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Effects of food waste compost on the shift of microbial community in water saturated and unsaturated soil condition

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Abstract

Despite the widespread use of food waste compost as a soil organic amendment, there is limited information on how it affects the composition of the microbial community as well as its relationship on soil environmental factors. This study investigated the effects of food waste compost on soil microbial-community composition by using FAME analysis. It was established that the application of food waste composts in water saturated paddy and unsaturated upland soils increased pH levels, electrical conductivity (EC) values, total carbon (TC), and ESP contents. It also increased the total phospholipid fatty acid (T-PLFA) and fungi resulting in a significant rise in the fungi to bacterial ratio. Furthermore, microbial community composition shifted depending on the quantity of food waste compost applied after crop harvest in both paddy and upland soils. Also, a positive correlation was found between changes in soil microbial community and changes in TC, EC, and water availability for crop growth. These results suggest that soil fertility and its microbial composition depends on the amount of food waste compost applied in both water saturated the paddy and unsaturated upland soils.

Introduction

More than 5 million tons of food waste is produced in Korea annually, of which approximately 40% is recycled through composting [1]. Food waste compost supplies organic matter that confers significant improvement of soil properties such as soil bulk density and water holding capacity, etc. [2]. With inherently higher N, P and K concentrations amounting to 4, 2 and 1% respectively, food waste compost could be harnessed as a fertilizer for crop production [3]. The major impediment to its usage in agricultural production is the potential risk of inducing soil salinity since food waste is contaminated with salt.

High salinity in food waste results in poor stabilization, lower efficiency of solids degradation during the composting process [4], and incomplete maturity of food waste compost. Consequently, NaCl content typifying salinity in food waste compost was established below 2% by law for sustainable crop cultivation. However, there is limited information on the effects of food waste compost on relation to soil productivity and properties. Application of food waste compost to soil culminates into increased pH and in electrical conductivity (EC) due to the supply of Na ions to the soil [3]. However, sodium (Na) input from food waste compost, might have a negative effect on the microbial process due to the induced-high osmotic pressure induced concomitantly scaling-down crop productivity.

Soil microorganisms are the engine of nutrient cycling. Soil microbes degrade soil organic materials in the soil releasing nutrients for plant uptake through the mineralization process with the rate of all these processes dependent on microbial population and activity. Generally, organic amendment in arable soil might stimulate microbial activity [1, 5], and a shift in microbial community composition [6]. These shifts are induced alongside changes in water contents, carbon substrate, and soil pH depending on the crop cultivation condition such as fertilization and irrigation [7], which also can in turn alter soil fertility and crop production [8, 9]. We hypothesized that water management regimes in upland and lowland could be the main factor influencing microbial community composition, because microbial species was adapted to soil environmental conditions. Unfortunately, there is little information on the relationship between soil properties and microbial community composition in different water management regimes [10, 11]. Therefore, this study aimed to evaluate the effect of food waste compost addition on soil chemical properties and microbial community composition using a biomarker of fatty acid in upland and lowland cultivation condition.

Materials and methods

Experimental setup

The soil used for this study was Wansan series, a member of the fine loamy, micaceous, mesic family of Typic Hapludults, located in the National Institute of Agricultural Science (NAS) experiment area (35°49′28.61″N, 127°2′42.77″E). The soil pH and electrical conductivity (EC) were 7.28 and 0.73 dS m−1, respectively, and soil organic carbon was 17.3 g kg−1 (Table 1). The soils were root-picked and sieved with a 4 mm mesh sieve before the pot experiment. The food waste compost contained 41.4%, 3.0%, 3.29%, and 1.20% of total C, N, P and K, respectively (Table 2). The experiment was conducted with two treatment factors which included water management in both lowland (rice) and upland (pepper) conditions, and the levels of food waste compost applied to the soil. Food waste compost was applied to the soil at five different rates of 0, 10, 20, 40, and 60 Mg ha−1 of fresh materials (about 50% of water content) with each of the rates replicated thrice. Each Wagner pot (25 cm in diameter and 30 cm in height) was filled with 14.7 kg of soil and adjusted to a bulk density of 1.2 g cm−3. Then, rice (Oryza sativa L.) and pepper (Capsicum annuum L.) were transplanted into Wagner pots on June 15, 2015 and were kept under greenhouse conditions. For rice and pepper cultivation, inorganic fertilizers were applied at nitrogen (N)-phosphorus (P)-potassium (K) 110-45-57 and 190-112-149 kg ha−1, respectively. The basal fertilizer application supplied 50%, 100%, and 50% of N, P, and K, respectively. 20% of N was top-dressed on the 15th day after transplanting, and the remainder (30%) of N and K were applied during near heading.

Table 1 Chemical properties of the basic soil used in the experiment
Table 2 Chemical composition of food waste compost mixed within the 10 cm depth of the potted surface soil

Sampling and analysis

Soil samples for soil properties and microbial community composition were collected at the surface soil (0–10 cm) of rhizosphere in each pot treatment by a core with 2 cm diameter after crop harvest. The soil sample was divided into two groups. One group was dried with air drying condition, and sieved 2 mm mesh for chemical properties. The other soil sample was stored at − 80 °C and lyophilized for before FAME analysis. Soil pH and EC were determined through a suspension sample with a soil to water ratio of 1:5 and were measured using digital pH and EC meter. Soil organic carbon and total nitrogen were determined by the elemental analyzer (Vario Max, Elmentar). Soil available phosphate (Av. P2O5) was analyzed by Lancaster Methods (NAE, 2001). Briefly, 5 g of soil was extracted by mixture solution (pH 4.25) with 0.33 M acetic acid, 0.15 M lactic acid, 0.03 M ammonium fluoride 0.05 M ammonium sulfate, and 0.2 M sodium hydroxide. Exchangeable sodium (Ex. Na) and cation exchange capacity (CEC) were determined using 1 M ammonium acetate at pH 7.0. Firstly, 5 g of soil was extracted with 50 mL of 1 M NH4OAc for 3 h. Ex. Na was determined ICP-AES in this solution. Secondly, 0.2 M CaCl2 re-extracted NH4 ion from remained soil. Kjeldahl methods were employed in the measurement of the NH4+ concentrations. Exchangeable sodium percentage (ESP) was calculated as the proportion of exchangeable Na+ to cation exchange capacity (CEC).

Microbial community composition

Microbial community composition was determined using the modified ester-linked fatty acid method. This method was conducted in three steps. Firstly, fatty acid was extracted from 3 g of lyophilized soil with 10 mL of 0.2 M KOH for 1 h at 37 °C on 180 rpm of orbital steering. Then, solution pH was adjusted with 1.0 M acetic acid and inserted 10 mL of n-hexane was poured into 50 mL centrifuge tube. After vortexing for 1 min, the mixture solution was centrifuged at 1600 rpm for 20 min. Finally, 5 mL of the supernatant (hexane layer) was transferred into a 10 mL tube and evaporated to N2 gas. The residue was dissolved in 170 μL of 1:1 solution of hexane and methyl-t-butyl ether, and then 30 μL of 0.01 M methyl nonadecanoate (19:0) was added as an internal fatty acid. Fatty acid was quantified and identified using a Hewlett-Packard 5890 Series II (Palo Alto, CA) and MIDI software following MIDI microbial calibration standards. HP Ultra 2 capillary column (5% diphenyl-95% dimethylpolysiloxane, 25 m by 0.2) was used with column temperatures varied between 170 and 270 °C at 5 °C per min. Total FAME summed each fatty acid quantity. Total bacterial biomarkers i15:0, a15:0, 15:0, i16:0, 16:1ω7, i17:0, a17:0, 17:0, cy17:0, 18:1ω7 and cy19:0, which used branched fatty acids of iso- and ante iso series for gram(+) and cy17:0 for gram(−) bacteria were utilized. Fungi bio-markers used were: 18:2 ω6,9 and 18:3ω6 while The 16:lω5 served as arbuscular mycorrhiza. Fungal to bacterial ratio was determined from the total fungi and bacteria bio-markers (n mol g−1).

Data analysis

All data were analyzed with a general linear model in R 3.5.2. The least significant difference deviations (LSD) of the mean values of each plot were compared through ANOVA test at p < 0.05. To analyze the change of microbial community composition, a principal component analysis (PCA) was performed on the proportion of individual fatty acids as mol%. Principle component (PC) score was assessed by using ANOVA at p < 0.05. Redundancy analysis (RDA) was used to test the relationships between soil properties and microbial community composition in soil under different water conditions and food waste compost application rates. The contribution of soil properties to changes in soil microbial composition was assessed with the Monte Carlo permutation test observing strict adherence to the 999 random permutations basing on p-levels < 0.05 [12]. Soil properties significantly correlated with the changes in microbial community composition in the plot. Vectors of greater magnitude and forming smaller angles with an axis were more strongly correlated with that axis [13, 14].

Results and discussion

Soil properties

Applying organic matter to the soil can also improve its properties and promote effective decomposition by increasing the activity of soil microbes thus enhancing agricultural production [15]. The application of food waste compost to saturated and unsaturated soils had a significant effect on the soil properties (Table 3). All rates of food waste compost applied to both saturated and unsaturated soils increased soil pH, EC, T-C, T-N, Ex. Na, and ESP as were determined after harvesting rice and pepper. Studies by Lou et al. [16] and Abro et al. [17] indicated that addition of organic amendments into soil increased soil carbon and nitrogen contents subsequently improving soil quality. Soil organic carbon in our current study was higher in saturated soil as compared to unsaturated one. The reason for this observation might lie in the differences in the degree of soil water saturation between the rice and pepper cultivated soils. Microbial degradation of organic matter in the soil is dependent on oxygen availability which in turn relates to the water saturation levels with slower rates of degradation reported in anoxic soil conditions [18, 19]. Degradation of soil organic carbon in the saturated soil might be restricted carbon substrate availability by microbes as well as oxygen supply into the soil. In contrast, aerobic soil condition would highly influence at the decomposition of soil organic carbon compared to the saturated paddy like anoxic status.

Table 3 Yields and chemical properties in soil applied with food waste after harvesting rice and pepper at harvesting stage

Soil pH and EC might be important factors crop productivity as well as microbial population and activity in the soil. Nutrient supply from soil to plant could be affected by declines in microbial population and activity caused by Na ions released from food waste compost into the soil. As Lou et al. [16] and Abro et al. [17] found Soil pH could change the microbial composition because the bacteria population was dominant at around neutral pH [20]. As shown in Table 3, soil pH slightly increased with increasing food waste compost application rates and the patterns of increment were similar in both soil water saturation conditions. These results therefore, indicate that food waste compost might impact the microbial status of the soil through raising soil pH. Besides soil pH and EC contents could also affect crop growth by inhibiting water uptake and inducing ion toxicity around the rhizosphere [21]. Rice grain yield decreased with the increasing rates of food waste compost applied. Conversely, pepper yield increased with increasing rates of food waste compost up to the rate of 40 Mg ha−1 beyond which it declined. Therefore, food waste compost application affects soil properties, nutrients availability and increases potential risks for retardation of crop productivity.

Microbial community composition

Adding organic materials to soil is very important in increasing soil organic carbon levels and improving soil fertility and soil microbial activity [22,23,24]. The microbial community composition shown in Table 4 indicates that food waste compost application enhanced the total PLFA significantly in the two soil water management conditions under rice and pepper cultivation. However, total PLFA in unsaturated soil with pepper cultivation was higher than in the saturated soil. Fugal PLFA was enhanced with increasing application rates of food waste compost in both the saturated and unsaturated soil conditions while the changes in bacterial PLFA differed across the saturated and unsaturated soils. Unsaturated soil conditions culminated into enhanced total bacterial PLFA, i.e. both gram-positive and gram-negative bacteria, although the gram-positive bacteria were the most dominant group. However, there was no observable change in total bacterial PLFA when food waste compost was applied to the saturated soil. Nevertheless, gram-negative bacteria were the most dominant type under this soil condition. Irrespective of soil water saturation conditions, the relative fugal PLFAs positively correlated with food waste compost application rates and their concentrations were significantly higher than bacterial PLFAs at any given compost application rate.

Table 4 Microbial community in the soil of paddy and upland applied food waste compost at harvest stages

Individual PLFAs of the soil microbes may be sensitive indicators of soil water condition [25, 26]. The ratio of fungal-to-bacterial PLFAs is an important indicator of the changes in the relative abundance of soil microbial communities [27, 28]. The differences in fungal to bacterial PLFA ratios between the two soil water conditions would have been due to differences in carbon substrate availability and osmotic pressure induced by food waste compost. It has been reported that fungi contribute to the nutrient cycling recalcitrant C, thereby improving soil structure [29,30,31]. Fungal PLFA composition increased with increasing application rates of food waste compost in both saturated and unsaturated soils because fungi converted the recalcitrant carbon contained in food waste in labile C forms which proliferated microbial generation as indicated by Cao et al. [13]. There are several previously concluded studies for example by Frostegård et al. [27] and, Bååth and Anderson [28] that have reported high fungal-to-bacterial PLFA ratios due to the higher SOC levels in agricultural soils. The variations in the two kinds of bacteria (gram positive and negative bacteria) were due to differences in soil salinity tolerance. Gram-positive bacteria are highly tolerant to salt because their peptidoglycan layers the in cell wall are thicker than those of the gram-negative bacteria. That kind of a cell structure is most likely to render resistance to changes in osmotic pressure triggered by changes in the soil environment such as salinity and soil saturation as was in the current study. Our results therefore, indicate that food waste compost induced changes in microbial community composition depending on the degree of soil water saturation.

Relationship between soil microbial community composition and soil properties

Microbial communities respond to alterations in the soil environment. The principal components analysis (PCA) was conducted to confirm the changes in the microbial community compositions in the soils at two different saturation levels treated with food waste compost. The PC 1 and PC 2 in the PCA bi-plot attributed 60.7 and 11.4% of the total variation in the microbial community to the rate of food waste compost applied in both the saturated and unsaturated soils (Fig. 1). The microbial community varied distinctly between the saturated and unsaturated soil and changed with levels of food waste compost. The microbial community composition correlated significantly with the PC 1(r = 0.67, p < 0.01) and PC 2 (r = 0.42, p < 0.01) axis. In this study, bacteria community was shown different patterns under water regimes with food waste compost application. Especially, Gram positive bacteria significantly decreased in water saturated soil (Table 4), but fungi and AM fungi increased under water saturated and unsaturated soils. Water status was an important factor for soil microbial community due to nutrient availability such as carbon substrates [11, 32, 33]. Soil water regimes for crop cultivation might affect the partitioning and allocation of plant photosynthathes by depending soil nutrient status [34]. Also, roots exduates composition might be key factors affecting the shifts of soil microbial communities [35, 36].

Fig. 1
figure1

Principal component analysis (PCA) score plots of the microbial-community structures in water saturated paddy (left) and unsaturated upland (right) soils at harvesting. FWC food waste compost. The numbers after EWC of the code name indicate the fresh-FWC level (0, 10, 20, 40, and 60 Mg FWC ha−1). The data are presented as the ± standard deviation of the mean of three replications

Redundancy analysis (RDA) was utilized to test the relationship between the microbial community composition and soil properties at different rates of food waste compost and in varying soil water conditions. The environmental variables pH, EC, TC, TN, CN, Ex. Na, ESP, and yield were used to determine Monte Carlo permutation tests (p < 0.05). Seven environmental variables significant on the first axis (F = 21.12, p < 0.01) and all canonical axes (F = 4.60, p < 0.01). TC (F = 11.03, p < 0.01), EC (F = 8.35, p < 0.01), soil pH (F = 5.07, p < 0.01), and Yield (F = 2.84, p < 0.05) were influenced with the variations in microbial community composition. The distinct differences in the microbial communities of the saturated and unsaturated soils resulted from differences in total carbon, and was associated with lower pH values and salinity (Fig. 2). Soil microbial communities was affected from the changes of soil environmental condition under soil water regimes with organic amendments.

Fig. 2
figure2

Relationship between microbial communities and soil in water saturated paddy (left) and unsaturated upland (right) soils at harvesting. FWC food waste compost. The numbers after FWC of the code name indicate the fresh-FWC level (0, 10, 20, 40, and 60 Mg FWC ha−1). The data are presented as the ± standard deviation of the mean of three replications

Availability of data and materials

The datasets supporting the conclusions of this article are including within the article.

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Acknowledgements

This study was supported by Rural Development Administration (PJ010925), Republic of Korea.

Chang Hoon Lee is the first author.

Funding

No funding was received.

Author information

CHL, SJP and MSK conceived and designed the experiments. CHL, HYK and SHK conducted the experiments, analyzed the data and generated the figure and tables. HYH, HIJ, DL, and SYH reviewed the results of experiments and examined English grammar of the manuscript. CHL, TKO and SHK supervised the whole project and CHL and SHK wrote the manuscript. All authors read and approved the final manuscript.

Correspondence to Taek Keun Oh or Seong Heon Kim.

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Keywords

  • Food waste compost
  • Microbial community
  • Water saturation
  • Carbon
  • Salinity