  49. Yang ZB, Rao IM, Horst WJ. Interaction of aluminium and drought stress on root growth and crop yield on acid soils. Plant Soil. 2013;372:3–25.

    Article  CAS  Google Scholar 

  50. Lauber CL, Strickland MS, Bradford MA, Fierer N. The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem. 2008;40:2407–15.

    Article  CAS  Google Scholar 

  51. Strickland MS, Rousk J. Considering fungal:bacterial dominance in soils–methods, controls, and ecosystem implications. Soil Biol Biochem. 2010;42:1385–95.

    Article  CAS  Google Scholar 

  52. Anderson TH, Joergensen RG. Relationship between SIR and FE estimates of microbial biomass C in deciduous forest soils at different pH. Soil Biol Biochem. 1997;29:1033–42.

    Article  CAS  Google Scholar 

  53. Krasner SW, Westerhoff P, Chen B, Rittmann BE, Nam SN, Amy G. Impact of wastewater treatment processes on organic carbon, organic nitrogen, and DBP precursors in effluent organic matter. Environ Sci Technol. 2009;43:2911–8.

    Article  CAS  PubMed  Google Scholar 

  54. de Boer W, Folman LB, Summerbell RC, Boddy L. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev. 2005;29:795–811.

    Article  CAS  PubMed  Google Scholar 

  55. Bardi A, Yuan Q, Tigini V, Spina F, Varese GC, Spennati F, Becarelli S, Di Gregorio S, Petroni G, Munz G. Recalcitrant compounds removal in raw leachate and synthetic effluents using the white-rot fungus Bjerkandera adusta. Water. 2007;9:824.

    Article  CAS  Google Scholar 

  56. Dilly O. Microbial respiratory quotient during basal metabolism and after glucose amendment in soils and litter. Soil Biol Biochem. 2001;33(117–127):117–27.

    Article  CAS  Google Scholar 

  57. Dilly O. Microbial energetics in soils. In: Buscot F, Varma A, editors. Microorganisms in soils: roles in genesis and functions. Berlin: Springer; 2005. p. 123–38.

    Chapter  Google Scholar 

  58. Ström L, Owen AG, Godbold DL, Jones DL. Organic acid behaviour in a calcareous soil: sorption reactions and biodegradation rates. Soil Biol Biochem. 2001;33:2125–33.

    Article  Google Scholar 

  59. Haney RL, Haney EB, White MJ, Smith DR. Soil CO2 response to organic and amino acids. Appl Soil Ecol. 2018;125:297–300.

    Article  Google Scholar 

  60. Dechassa N, Schenk M. Exudation of organic anions by roots of cabbage, carrot, and potato as influenced by environmental factors and plant age. J Plant Nutr Soil Sci. 2004;167:623–9.

    Article  Google Scholar 

  61. Frey-Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A. Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol Molec Biol Rev. 2011;75:583–609.

    Article  CAS  Google Scholar 

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The technical assistance of Gabriele Dormann, Martin Lüttge, and Larissa Krause in soil analysis is highly appreciated.


Open Access funding enabled and organized by Projekt DEAL. The field work of this study was funded by the German Ministry of Education and Research (BMBF) within the framework of the UrbanFoodPlus project ( as part of the GlobE initiative (BMBF, FKZ 031A242A).

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ALF: analyzed the soil samples, conducted literature review, data analysis and draft manuscript preparation. RJ: contributed to laboratory experiments, data analysis, and reviewed the draft manuscript. RB: contributed to laboratory experiments and reviewed the draft manuscript. CS: organized the field experiment, took the soil samples, and reviewed the draft manuscript. AB: conceived funding, designed the study, and reviewed the draft manuscript. RGJ: supervised analysis, contributed to data analysis and wrote the final manuscript. All authors read and approved the final manuscript.

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Correspondence to Rainer Georg Joergensen.

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Fritz, AL., Jannoura, R., Beuschel, R. et al. The combined application of nitrogen and biochar reduced microbial carbon limitation in irrigated soils of West African urban horticulture. Chem. Biol. Technol. Agric. 9, 48 (2022).

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