Original Paper Plant, and Environment, 66, 2020 (11): 590–597

https://doi.org/10.17221/385/2020-PSE

Effect of organic fertilisers on glomalin content and quality

Jiří Balík1*, Ondřej Sedlář1, Martin Kulhánek1, Jindřich Černý1, Michaela Smatanová2, Pavel Suran1

1Department of Agro-Environmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague, Czech Republic 2Central Institute for Supervising and Testing in Agriculture, Brno, Czech Republic *Corresponding author: [email protected]

Citation: Balík J., Sedlář O., Kulhánek M., Černý J., Smatanová M., Suran P. (2020): Effect of organic fertilisers on glomalin content and soil organic matter quality. Plant Soil Environ., 66: 590–597.

Abstract: Glomalin is one of the factors with an important role at forming and stabilising soil aggregates. Long-term stationary experiments were carried out to observe the influence of various fertilisation treatments on the content of glomalin in topsoil. The content of easily extractable glomalin (EEG) and total glomalin (TG) were determined. Mo- reover, glomalin was also determined by using the near-infrared reflectance spectroscopy (GNIRS). Both mineral and organic fertilisation significantly increased the content of glomalin compared to the unfertilised control. However, observed differences among individual fertilisation treatments were not significant. A significant correlation was de- termined between the content of EEG, TG, GNIRS, and the content of humic substances as well as humic acids. Both methods used (EEG, TG) can equally reflect soil organic matter quality. A significant correlation was also recorded between the GNIRS and extraction methods (EEG, TG).

Keywords: long-term experiments; mineral fertilisation; humic substances fractionation; glycoprotein; decomposition; quality indicator

Besides a range of soil organic matter quality in- (Rillig 2004, Gadkar and Rillig 2006, Nichols and dicators, a great attention has been recently paid Wright 2006). to the glomalin content observations (Bedini et al. The content of glomalin is influenced by the amount 2013). Glomalin is produced by arbuscular mycor- and type of organic fertilisation (Alguacil et al. 2008, rhizal fungi and is one of the most important soil Gispert et al. 2013, Singh et al. 2013). Lower glo- proteins. This compound was discovered and named malin concentrations were recorded in arable land in 1996 by Wright and Upadhyaya (1996). Glomalin compared to permanent grasses, which is probably is a glycoprotein excreted by fungi Glomeromycota related to higher aerification of cultivated and, (glomales). The exact molecular composition has not thus, more intensive soil organic matter mineralisa- been determined yet (Singh et al. 2013), because the tion (Smatanová and Komprsová 2019). Glomalin glomalin fraction obtained by extraction is not pure concentration is significantly lower in tilled soils enough (Schindler et al. 2007). This is the reason compared to no-till systems (Curaqueo et al. 2011). that some studies use the term "glomalin-related Glomalin is one of the factors with an important soil protein" or GRSP (Rillig 2004). role at forming and stabilising soil aggregates. It thus Glomalin is hydrophobic and thermally stable (the significantly influences soil organic matter stability extraction is carried out in an autoclave at 121 °C). (Wright and Upadhyaya 1998, Wright and Anderson It is significantly resistant to decomposition in soil 2000, Rillig 2004, Driver et al. 2005, Emran et al.

Supported by the European Regional Development Fund – Project NutRisk Centre, Project No. CZ.02.1.01/0.0/0.0/1 6_019/0000845.

590 Plant, Soil and Environment, 66, 2020 (11): 590–597 Original Paper https://doi.org/10.17221/385/2020-PSE

2012, Galazka et al. 2017), as soil aggregates slow MATERIAL AND METHODS down soil organic matter decomposition (Jastrow 1996, Six et al. 2000). The presence of glomalin in The effect of fertilisation on the content of glomalin the soil further increases water retention, prevents in soil was observed in long-term field trials established erosion, supports the development of , affects in 1996 at the experimental base Červený Újezd – the activity of soil enzymes, and stimulates plant 50°4'22''N, 14°10'19''E. Except for low potassium growth (Wang et al. 2015). Reduced soil glomalin content, the content of other available nutrients concentration has been usually reported at sites (P, Mg, Ca) in soil (Mehlich 3) was sufficient (Table 1). where the was disturbed, e.g., by tillage Within these trials, three crops were rotated in or drought (Wright and Anderson 2000). the following order: maize, winter wheat, and spring Glomalin content also varies in relation to the soil barley. Each year, all of the crops were grown. The 2 profile depth, as reported in the results of Galazka size of the experimental plots was 80 m , every plot 2 et al. (2017); they determined the highest content was divided into four sub-plots during harvest (20 m of easily extractable glomalin (EEG), total gloma- each). The trial included seven treatments: (1) no lin (TG), and glomalin-related soil protein (GRSP) fertilisation (control); (2) sewage sludge (SS1); (3) in the 5–20 cm layer, whereas it was significantly high dose of sewage sludge (SS3); (4) farmyard manure lower in the 30–35 cm layer. Gispert et al. (2013) (FYM1); (5) half dose of farmyard manure + N in determined higher glomalin content in larger soil mineral nitrogen fertiliser (FYM1/2 + N); (6) mineral aggregates (2.0–5.6 mm) compared to the smaller nitrogen fertiliser (N); (7) spring barley straw + N ones (0.25–2.00 mm). in mineral nitrogen fertiliser (N + St) (Table 2). The impact of rotated crops selection is also sig- Organic fertilisers (farmyard manure, sewage sludge, nificant: in long-term experiments in Skierniewice and straw) were always applied in autumn (October) (Poland), the TG content was lower at plots with rye to maize and were immediately incorporated in the monoculture compared to those with rotated crops soil to approximately 28 cm depth with ploughing. (potato/rye) (Wojewódzki and Cieścińska 2012). The remaining treatments were ploughed to the same Steinberg and Rillig (2003) reported slight seasonal depth at the same time. Mineral nitrogen fertilisers oscillations of glomalin content in the soil; it is thus in the form of calcium ammonium nitrate were ap- possible that it may also vary during the vegetation plied to maize and spring barley in spring, prior to period. For instance, Galazka et al. (2017) recorded the crop establishment. In the case of winter wheat, significantly higher TG content in the soil during the dose of nitrogen was divided in half, with the first the maize growth compared to the soil glomalin half applied at BBCH 21 and the second at BBCH content before sowing. 31–32. The content of nitrogen was 140 kg N/ha for Generally, it may be concluded that the use of wheat and 70 kg N/ha for spring barley; FYM1/2 + N mineral and organic fertilisers increases the glomalin content in soils compared to the unfertilised control Table 1. Characteristics of the Červený Újezd experi- (Curaqueo et al. 2011, Dai et al. 2013, Turgay et al. mental site 2015, Sandeep et al. 2016). Altitude (m a.s.l.) 410 The evaluation of glomalin content as an indica- Mean annual temperature (°C) 7.7 tor of changes in quality of soil fertility is due to its Mean annual precipitation (mm) 493 positive correlation with the changes of soil organic Soil type Luvisol matter carbon content (CSOM) (Wright and Upadhyaya 1996, 1998, Wilson et al. 2009, Dai et al. 2013, Xie et Soil texture loam pH 6.5 al. 2015). Contrariwise, results published by Galazka CaCl2 et al. (2017) show a negative correlation between the CSOM (%) 1.2 content of GRSP and CSOM. Cation exchange capacity (mmol+/kg) 145 The aim of this paper was to study the effect of P – Mehlich 3 (mg/kg) 100 various fertilisation systems on soil organic matter K – Mehlich 3 (mg/kg) 80 quality using the glomalin content as an indicator, Mg – Mehlich 3 (mg/kg) 110 and further to quantify the relationship between the Ca – Mehlich 3 (mg/kg) 3 600 glomalin content and the content of humic substances, humic acids, and fulvic acids. CSOM – soil organic matter carbon content

591 Original Paper Plant, Soil and Environment, 66, 2020 (11): 590–597

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Table 2. Experimental design

Maize Wheat Barley Organic fertiliser Treatment N (kg/ha/year) C (kg/ha/year) C/N Cont 0 0 0 0 0 SS1 3301 0 0 813 7.4/1 SS3 9901 0 0 2 439 7.4/1 FYM1 3301 0 0 1 482 13.4/1 FYM1/2 + N 1651 1152 502 741 13.4/1 N 1202 1402 702 0 0 N + St 1202 + St 1402 702 712 79.3/1

1Total dose of nitrogen applied in organic fertiliser; average yearly dose based on the analysis of farmyard manure and of sewage sludge; 2Applied as follows: N – calcium ammonium nitrate (27% N); FYM – farmyard manure – average dose of fresh FYM was as follows: 51.42 t/ha/3 years (15.82 t of dry matter/ha/3 years); SS1 – sewage sludge – average dose of fresh sewage sludge was: 30.18 t/ha/3 years (9.38 t of dry matter/ha/3 years); SS3 – high dose of sewage sludge – average dose of fresh sewage sludge was: 90.54 t/ha/3 years (29.49 t of dry matter/ha/3 years); straw was applied in doses of 5 t of dry matter/ha/3 years was applied at the rate of 115 kg N/ha for wheat and Easily extractable glomalin (EEG) and total glo- 50 kg N/ha for spring barley. malin (TG) fractions were performed according to Soil analysis. Topsoil (depth of 30 cm) analyses Wright and Upadhyaya (1998), i.e., to 1 g of ground were performed with air-dried soil samples (≤ 2 mm) dry-sieved soil 8 mL of sodium citrate (20 mmol/L collected after harvest in September 2018. The con- of pH 7.0 – EEG, 50 mmol/L of pH 8.0 – TG) was tent of total organic carbon in air-dried samples of added, followed with autoclaving at 121 °C (30 min – soils, in farmyard manure, and in sewage sludge was EEG, 60 min – TG), cooling down and centrifugation determined using oxidation on the CNS analyser at 5 000 rpm (10 min – EEG, 15 min – TG). In the Elementar Vario Macro (Elementar Analysensysteme, case of the TG, the centrifugation of supernatant Hanau-Frankfurt am Main, Germany). of the same sample was repeated 5 times, until the

Fractionation of humic substances (CHS) was done supernatant no longer showed the red-brown colour according to Kononova (1963) to obtain the pyroph- typical for glomalin. osphate extractable fraction, which represents the The results were assessed using the ANOVA sta- sum of the carbon in humic acids (CHA) and fulvic tistical analysis with Tukey’s test. The Statistica acids (CFA). In brief, CHA and CFA were extracted program (StatSoft, Tulsa, USA) was used. from a 5 g soil sample with a mixture of 0.1 mol/L NaOH and 0.1 mol/L Na4P2O7 (1 : 20, v/v) solution. RESULTS AND DISCUSSION The carbon of humic substances CHS and CHA was determined by an oxidimetric titration method. Individual treatments varied significantly in the

The content of CFA was calculated as the difference amount of organic matter supplied by the fertilisers between CHS and CHA. (Table 2). The highest amount of organic matter (ex- NIRS measurement of glomalin (GNIRS) was per- pressed as the carbon content) was supplied in treat- formed, according to Zbíral et al. (2017). The NIRS ment SS3 (high dose of sewage sludge), 2 439 kg C/ spectra were recorded by an FT-NIR instrument ha/year. Over the experimental period of 22 years, the Nicolet Antaris II (Thermo Fisher Scientific, Waltham, total amount of carbon supplied there was 53 676 kg USA). The reflectance spectra were measured from C/ha. In treatment N + St, it was 15 660 kg C/ha in 4 000 to 10 000/cm, resolution 2/cm. The spectra total (e.g. 29% compared to SS3). In treatment with were processed using the TQ Analyst 8 instrument manure, it was 32 604 kg C/ha (e.g., 60% compared software (Thermo Electron Corporation, Waltham, to SS3). An important quality indicator of organic USA). The NIR spectrometer was calibrated for TG fertilisers is the C/N ratio; the lowest ratio was in the at a completely different data set than the samples case of sewage sludge (7.4/1), manure had a medium of our long-term trials. value (13.4/1), and straw the highest (79.3/1).

592 Plant, Soil and Environment, 66, 2020 (11): 590–597 Original Paper https://doi.org/10.17221/385/2020-PSE

6.5 lar trend was also determined in the case of barley 6 b and maize. These results indirectly inform us about ab ab ab

the relations between individual treatments, as to

) 5.5 a ab h the amount of postharvest residues and mass. / 5 ab t ( Organic fertilisation and the amount of organic 4.5

tt e r matter from postharvest residues and roots were 4 m a

subsequently reflected in the content of soil organic y r 3.5 a

D matter (Table 3). The original content of CSOM in 3 topsoil was 1.26%. Over a period of 22 years, it de- 2.5 creased to 1.10% at the unfertilised control. Other 2 fertilised plots show a slightly increasing tendency. Cont SS1 SS3 FYM1FYM FYM N N + St Fertilised plots did not differ significantly in the 1/21/ +2 N content of C , except for an extremely high dose SOM Figure 1. The yield of winter wheat grain (average of of sewage sludge (SS3). 22 years). Cont – control (no fertilisation); SS1 – sew- An important qualitative indicator of soil organic age sludge; SS3 – high dose of sewage sludge; FYM – matter is humic to the fulvic acid ratio (Kononova farmyard manure; FYM1/2 + N – half dose of farmyard 1963). Generally, the higher the ratio, the higher the manure + N in mineral nitrogen fertiliser; N – mineral quality of soil organic matter. Even though the content nitrogen fertiliser; N + St – spring barley straw + N in of humic acids was significantly lower at the control mineral nitrogen fertiliser unfertilised treatment, significant differences among fertilised treatments were not recorded (Table 3).

Other fertilised plots did not vary. The CHA/CFA ratio To illustrate the yields obtained in individual treat- was the lowest at control (0.812), which did not sig- ments, the average yields of winter wheat grain over nificantly differ from the sewage sludge treatments. a period of 22 years are presented (Figure 1). It clearly It clearly shows that sewage sludge contributes to the shows the lowest yields obtained at the unfertilised formation of relatively unstable humic substances with control plot (3.22 t/ha). Fertilised plots gave the yields a low C/N ratio. The C/N ratio of the applied sewage higher by 57–100%. However, differences among the sludge is nearing the "fast-effect" organic fertilisers, fertilisation treatments were not significant. A simi- such as slurry. The content of humic substances is

Table 3. The contents of different organic carbon fractions and the content of glomalin determined using different methods

Cont SS1 SS3 FYM1 FYM1/2 + N N N + St Average Carbon (%) a bc c b b b b CSOM 1.099 1.365 1.568 1.388 1.314 1.331 1.404 1.353 a c d c bc b ab CFA 0.145 0.178 0.208 0.173 0.160 0.160 0.148 0.167 a b b b b b b CHA 0.118 0.150 0.183 0.175 0.193 0.175 0.178 0.167 a b c bc b b b CHS 0.263 0.328 0.390 0.348 0.353 0.335 0.325 0.335 a ab ab b b b b CHA/CFA 0.812 0.842 0.882 1.011 1.209 1.096 1.213 1.009 a ab ab ab ab a b CSOM/Nt 9.601 9.778 9.661 9.966 10.02 9.731 10.21 9.852 Glomalin (mg/g) EEG 0.364a 0.427b 0.482bc 0.508c 0.493c 0.477bc 0.484bc 0.462 TG 2.185a 2.403b 2.764c 2.639bc 2.717c 2.795c 2.439bc 2.563 a b d c b b bc GNIRS 1.308 1.673 2.100 1.863 1.730 1.668 1.795 1.734

Cont – control (no fertilisation); SS1 – sewage sludge; SS3 – high dose of sewage sludge; FYM – farmyard manure; FYM1/2 + N – half dose of farmyard manure + N in mineral nitrogen fertiliser; N – mineral nitrogen fertiliser; N +

St – spring barley straw + N in mineral nitrogen fertiliser; CSOM – soil organic matter carbon; CFA – carbon in fulvic acids; CHA – carbon in humic acids; CHS – carbon of humic substances; Nt – soil total nitrogen; EEG – easily extractable glomalin; TG – total glomalin; GNIRS – glomalin determined using the near-infrared reflectance spectroscopy 593 Original Paper Plant, Soil and Environment, 66, 2020 (11): 590–597

https://doi.org/10.17221/385/2020-PSE the sum of CHA + CFA. The highest CHS content was In accordance with our results, increased glomalin again at the SS3 treatment (0.39%). content was also observed by Dai et al. (2013) after Different fertilisation systems used in the experi- the manure application, or by Nie et al. (2007) and ment also affected the change of the CSOM/Nt (soil Zhang et al. (2014) after the straw application. Even total nitrogen) ratio in topsoil (Table 3). Even though though Sandeep et al. (2016) recorded an increase a high amount of carbon was supplied in the SS3 treat- in glomalin content after the application of sewage ment, no significant increase of the CSOM/Nt ratio in sludge, the SS1 treatment achieved significantly lower topsoil was observed. The reason is the high amount of glomalin content compared to treatments with the nitrogen supplied to the soil within this treatment. The highest glomalin contents. Based on the statistical highest CSOM/Nt ratio was recorded at the treatment evaluation in Table 3, it was not possible to definitely N + St, which corresponds to the high C/N ratio of determine fertilisation treatment with the highest the input straw (79.3/1). impact on the glomalin content. One of the reasons

The content of CSOM correlated significantly with may be the glomalin stability and slow cycle of its CFA (r = 0.539***) and CHA (r = 0.438***). An even decomposition in soil (Harner et al. 2004). It may tighter linear correlation was calculated for the also be presumed that the influence of individual amount of humic substances (r = 0.572***). At the fertilisation systems on the glomalin content will same time, no significant correlation was found be- manifest more significantly during the longer time tween CSOM and the CHA/CFA ratio (r = 0.174). The horizon of the experiments; it is similar to the con- obtained results confirm that as to the CSOM quality, tent of organic matter in the soil. it is a very diverse set; it was subsequently used for As follows from Table 4, the correlation between testing of the glomalin content as an indicator of GNIRS and CSOM was tight. Surprisingly the relation soil organic matter quality. between TG and CSOM was insignificant, although Soil samples taken after harvest of crops in autumn a positive correlation of glomalin content and CSOM 2018 were analysed. The set comprised all three was reported by many authors (Wright and Upadhyaya blocks; the crops were maize, wheat, and barley. It 1998, Wilson et al. 2009, Dai et al. 2013, Xie et al. followed the results of Steinberg and Rillig (2003), 2015). Contrariwise, Galazka et al. (2017) published who reported slight seasonal oscillations of the glo- the results with a negative correlation between the malin content in soils; thus, the soil analyses were content of TG and CSOM. not carried out during vegetation. Table 3 presents A very important finding is a tighter correlation the contents of easily extractable glomalin and total of glomalin content (EEG, TG, GNIRS) with humic glomalin. The average content of TG was 2.563 mg/kg; substances than with CSOM. A significant correla- for EEG, it was 0.462 mg/kg (i.e., only 18% of TG). tion was also determined between the content of

The determined TG values correspond to the results glomalin (EEG, TG, GNIRS) and CHA, which corre- of many other authors (Wuest et al. 2005, Wilson et sponds to the results published by Šarapatka et al. al. 2009, Luna et al. 2016). The average GNIRS con- tent of all treatments was 1.734 mg/kg. This result Table 4. Pearson correlation coefficients of glomalin corresponds to the values obtained with the same content changes in relationship with different organic method for soils in the Czech Republic; Smatanová carbon fractions and Komprsová (2019) reported the results of large monitoring of arable soils in the Czech Republic EEG TG CNIRS

(13 083 samples) with the median value of 2.51 mg/kg. CSOM 0.379** 0.250 0.766*** Results of the three methods used (EEG, TG, G ) NIRS CHS 0.472*** 0.563*** 0.834*** suggest that significantly lowest glomalin content CHA 0.524*** 0.452*** 0.683*** was obtained at the unfertilised control. In compli- CFA 0.155 0.449*** 0.716*** ance with the results published by Curaqueo et al. CHA/CFA ratio 0.460*** 0.213 0.297* (2011), a positive effect of sole mineral fertilisation on the glomalin content in topsoil was observed in *P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001; EEG – easily extractable our study, too. Also, the combination of mineral glomalin; TG – total glomalin; GNIRS – glomalin determined and organic fertilisation positively influenced the using the near-infrared reflectance spectroscopy; CSOM – soil content of glomalin, which corresponds to the re- organic matter carbon; CHS – carbon of humic substances; sults by Dai et al. (2013) or Sandeep et al. (2016). CHA – carbon in humic acids; CFA – carbon in fulvic acids

594 Plant, Soil and Environment, 66, 2020 (11): 590–597 Original Paper https://doi.org/10.17221/385/2020-PSE

(2019). Similarly, the relationship of the content of Positive correlations of glomalin with humic sub-

TG, GNIRS, and CFA was insignificant. The weakest stances, humic acids, and fulvic acids confirm the correlation was found between the glomalin content hypothesis that the glomalin content may be used as and the CHA/CFA ratio. an indicator of changes of soil organic matter qual- ity. This finding is important, especially in the case 0.70 of easily extractable glomalin and total glomalin. y = 0.0785x + 0.2893 0.65 To determine GNIRS by the NIR spectroscopy r = 0.420** 0.60 method, the essential prerequisite is the proper

) calibration of the machine and thorough validation g 0.55 of this method, as reported by Zbíral et al. (2017); 0.50 ( mg / the importance is confirmed by a significant corre- 0.45

EE G lation of G with easily extractable glomalin and 0.40 NIRS total glomalin determined in our study (Figure 2). 0.35 Surprisingly, lower tightness values were determined 0.30 for the content of easily extractable glomalin and 0.25 total glomalin. 0.20 As shown in Table 4, it is not possible to determine 1.5 2 2.5 3 3.5 which glomalin pool (EEG or TG) is more suitable to TG (mg/g) evaluate the quality of soil organic matter (SOM). The 0.70 y = 0.1651x + 0.1906 EEG method may be preferred for its lower labour in- 0.65 r = 0.552*** tensity. However, the determined EEG contents were 0.60 low, which means a possibility of higher analytical un-

)

g 0.55 certainty. In our case, a conclusive correlation of EEG 0.50 with C /C increased the perspective of the EEG ( mg / HA FA

0.45 method to indicate soil organic matter quality. The EE G 0.40 relative response of the EEG to fertilisation was slightly 0.35 higher than of the TG. Moreover, in case of appropriate 0.30 validation, NIR spectroscopy may also be used, espe- 0.25 cially for larger data sets. A significant positive factor 0.20 is especially the lower labour intensity of the analysis. 1 1.5 2 2.5 Suitability of glomalin content as a possible in- dicator of soil organic matter quality thus appears GNIRS (mg/g) rather perspective. Yet, this conclusion must be 2.4 y = 0.3237x + 0.9593 confirmed by the evaluation of a large data set. It is 2.2 r = 0.513*** also necessary to remind that long-term experiments

have a greater potential to obtain positive results )

g 2 than smaller sets of less differentiated data. On the

( mg / 1.8

other hand, the changes of glomalin content caused

S R I by different fertilisation treatments may be expected N 1.6 G after a longer time interval (min. 10 years). The 1.4 content of glomalin in the soil is a result of several 1.2 factors. Besides fertilisation, it is, e.g., the influence of cultivated crops (Wojewódzki and Cieścińska 1 2012). As reported by Wright and Anderson (2000) 1.5 2 2.5 3 3.5 and Curaqueo et al. (2011), changes in the glomalin TG (mg/g) content are more dynamic at improper soil cultiva- Figure 2. Relationships among different procedures to tion or under drought conditions. the determining of glomalin. EEG – easily extractable glomalin; TG – total glomalin; GNIRS – glomalin deter- Acknowledgment. We thank Ing. Jana Najmanová mined using the near-infrared reflectance spectroscopy; for the CNS analyses and Ing. Lenka Latková for **P ≤ 0.01; ***P ≤ 0.001 glomalin determination.

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