Abstract
Saline–alkaline conditions can limit crop productivity and the role of soil microbes in nutrient cycling in arid and semi-arid regions throughout the world. A better understanding of how soil amendments and plant varieties affect rhizosphere microbial communities in saline–alkaline environments is important for the development of sustainable and productive agricultural systems under these challenging conditions. The objective of this study was to determine the effect of organic soil amendments on crop yield, soil physicochemical properties and rhizosphere bacterial communities of two oat cultivars in a saline–alkaline soil. The experiment was conducted in a semi-arid region of Northern China and involved growing two oat cultivars with varying levels of saline–alkaline tolerance under four different amendment treatments: (1) control (no amendments), (2) bio-fertilizer, (3) rotten straw, and (4) combination of bio-fertilizer and rotten straw. The combined bio-fertilizer and rotten straw amendment treatment resulted in the highest oat yields, reduced soil pH, and increased soil salt content for both cultivars. Baiyan2 (tolerant cultivar) had a higher bacterial α-diversity, relative abundance of Proteobacteria and Acidobacteria, and lower relative abundance of Firmicutes compared to Caoyou1 (sensitive cultivar). The rotten straw treatment and combined amendment treatment decreased bacterial α-diversity and the abundance of Proteobacteria, and increased the abundance of Firmicutes, which were positively correlated with soil salt, available nitrogen, phosphorous and potassium for both cultivars. Our study suggested using tolerant oat cultivars with the combined application of rotten straw and bio-fertilizer could be an effective strategy in remediating saline–alkaline soils.
Similar content being viewed by others
Introduction
Soil saline–alkalization is a key environmental factor that severely limits the functional roles of soil microbes in arid and semi-arid regions globally1,2. It has been suggested that crop management practices such as organic amendments (e.g., bio-fertilizer and rotten straw) are more effective than inorganic amendments (e.g., gypsum3) for altering soil nutrient and physiochemical properties, shifting the composition of soil microbial communities and increasing crop yields4,5. Bio-fertilizers are natural organic amendments6,7,8, which have been widely used in saline–alkali soils9 to improve soil fertility and productivity10. Bio-fertilizers refer to the use of inoculants composed of soil microorganisms that promote plant growth by increasing the uptake or availability of primary nutrients to the host plant11. Plant straw, a precursor for humus, is a major lignocellulose waste produced in agricultural processes and has been traditionally used for soil amendments in the form of compost. Tan et al.12 and Han13 found that the decay and nutrient release rate of rotten straw application was faster than direct straw application. In addition, the application of rotten straw has been shown to have a positive effect on soil physicochemical properties (e.g., soil organic carbon and potassium content) and enzyme activity12,14. There is increasing evidence that the combined application of bio-fertilizer and rotten straw amendments may be an effective strategy to remediate saline–alkaline soil properties and improve soil productivity in a saline–alkali ecosystem15,16.
Applications of bio-fertilizer and rotten straw can potentially alter the bulk and rhizosphere soil environment and microbial community under saline–alkaline conditions. Previous studies have observed that bio-fertilizer application increased the abundance of disease suppressive microorganisms, such as Acidobacteria and Firmicutes17,18, and increase soil bacterial diversity19,20,21,22. In a long-term experiment, Zhao et al.23 found that high rates of maize straw addition altered the structure of soil microbial communities and increased enzyme activities. However, straw additions under controlled conditions were linked to decreased microbial diversity and altered community structures24. This shift in the microbial community appears to be linked to the improvement of environmental factors such as soil pH and soil nutrient status, which have been identified as important drivers of bacterial community assembly and diversity in both acid and alkaline conditions25,26,27,28,29. Soil enzymes (e.g., catalase, urease, alkaline phosphatase and sucrase) are sensitive to changes in the soil environment and play crucial roles in nutrient cycling and are tightly linked to the bacterial community27. Soil microorganisms are essential to the soil environment and play vital roles in soil biogeochemical cycling in agricultural systems30,31, and are particularly important in the rhizosphere32. As a result, soil pH, salinity and enzyme activities are relevant soil indicators to evaluate the impact that soil amendments have on the soil bacterial community and general soil health in saline–alkaline ecosystems.
Bio-fertilizers and rotten straw amendments have also been shown to benefit plant establishment32. However, plant species and genotypes exhibit different responses to soil amendments via enhanced rhizosphere microbial communities33,34,35,36,37,38. For example, alfalfa rhizosphere microbial communities have been shown to differ between genotypes33,34, while no differences have been observed in different cultivars of soybean, canola, wheat, rice or maize35,36,37,38. To this date, there has been no research focused on how soil organic amendments affect the rhizosphere bacterial community structure of plant cultivars with a range of saline–alkaline-tolerance. Oat (Avena nuda L.) is considered a pioneer crop for improving saline soil in arid and semi-arid areas because of its saline–alkaline tolerance39,40. Different oat genotypes exhibit different saline–alkaline tolerance and productivity under these conditions41,42,43 and it is important to understand how oat varieties with differing saline–alkaline tolerance respond to soil amendments.
We hypothesized that the addition of bio-fertilizer and rotten straw amendments to saline–alkali soil will alter rhizosphere soil physicochemical properties, microbial communities and improve the productivity of oats with different saline–alkaline tolerance. To test this hypothesis, a field experiment was conducted in a typical saline–alkaline region and involved growing two oat cultivars with the following treatments: control (no amendments), bio-fertilizer, rotten straw, and combined bio-fertilizer and rotten straw. The objectives of this study were to analyze the effects of rotten straw and bio-fertilizer on: (1) soil physicochemical properties, (2) enzyme activities, (3) yield of two oat cultivars with different saline–alkali tolerance, and (4) diversity and composition of rhizosphere bacterial communities (Table 1).
Results
Oat productivity
The grain, dry grass and fresh grass yields of Baiyan2 was significantly higher than Caoyou1 (Fig. 1). The bio-fertilizer amendment significantly increased the grain yield of both cultivars, but maximum yields were observed with the combined application of bio-fertilizer and rotten straw. There was no effect of the amendments on the fresh and dry grass yields of the Baiyan2 cultivar. However, the combined amendment treatment significantly increased the grass yield for Caoyou1, which produced similar yields as the Baiyan2 cultivar.
Effect of soil amendments on grain yield and grass biomass production of two oat cultivars. CK was negative control; F was application of bio-fertilizer; R was application of rotten straw; RF was co-application of bio-fertilizer and rotten straw.
Rhizosphere soil properties
Compared to the control, the combined amendment treatment significantly reduced soil pH, increased soil water content, but also led to higher salt content (Table 2). Rotten straw significantly increased rhizosphere soil available potassium (AK), available phosphorus (AP) and available nitrogen (AN) for both cultivars, whereas the bio-fertilizer had no significant effect on these soil nutrients compared to the control. Cultivar had significant effect on AP content as Baiyan2 had a significantly higher AP content compared to Caoyou1.
Catalase and alkaline phosphatase activity were significantly increased by the rotten straw amendment for Baiyan2, while significantly increased by the bio-fertilizer amendment for Caoyou1. For both cultivars, the rotten straw amendment significantly increased sucrase activity, and the combined amendment treatment significantly decreased urease activity.
Rhizosphere bacterial community
All of the organic amendment treatments significantly reduced the observed richness of the rhizosphere bacterial community associated with Baiyan2, whereas the combined amendment treatment significantly increased the observed richness of the rhizosphere bacterial community associated with Cayou1 (Fig. 2 and Table 3). Furthermore, cultivar significantly affected the estimated richness (Chao1) and diversity (Shannon index) of the rhizosphere bacterial community, with Baiyan2 exhibiting higher levels than Caoyou1 (Table 3). Amendment treatments that included rotten straw significantly decreased the rhizosphere bacterial diversity for Cayou1, and the combined amendment treatment significantly decreased the bacterial diversity for Baiyan2. The permanova and PCA results revealed that cultivar (C), amendment (M) and C × M interactions significantly affected the rhizosphere bacterial community composition (Fig. 3). In particular, the rhizosphere bacterial community associated with amendment treatments that included rotten straw were distinct and separated along the first axis (PC1, Fig. 3) from those associated with treatments that did not include rotten straw (Fig. 3). The rhizosphere bacterial community associated with each cultivar were distinct and separated along the second axis (PC2), with the exception of the combined amendment treatment where both cultivars clustered together.
Effect of soil amendments on soil bacterial α-diversity in the rhizosphere of Caoyou1 (a) and Baiyan2 (b) oat cultivars. A1 and B1 were negative control; A2 and B2 were application of bio-fertilizer; A3 and B3 were application of rotten straw; A4 and B4 were the combined application of bio-fertilizer and rotten straw. The same as below.
Principal component analysis (PCA) of the rhizosphere soil bacterial community associated with the two oat cultivars and organic soil amendment treatments.
The dominant rhizosphere bacterial phyla were Proteobacteria (27.28–41.09%), Actinobacteria (24.17–30.36%) and Firmicutes (2.82–22.95%) across all treatments (Fig. 4). Baiyan2 had a higher abundance of Proteobacteria (i.e. Azotobacter, Massilia Pseudomonas) and lower the abundance of Firmicutes than Caoyou1 (Table S2). Rotten straw significantly increased the abundance of Firmicutes, and decreased the abundance of Proteobacteria and genera Massilia and Nocardioides (Fig. 4, Tables S2 and S3). In contrast, the bio-fertilizer significantly increased Massilia and Nocardioides for Caoyou1, and significantly increased Azotobacter and Pseudomonas for Baiyan2 (Table S3).
Effect of organic soil amendments on the rhizosphere bacterial community structure at the phylum level.
Correlation analysis
The RDA results revealed that the oat rhizosphere bacterial communities associated with treatments that included rotten straw were positively related to soil salt, AK, AP and grass yield for both cultivars (Fig. 5 and Table S4). Spearman correlation analysis showed that soil salt, AK, AP and AN were positively correlated with the relative abundance of Bacillus, Pseudarthrobacter and Planomicrobium, while negatively correlated with the relative abundance of Sphingomonas, Massilia, Nocardioides and Pseudomonas. Oat yield and ALP were negatively correlated with the relative abundance of Massilia (Fig. S1). Grain yield, soil salt, AK, AP, and AN were positively correlated with each other, and negatively correlated with soil pH and urease.
Redundancy analysis (RDA) of the rhizosphere bacterial community, soil properties and oat productivity measurements of both cultivars in different amendment treatments. The parameters were: GY grain yield, FGY fresh grass yield, Salt soil salt content, AK soil available potassium, AP soil available phosphorus.
Discussion
Change in oat productivity and rhizosphere soil environment
The combined application of bio-fertilizer and rotten straw resulted in the highest oat productivity, particularly in respect to grain yield and dry biomass production. Turmuktini et al.15 also reported that the combination of composted straw and biological fertilizer significantly increased rice yield. More specifically, we found that the combined amendment treatment was able to increase grain yield and biomass productivity of the saline–alkaline sensitive oat cultivar to comparable levels of the tolerant cultivar. Reduction of soil pH and promotion of nutrients in the rhizosphere appear to be linked to increased oat productivity. One of the drawbacks of the combined amendment treatment was the higher salt content of the soil. This was possibly due to the combined organic materials containing higher salt content than the bio-fertilizer or rotten straw applications alone44. In addition, the soil salt content moved with the moisture and the preservation of soil moisture likely promoted the retention of salt45.
In our study, the addition of rotten straw increased the levels of available nutrients (N, P, K) in the rhizosphere soil, which appears to be linked to the added nutrients from these amendment materials. Tan, et al.12 found that saline alkaline soil nutrients were directly improved when rotten straw was added due to the quick release of nutrients. The other reason was linked to the greater reduction in soil pH with bio-fertilizer and rotten straw addition, which may increase the availability of N, P and K in solution46. Overall, our results indicated that the combined application of rotten straw and bio-fertilizer was an effective management tool for improving soil nutrient availability and productivity of oats in saline–alkaline soils.
Shift in rhizosphere bacterial community
Our study demonstrated that the soil organic amendments had a contrasting effect on the rhizosphere bacterial community associated with the oat cultivars (i.e., richness decreased in Baiyan2 and increased and Cayou1), with Baiyan2 exhibiting a higher overall richness compared to Caoyou1 under saline–alkaline conditions. Our observations showed that the addition of bio-fertilizer alone significantly increased Proteobacteria Massilia for Caoyou1 and increased Proteobacteria (i.e. Azotobacter and Pseudomonas) for Baiyan2, which may be caused by lower soil salt content and available nutrients in this study. Previous studies observed that the application of bio-fertilizer increased the abundance of beneficial microorganisms such as Azotobacter that can increase crop yields49,50.
The application of rotten straw induced a strong shift in the composition of the rhizosphere bacterial community associated with both oat cultivars. More specifically, rotten straw decreased the abundance of Proteobacteria (i.e. Massilia) and Actinobacteria (i.e., Nocardioides), which were negatively correlated with soil salt, and increased the relative abundance of Firmicutes (i.e. Bacillus and Planomicrobium), which was positively correlated with AK, AP and AN in this study. Other studies have also shown that rotten straw can cause higher N availability and/or lower C/N litter input51 and higher salinity in the soil that can lead to lower abundance of Proteobacteria and Actinobacteria52. Massilia and Nocardioides were widely reduced in the process of plant litter decomposition and may be driven by shifts in nutrient availability or pH conditions53,54. Similar to Zhao et al.23 and Sun et al.55, the relative abundance of Firmicutes was increased and Acidobacteria was decreased by straw addition. Zhao et al.29 reported that K+ ions play a critical role in promoting bacterial growth (e.g. Firmicutes) as the protons are replaced to cope with high external Na+ stress. Thus, the application of rotten straw promoted beneficial microbial taxa such as Firmicutes and enhanced soil enzyme activities main caused by shifted soil nutrients, which are good for soil health56.
Rhizosphere bacteria are essential component of the soil environment and play vital roles in soil–plant systems30,31, which are affected by crop cultivar genotypes33,34. Our results showed that Baiyan2 (tolerant cultivar) had higher bacterial richness and diversity than Caoyou1 (sensitive cultivar). The rhizosphere bacterial community associated with Baiyan2 was characterized by a higher relative abundance of beneficial Proteobacteria genera (i.e. Azotobacter, Massilia and Pseudomonas49,50) and lower relative abundance of Firmicutes (i.e. Bacillus) compared to Caoyou1. This difference may be due to variation of root exudates produced by the two oat cultivars, as root exudate profiles have been shown to vary among varieties and cultivars of the same species57,58.
Compared the bacterial communities appeared in soil amendments (bio-fertilizer and rotten straw) with that detected in different treatment soils, our data revealed that soil organic amendments appear to alter the rhizosphere bacterial communities primarily via changes to the soil physicochemical properties, rather than the direct input of exogenous bacterial species from organic materials in the saline–alkali soil. It was reported that most bacteria in the organic materials are adapted to their environments and are likely less competitive than indigenous bacterial species in the soil47,48.
Altered rhizosphere soil enzyme activity
Soil enzymes are involved in the biological cycling of carbon, phosphorus and nitrogen in soil23,59,60 and are regarded as potential indicators of soil nutrient cycling2,61. The improved enzyme activities in rhizosphere soil from our study could be attributed to the exogenous addition of enzymes from the organic amendments56, from the contributions of soil microorganisms62, and/or a result of the increased C and N substrate availability2,4,61,63. Rotten straw and bio-fertilizer improved soil catalase, alkaline phosphatase and sucrase activities for both cultivars, which all were related to bacterial communities, but had no significant effect on oat yields in this study. Shi et al.27 showed that soil enzymes are sensitive to changes in the soil environment and are tightly linked to the bacterial community. However, the combination of bio-fertilizer and rotten straw inhibited urease activity in saline–alkaline soil, which may be due to the higher salt content in rhizosphere soil or addition of N from organic materials64. The reduced urease activities in the combined amendment treatment may have been a limiting factor in maximizing the oat productivity.
Mechanisms of improving oat productivity by bio-fertilizer and rotten straw amendments
In the saline–alkaline environment, the productivity of both oat cultivars were improved through the application of the bio-fertilizer, rotten straw and the combined amendment treatments. This was primarily linked to a reduction in soil pH, increased availability of nutrients, and shift in the rhizosphere bacterial community and enzyme activities. With the process of soil health improvement at this study site, Baiyan2, a tolerant cultivar, has a higher relative abundance of potentially beneficial bacteria (i.e., Azotobacter and Pseudomonas), which would then foster greater crop yields than Caoyou149,50. Although Caoyou1 is a sensitive cultivar, the oat yields and soil nutrients significantly improved along with a shift in the rhizosphere bacterial community following the application of rotten straw and bio-fertilizer. However, it is important to consider a tolerant cultivar with the highest yields to avoid increasing salinity issues through the application of organic amendment in saline–alkaline land. Our study indicates that tolerant crops with the combination of rotten straw and bio-fertilizer applications should be an effective strategy in remediating saline–alkaline land in semi-arid regions, which could be further investigated in long-term studies.
Materials and methods
Study site
The field experiment was conducted from 2016 to 2017 in the Tumote Zuoqi Hailiu village (East 111°22′30″, Latitude 40°41′30″) of Hohhot, Inner Mongolia, China. At the experimental site, the mean annual temperature is 13.2 °C and mean annual rainfall is 410 mm. Soil samples were collected at the beginning of the experiment in April 2016 to determine the baseline soil physicochemical properties (Table 1).
Characterization of organic soil amendments
Rotten straw was made using corn straw that was cut into pieces of 5 cm in length and fermented without oxygen from Sep. 2015 to Apr. 2016 and from Sep. 2016 to Apr. 2017 for the 2016 and 2017 experiments, respectively. Physicochemical properties of the bio-fertilizer and the rotten straw were determined using the same methods as described for the soil samples below.
Experimental design and management
The experiment was designed as a 4 × 2 factorial experiment in which the 8 treatments were arranged in a randomized complete block design with three replications for each year (2016 and 2017). Each block had an area of 5 m × 4 m. A (Caoyou1, saline–alkaline sensitive cultivar) and B (Baiyan2, saline–alkaline tolerant cultivar) represented two oat cultivars with different saline–alkaline tolerance41. The treatments were as follows: A1 and B1 (no amendments); A2 and B2 (1500 kg ha−1 year−1 bio-fertilizer); A3 and B3 (12,000 kg ha−1 year−1 rotten straw); A4 and B4 (combined 1500 kg ha−1 year−1 bio-fertilizer and 12 000 ha−1 year−1 rotten straw). Oats were seeded at a rate of 150 kg ha−1 year−1 and row spacing of 25 cm. Diammonium phosphate was applied at a rate of 150 kg ha−1 year−1 (DAP: 18-46-0) as the basal fertilizer for each plot. Bio-fertilizer and rotten straw were broadcast uniformly on the soil surface and incorporated into the soil (about 15 cm) by cultivation with a rotary tiller before sowing.
Field and laboratory measurements
Soil samples were randomly taken from three points within each block at the pre-seeding and heading stages. Rhizosphere soil was collected by excavating oat plants along 50 cm of a row by gently shaking off the loose soil and retaining the soil within 2 mm of the oat root using a bristle brush. Each sample was sieved through a 2 mm mesh screen and divided into three subsamples: fresh soil was stored at 4 °C, air-dried for soil physicochemical and enzyme activity assays, and soil for DNA extraction stored at − 80 °C.
Determination of the soil physicochemical properties
Soil water content (SW, %) was determined by oven-drying at 105 °C until stable weight and calculated according to the following formula: SW = (soil fresh weight − soil dry weight)/soil dry weight*100. Soil pH was determined by pH meter (STARTER3100) at a ratio of 1:5 for soil to RO water. The soil salt content (Salt) was determine using an electrical conductivity meter (STARTER3100C) at a ratio of 1:2.5 for soil to RO water. Soil available potassium (AK) was determined in 1 M of ammonium acetate extracts by flame photometer (FP6410). Soil available phosphorus (AP) was extracted with 0.5 M NaHCO3 and determined using the molybdenum blue method65. Soil available nitrogen (AN) was determined by diffusion methods66.
Determination of the soil enzyme activities
Catalase activity was assayed by the potassium permanganate titration method67,68,69. Alkaline phosphatase activity was assayed by the disodium phenyl phosphate method67,68,70. Urease activity was assayed by the colorimetric method67,68,71. Sucrase activity was assayed with the 3,5-dinitrosalicylic acid method67,72.
High-throughput sequencing
Soil DNA Isolation Kit (MO BIO Laboratories, Inc., Carlsbad, CA, USA) was used to extract DNA from fresh soil samples following the manufacturer's protocol. 1% agarose gel (1% AGE, 100 V/40 min) was used to test the concentrations and purities of DNA and then stored at − 80 °C until analysis. The libraries for the V4 region of bacterial 16S rRNA gene using the primer set of 515F (5′-GTGCCAGCMGCCGCGGTAA-3′) and 806R (5′-GGACTACVSGGGTATCTAAT-3′)73 were prepared and sequenced on an Illumina HiSeq2500 platform by Novogene Bioinformatics Technology Co. Ltd (Beijing, China).
Raw sequences were divided into sample libraries using unique barcodes and trimmed to remove the primers and barcodes. Raw sequences were merged using FLASH74 and processed using Qiime75. Chimeric sequences were removed using UCHIME by comparing with the reference Gold database76. OTUs (Operational Taxonomic Units) were clustered at 97% identity and the most abundant sequence in each OTU was selected as a representative sequence using UPARSE software77. For each representative sequence, the bacterial 16S database was classified using the SILVA database78 and RDP classifier79 algorithm to annotate taxonomic information.
Statistical analysis
Oat productivity (grain yield, dry and fresh biomass production), soil properties and bacterial α-diversity (observed richness, Chao1 richness estimator, Shannon diversity index) were evaluated using the general linear models (GLM) procedure and significant differences among means were separated using Fisher's least significant difference (F-LSD) at 5% level by SAS 9.080. Permutational multivariate analysis of variance based on Bray–Curtis dissimilarity matrices using the “adonis” function in R and principal component analysis (PCA) were used to test and visualize cultivar and amendment treatment effects on the rhizosphere bacterial communities using the R packages “vegan”, “pairwise”, “ade4” and “ggplot2”. Soil properties and oat productivity measurements with significant effects (P < 0.05) were kept for redundancy analysis (RDA), excluding collinear variables with a variance inflation factor (VIF > 10) using the “vif.cca” function in R. RDA was used to evaluate the relationships between bacterial communities, oat productivity and soil properties using the “rda” and “ggplot2” function in R81,82. In addition, the relationships among bacterial communities, soil properties and oat productivity were examined by performing Spearman’s correlations, and relationships between soil properties and oat productivity were analyzed by performing Pearson correlation analysis.
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Qadir, M. et al. Productivity enhancement of salt-affected environments through crop diversification. Land Degrad. Dev. 19, 429–453 (2008).
Liu, G. M. et al. Soil enzymes as indicators of saline soil fertility under various soil amendments. Agric. Ecosyst. Environ. 237, 274–279 (2017).
Shaaban, M., Abid, M. & Abou-Shanab, R. Amelioration of salt affected soils in rice paddy system by application of organic and inorganic amendments. J. Plant Soil Environ. 59, 227–233 (2013).
Tejada, M., Garcia, C., Gonzalez, J. L. & Hernandez, M. T. Use of organic amendment as a strategy for saline soil remediation: influence on the physical, chemical and biological properties of soil. Soil Biol. Biochem. 38, 1413–1421 (2006).
Celestina, C., Hunt, J. R., Sale, P. W. G. & Franks, A. E. Attribution of crop yield responses to application of organic amendments: a critical review. Soil Tillage Res. 186, 135–145 (2019).
Mahdi, S. S. et al. Bio-fertilizers in organic agriculture. J. Phytol. 2, 42–54 (2010).
Pindi, P. K. & Satyanarayana, S. D. V. Liquid microbial consortium-a potential tool for sustainable soil health. J. Biofertil. Biopestic. 3, 124 (2012).
Borkar, S. G. Microbes as Bio-fertilizers and Their Production Technology (Woodhead Publishing India Pvt Ltd, New Delhi, 2015).
Abd-Alla, M. H., El-Enany, A.-W.E., Nafady, N. A., Khalaf, D. M. & Morsy, F. M. Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiol. Res. 169, 49–58 (2014).
Singh, M. et al. Plant growth promoting rhizobacteria: application in biofertilizers and biocontrol of phytopathogens. In PGPR Amelioration in Sustainable Agriculture (eds Singh, A. K., Kumar, A. & Singh, P. K.) 41–66 (Woodhead Publishing, 2019).
Vessey, J. K. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255, 571–586 (2003).
Tan, D. S., Jin, J. J., Huang, S. W., Li, S. T. & He, P. Effect of long-term application of K fertilizer and wheat straw to soil on crop yield and soil K under different planting systems. Agric. Sci. China 6, 200–207 (2007).
Han, Z. Effects of treating different crop straw returning to field with decomposition on the physicol-chemical properties of soil and crop yield. Anhui Agric. Sci. Bull. 19, 80–82 (2013).
Chen, H. L., Liu, G. S., Yang, Y. F., Chang, Y. M. & Zhao, L. L. Effects of rotten wheat straw on organic carbon and microbial biomass carbon of tobacco-planted soil. J. Food Agric. Environ. 11, 1017–1021 (2013).
Turmuktini, T. et al. Restoring the health of paddy soil by using straw compost and biofertilizers to increase fertilizer efficiency and rice production with SOBARI (system of organic based aerobic rice intensification) technology. Asian J. Agric. Rural Dev. 2, 519–526 (2012).
Sun, J., Tian, Y., Gao, L., Peng, X. & Tong, E. Effects of straw biological reactor and microbial agents on physicochemical properties and microbial diversity of tomato soil in solar greenhouse. Trans. Chin. Soc. Agric. Eng. 30, 153–164 (2014).
Shen, Z. et al. Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biol. Fertil. Soils 51, 553–562 (2015).
Shen, Z. et al. Effect of biofertilizer for suppressing Fusarium wilt disease of banana as well as enhancing microbial and chemical properties of soil under greenhouse trial. Appl. Soil Ecol. 93, 111–119 (2015).
Wu, K. et al. Effects of bio-organic fertilizer plus soil amendment on the control of tobacco bacterial wilt and composition of soil bacterial communities. Biol. Fertil. Soils 50, 961–971 (2014).
Fu, L. et al. Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biol. Biochem. 104, 39–48 (2017).
Shen, Z. et al. Induced soil microbial suppression of banana fusarium wilt disease using compost and biofertilizers to improve yield and quality. Eur. J. Soil Biol. 57, 1–8 (2013).
Ling, N. et al. Variation of rhizosphere bacterial community in watermelon continuous mono-cropping soil by long-term application of a novel bioorganic fertilizer. Microbiol. Res. 169, 570–578 (2014).
Zhao, S. et al. Change in straw decomposition rate and soil microbial community composition after straw addition in different long-term fertilization soils. Appl. Soil Ecol. 138, 123–133 (2019).
Zhao, S. et al. Changes in soil microbial community, enzyme activities and organic matter fractions under long-term straw return in north-central China. Agric. Ecosyst. Environ. 216, 82–88 (2016).
Prosser, J. I. et al. The role of ecological theory in microbial ecology. Nat. Rev. Microbiol. 5, 384–392 (2007).
Lauber, C. L., Hamady, M., Knight, R. & Fierer, N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75, 5111–5120 (2009).
Shi, S. et al. Response of microbial communities and enzyme activities to amendments in saline–alkaline soils. Appl. Soil Ecol. 135, 16–24 (2019).
Peng, M., Jia, H. & Wang, Q. The effect of land use on abcterial communities in saline–alkali soil. Curr. Microbiol. 74, 325–333 (2017).
Zhao, S. et al. Soil pH is equally important as salinity in shaping bacterial communities in saline soils under halophytic vegetation. Sci. Rep. 8, 4550 (2018).
Soto, M. et al. Pathogenic and mutualistic plant-bacteria interactions: ever increasing similarities. Open Life Sci. 6, 911–917 (2011).
Singh, V. K., Singh, A. K. & Kumar, A. Disease management of tomato through PGPB: current trends and future perspective. 3 Biotech 7, 255 (2017).
Zhang, R., Vivanco, J. M. & Shen, Q. The unseen rhizosphere root-soil-microbe interactions for crop production. Curr. Opin. Microbiol. 37, 8–14 (2017).
Di Giovanni, G., Watrud, L., Seidler, R. & Widmer, F. Comparison of parental and transgenic alfalfa rhizosphere bacterial communities using Biolog GN metabolic fingerprinting and enterobacterial repetitive intergenic consensus sequence-PCR (ERIC-PCR). Microbial. Ecol. 37, 129–139 (1999).
Carelli, M. et al. Genetic diversity and dynamics of Sinorhizobium meliloti populations nodulating different alfalfa cultivars in Italian soils. Appl. Environ. Microbiol. 66, 4785–4789 (2000).
Cattelan, A., Hartel, P. & Fuhrmann, J. Bacterial composition in the rhizosphere of nodulating and non-nodulating soybean. Soil Sci. Soc. Am. J. 62, 1549–1555 (1998).
Marschner, P., Fu, Q. & Rengel, Z. Manganese availability and microbial populations in the rhizosphere of wheat genotypes differing in tolerance to Mn deficiency. J. Plant Nutr. Soil Sci. 166, 712–718 (2003).
Lu, T. et al. Investigation of rhizospheric microbial communities in wheat, barley, and two rice varieties at the seedling stage. J. Agric. Food Chem. 66, 2645–2653 (2018).
Peiffer, J. A. et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl. Acad. Sci. U.S.A. 110, 6548–6553 (2013).
Bai, J. et al. Proteomic response of oat leaves to long-term salinity stress. Environ. Sci. Pollut. Res. Int. 24, 3387–3399 (2017).
Bai, J. et al. Effect of alkali stress on soluble sugar, antioxidant enzymes and yield of oat. J. Integr. Agric. 12, 1441–1449 (2013).
Lu, P. et al. Comparison of quality and yield of different oat varieties in saline–alkali land. J. Triticeae Crops 36, 1510–1516 (2016) ((In Chinese)).
Bai, J. et al. Screening oat genotypes for tolerance to salinity and alkalinity. Front. Plant Sci. 9, 1302 (2018).
Li, X. et al. Effects of genotype and environment on avenanthramides and antioxidant activity of oats grown in northwestern China. J. Cereal Sci. 73, 130–137 (2017).
Ahmad, W., Shah, Z., Khan, F., Ali, S. & Malik, W. Maize yield and soil properties as influenced by integrated use of organic, inorganic and bio-fertilizers in a low fertility soil. Soil Environ. 32, 121–129 (2013).
Ji, Y., Lin, H., Yang, Z., He, F. & Liu, H. Study on the effects of covering land on salt and moisture contents in saline or alkaline soil in summer. Arid Zone Res. 3, 375–381 (2007).
Marschner, H. Marschner’s Mineral Nutrition of Higher Plants 347–368 (Academic Press, London, 2012).
Sun, R., Zhang, X., Guo, X., Wang, D. & Chu, H. Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biol. Biochem. 88, 9–18 (2015).
Chu, H. et al. Soil microbial biomass, dehydrogenase activity, bacterial community structure in response to long-term fertilizer management. Soil Biol. Biochem. 39, 2971–2976 (2007).
Banik, A. et al. Application of rice (Oryza sativa L.) root endophytic diazotrophic Azotobacter sp. strain Avi2 (MCC 3432) can increase rice yield under green house and field condition. Microbiol. Res. 219, 56–65 (2019).
Hassanein, M., Ahmed, A. G. & Zaki, N. M. Effect of nitrogen fertilizer and bio-fertilizer on yield and yield components of two wheat cultivars under sandy soil. Middle East J. Appl. Sci 8, 37–42 (2018).
Tardy, V. et al. Land use history shifts in situ fungal and bacterial successions following wheat straw input into the soil. PLoS ONE 10, e0130672 (2015).
Shao, T. et al. Industrial crop Jerusalem artichoke restored coastal saline soil quality by reducing salt and increasing diversity of bacterial community. Appl. Soil Ecol. 138, 195–206 (2019).
Zeng, Q., Liu, Y., Zhang, H. & An, S. Fast bacterial succession associated with the decomposition of Quercus wutaishanica litter on the Loess Plateau. Biogeochemistry 144, 119–131 (2019).
Abdulla, H. M. & El-Shatoury, S. A. Actinomycetes in rice straw decomposition. Waste Manag. 27, 850–853 (2007).
Sun, L., Pope, P. B., Eijsink, V. G. & Schnurer, A. Characterization of microbial community structure during continuous anaerobic digestion of straw and cow manure. Microb Biotechnol. 8, 815–827 (2015).
Lu, H. et al. Changes in soil microbial community structure and enzyme activity with amendment of biochar-manure compost and pyroligneous solution in a saline soil from Central China. Eur. J. Soil Biol. 70, 67–76 (2015).
Eisenhauer, N. et al. Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci. Rep. 7, 44641 (2017).
Dennis, P. G., Miller, A. J. & Hirsch, P. R. Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities?. FEMS Microbiol. Ecol. 72, 313–327 (2010).
Zornoza, R. et al. Assessing air-drying and rewetting pre-treatment effect on some soil enzyme activities under Mediterranean conditions. Soil Biol. Biochem. 38, 2125–2134 (2006).
Acosta-Martinez, V., Moore-Kucera, J., Cotton, J., Gardner, T. & Wester, D. Soil enzyme activities during the 2011 Texas record drought/heat wave and implications to biogeochemical cycling and organic matter dynamics. Appl. Soil Ecol. 75, 43–51 (2014).
Dick, R. P. & Burns, R. G. Methods of Soil Enzymology-SSSA Book Series (ed. Dick, R. P.) 1–34 (2011).
Geisseler, D., Horwath, W. R., Joergensen, R. G. & Ludwig, B. Pathways of nitrogen utilization by soil microorganisms—a review. Soil Biol. Biochem. 42, 2058–2067 (2010).
Li, R., Tao, R., Ling, N. & Chu, G. Chemical, organic and bio-fertilizer management practices effect on soil physicochemical property and antagonistic bacteria abundance of a cotton field: implications for soil biological quality. Soil Tillage Res. 167, 30–38 (2017).
Chen, Z. et al. Changes in soil microbial community and organic carbon fractions under short-term straw return in a rice–wheat cropping system. Soil Tillage Res. 165, 121–127 (2017).
Olsen. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate (United States Department of Agriculture, Washington, 1954).
Khan, S., Mulvaney, R. & Mulvaney, C. Accelerated diffusion methods for inorganic-nitrogen analysis of soil extracts and water. Soil Sci. Soc. Am. J. 61, 936–942 (1997).
Mi, J., Gregorich, E. G., Xu, S., McLaughlin, N. B. & Liu, J. Effects of a one-time application of bentonite on soil enzymes in a semi-arid region. Can. J. Soil Sci. 98, 542–555 (2018).
Guan, S., Zhang, D. & Zhang, Z. Soil Enzyme and Its Research Methods, vol 1986 (China Agriculture Press, Beijing, 1986).
Johnson, J. L. & Temple, K. L. Some variables affecting the measurement of “catalase activity” in soil 1. Soil Sci. Soc. Am. J. 28, 207–209 (1964).
Ahmad, I. et al. Effect of pepper–garlic intercropping system on soil microbial and bio-chemical properties. Pak. J. Bot. 45, 695–702 (2013).
Hoffmann, G. & Teicher, K. Ein kolorimetrisches verfahren zur bestimmung der ureaseaktivität in Böden. Z. Pflanzenernähr. Düng. Bodenkunde 95, 55–63 (1961).
Frankeberger, W. & Johanson, J. Method of measuring invertase activity in soils. Plant Soil 74, 301–311 (1983).
Bergmann, G. T. et al. The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol. Biochem. 43, 1450–1455 (2011).
Magoč, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335 (2010).
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996 (2013).
Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).
Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).
Inc., S. I. SAS/STAT® 15.1 User’s Guide-The GLM Procedure. https://support.sas.com/documentation/onlinedoc/stat/151/glm.pdf (2018).
McMurdie, P., Holmes, S., Kindt, R., Legendre, P. & O’Hara, R. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).
Sheik, C. S. et al. Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. PLoS ONE 7, e40059 (2012).
Acknowledgements
We are very grateful to Novogene Co., Ltd. for deep 16S rRNA gene sequence barcode sequencing. We thank all the supporter by The Scientific and Technological Innovation Team of Inner Mongolia, The Multi-grain Engineering and Technology Center of Inner Mongolia, The Talent Introduction Project of Inner Mongolia Agricultural University (NDYB2018-29) and The MOE-AAFC PhD Research program (201808150135). We really thank Bianca Evans for her assistance in English language correction.
Author information
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Lu, P., Bainard, L.D., Ma, B. et al. Bio-fertilizer and rotten straw amendments alter the rhizosphere bacterial community and increase oat productivity in a saline–alkaline environment. Sci Rep 10, 19896 (2020). https://doi.org/10.1038/s41598-020-76978-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s41598-020-76978-3
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.
