Effect of biochar applied with plant growth-promoting rhizobacteria (PGPR) on soil microbial community composition and nitrogen utilization in tomato

doi:10.1016/S1002-0160(21)60030-9

Pedosphere

Volume 31, Issue 6, December 2021, Pages 872-881

https://doi.org/10.1016/S1002-0160(21)60030-9 Get rights and content

Abstract

Plant growth-promoting rhizobacteria (PGPR) represent an important microbial community group and have beneficial effects on plant growth and development. A pot experiment was conducted to study the effect of biochar applied with PGPR on the soil microbial community composition and nitrogen use efficiency (NUE) of tomato, which could provide a theoretical basis for rational fertilization. Six treatments were designed: no nitrogen (N), PGPR, or biochar control (CK); biochar without N or PGPR (BCK); N without PGPR or biochar (U); N and PGPR without biochar (UP); N and biochar without PGPR (UB); and N, PGPR, and biochar (UBP). The tomato yield in the UP treatment was 9.09% lower than that in the U treatment, whereas that in the UB treatment was 19.93% higher than that in the U treatment. The tomato yield in the UBP treatment was 32.45%, 45.69%, and 10.44% higher than those in the U, UP, and UB treatments, respectively. Biochar combined with PGPR increased the relative abundance of Nitrospira and Bradyrhizobium in the soil. At the tomato maturity stage, the soil NO₃^–-N content in the UBP treatment was 87.12%, 88.12%, and 31.04% higher than those in the U, UP, and UB treatments, respectively. The NUE in the UP treatment was 4.03% lower than that in the U treatment, and that in the UBP treatment was 13.63%, 17.66%, and 10.77% higher than those in the U, UP, and UB treatments, respectively. This study showed that biochar combined with PGPR can improve soil microbial community structure and increase the NUE of tomato.

References (48)

H Aebi
Catalase in vitro
Methods Enzymol
(1984)
M Albareda et al.
Alternatives to peat as a carrier for rhizobia inoculants: Solid and liquid formulations
Soil Biol Biochem
(2008)
S H Chien et al.
Recent developments of fertilizer production and use to improve nutrient efficiency and minimize environmental impacts
Adv Agron
(2009)
J R de Freitas et al.
Growth promotion of winter wheat by fluorescent pseudomonads under field conditions
Soil Biol Biochem
(1992)
M Devkota et al.
Combining permanent beds and residue retention with nitrogen fertilization improves crop yields and water productivity in irrigated arid lands under cotton, wheat and maize
Field Crops Res
(2013)
L P Di Salvo et al.
Plant growth-promoting rhizobacteria inoculation and nitrogen fertilization increase maize (Zea mays L.) grain yield and modified rhizosphere microbial communities
Appl Soil Ecol
(2018)
M Farrell et al.
Microbial utilisation of biochar-derived carbon
Sci Total Environ
(2013)
S Gagné et al.
Increase of greenhouse tomato fruit yields by plant growth-promoting rhizobacteria (PGPR) inoculated into the peat-based growing media
Soil Biol Biochem
(1993)
L Hale et al.
Biochar characteristics relate to its utility as an alternative soil inoculum carrier to peat and vermiculite
Soil Biol Biochem
(2015)
S Han et al.
Shifts in Nitrobacter- and Nitrospira-like nitrite-oxidizing bacterial communities under long-term fertilization practices
Soil Biol Biochem
(2018)

D L Jones et al.

Biochar-mediated changes in soil quality and plant growth in a three year field trial

Soil Biol Biochem

(2012)

D Laird et al.

Biochar impact on nutrient leaching from a midwestern agricultural soil

Geoderma

(2010)

K A Mackie et al.

The effects of biochar and compost amendments on copper immobilization and soil microorganisms in a temperate vineyard

Agric Ecosyst Environ

(2015)

R Posmanik et al.

Effect of high ammonia loads emitted from poultry-manure digestion on nitrification activity and nitrifier-community structure in a compost biofilter

Ecol Eng

(2014)

R B A Rafael et al.

Benefits of biochars and NPK fertilizers for soil quality and growth of cowpea (Vigna unguiculata L. Walp.) in an acid Arenosol

Pedosphere

(2019)

H M Sosik et al.

Light absorption by phytoplankton, photosynthetic pigments and detritus in the California Current System

Deep Sea Res Part I

(1995)

X P Tian et al.

Responses of soil microbial community structure and activity to incorporation of straws and straw biochars and their effects on soil respiration and soil organic carbon turnover

Pedosphere

(2019)

C Trasar-Cepeda et al.

An improved method to measure catalase activity in soils

Soil Biol Biochem

(1999)

B B Ward et al.

The utility of functional gene arrays for assessing community composition, relative abundance, and distribution of ammonia-oxidizing bacteria and archaea

Methods Enzymol

(2011)

D Wu et al.

Biochar combined with vermicompost increases crop production while reducing ammonia and nitrous oxide emissions from a paddy soil

Pedosphere

(2019)

H Daims et al.

Complete nitrification by Nitrospira bacteria

Nature

(2015)

P Das et al.

Oxidative environment and redox homeostasis in plants: Dissecting out significant contribution of major cellular organelles

Front Environ Sci

(2015)

Ş Dere

Spectrophotometric determination of chlorophyll-A, B and total carotenoid contents of some algae species using different solvents

Turk J Bot

(1998)

T Z DeSantis et al.

Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB

Appl Environ Microbiol

(2006)

Cited by (21)

Nitrogen (N) “supplementation, slow release, and retention” strategy improves N use efficiency via the synergistic effect of biochar, nitrogen-fixing bacteria, and dicyandiamide
2024, Science of the Total Environment
Irrational nitrogen (N) fertilizer management and application practices have led to a range of ecological and environmental problems that seriously threaten food security. In this study, an effective N fertilizer management strategy was established for improving N fertilizer utilization efficiency (NUE). Biochar, N₂-fixing bacteria (Enterobacter cloacae), and a nitrification inhibitor (dicyandiamide, DCD) were simultaneously added to the soil during maize cultivation. The goal was to increase soil ammonium nitrogen content and NUE by regulating the relative abundance, enzyme activity, and functional gene expression of N conversion-related soil microbes. Biochar combined with E. cloacae and DCD significantly increased soil N content, and the NUE reached 46.69 %. The relative abundance of Burkholderia and Bradyrhizobium and the activity of nitrogenase increased significantly during biological N₂ fixation. Further, the abundance of the nifH gene was significantly up-regulated. The relative abundance of Sphingomonas, Pseudomonas, Nitrospira, and Castellaniella and the activities of ammonia monooxygenase and nitrate reductase decreased significantly during nitrification and denitrification. Moreover, the abundance of the genes amoA and narG was significantly down-regulated. Correlation analyses showed that the increase in soil N₂ fixation and the suppression of nitrification and denitrification reactions were the key contributors to the increase in soil N content and NUE. Biochar combined with E. cloacae and DCD synergistically enabled the supplementation, slow release, and retention of N, thus providing adequate N for maize growth. Thus, the combination of biochar, E. cloacae, and DCD is effective for mitigating the irrational application of N fertilizers and reducing N pollution.
Ridge–furrow planting with film mulching and biochar addition can enhance the spring maize yield and water and nitrogen use efficiency by promoting root growth
2023, Field Crops Research
Promoting root growth is essential for improving crop yields and the efficient use of soil nutrients, especially in dryland areas of the Loess Plateau in China where water resources are scarce and nitrogen utilization is low. Adding biochar is a potential strategy to enhance root growth and consequently increase crop productivity. In this study, we investigated the effects of adding biochar at 0.0 t ha^–1, 4.5 t ha^–1, and 9.0 t ha^–1 on the growth and activity of roots, yield, and water and nitrogen use efficiency in spring maize under flat planting without film and ridge–furrow planting with film mulching. Adding biochar increased the root length density in spring maize by 7.1–13.8 %, root dry weight density by 4.8–9.2 %, root surface area density by 6.7–13.8 %, and root sap bleeding rate by 7.1–18.9 %, where the effects increased as the biochar application rate increased. Compared with flat planting without film mulching, the effect of adding biochar on the growth and activity of roots was more significant under ridge–furrow film mulching (P < 0.05), especially with biochar applied at 9.0 t ha^–1. Ridge–furrow planting with film mulching and adding biochar at 9.0 t ha^–1 increased the spring maize yield by 28.3 % and water use efficiency by 40.0 %. This method also increased the total nitrogen content of plants by 25.8 %, reduced the mineral nitrogen residue level in the 0–200 cm soil layer during the harvest period by 35.0 %, and increased the nitrogen use efficiency by 34.9 %. Therefore, the combination of ridge–furrow film mulching and adding biochar at 9.0 t ha^–1 can be used as an efficient soil management practice for improving the utilization of water and nitrogen to possibly improve yields and facilitate the efficient utilization of resources in dry farmland areas of the Loess Plateau.
Exogenous application of Bradyrhizobium japonicum AC20 enhances soybean tolerance to atrazine via regulating rhizosphere soil microbial community and amino acid, carbohydrate metabolism related genes expression
2023, Plant Physiology and Biochemistry
Atrazine is used to control broad-leaved weeds in farmland and has negative impacts on soybean growth. Legume-rhizobium symbiosis plays an important role in regulating abiotic stress tolerance of plants, however, the mechanisms of rhizobia regulate the tolerance of soybean to atrazine based on the biochemical responses of the plant-soil system are limited. In this experiment, Glycine max (L.) Merr. Dongnong 252, planted in 20 mg kg⁻¹ of atrazine-contaminated soil, was inoculated with Bradyrhizobium japonicum AC20, and the plant growth, rhizosphere soil microbial diversity and the expression of the genes related to soybean carbon and nitrogen metabolism were assessed. The results indicated that strain AC20 inoculation alleviated atrazine-induced growth inhibition via increasing the contents of leghemoglobin and total nitrogen in soybean seedlings. The psbA gene expression level of the soybean seedlings that inoculated strain AC20 was 1.4 times than that of no rhizobium inoculating treatments. Moreover, the inoculated AC20 increased the abundance of Acidobacteria and Actinobacteria in soybean rhizosphere. Transcriptome analysis demonstrated that strain AC20 regulated the genes expression of amino acid metabolism and carbohydrate metabolism of soybean seedlings. Correlation analysis between 16S rRNA and transcriptome showed that strain AC20 reduced Planctomycetes abundance so as to down-regulated the expression of genes Glyma. 13G087800, Glyma. 12G005100 and Glyma.12G098900 involved in starch synthesis pathway of soybean leaves. These results provide available information for the rhizobia application to enhance the atrazine tolerate in soybean seedlings.
Synergistic use of biochar and the plant growth-promoting rhizobacteria in mitigating drought stress on oak (Quercus brantii Lindl.) seedlings
2023, Forest Ecology and Management
The successful early establishment of seedlings is a challenging step for the management of forests in semi-arid regions, such as in the oak (Q. brantii) forests in western Iran. To address this challenge, we tested the separate and combined effects of different biofertilizers: we evaluated the influence of the application of biochar and plant growth-promoting rhizobacteria (PGPR) on the growth of oak seedlings subjected to water stress in controlled conditions. Two acorns were sown in a total of 216 pots distributed according to the following treatments: 3 water treatments (100, 75 and 50 % of field capacity), 4 biochar treatments (0, 1, 2 and 3 % of soil weight), 2 PGPR treatments (absence or presence) in 9 replicates. Biochar was derived from mistletoe (Loranthus europaeus), a widespread hemi-parasite plant in the studied oak forests. After emergence, a total of 20 ecophysiological, morphological and growth traits were measured on oak seedlings. We found that the interaction between irrigation, biochar and PGPR significantly influenced the ecophysiological attributes of the seedlings. Comparing application to non-application of PGPR, we found that chlorophyll content, photosynthesis rate and biomass of shoots were respectively increased by 21, 50 and 19 % in the absence of water stress and by 54, 14 and 18 % under severe water stress conditions. Moderate biochar concentrations improved seedling growth and ecophysiological responses whereas the highest concentration of biochar had a detrimental effect. A PLS path model revealed the direct and indirect relationships between the treatments, the seedling morpho-physiological traits and the final variable of interest (total dry biomass). The model explained 78 % of the total variance and showed that the root growth indices (path coefficient = 0.665) had a significant direct effect on oak dry matter whereas this effect was reduced with shoot growth indices. We found that the use of moderate levels of biochar alone or in combination with PGPR can benefit oak seedling development in water-limited conditions but further studies are still needed to test the effectiveness and applicability of these treatments in field conditions.
Greenhouse gas emission responses to different soil amendments on the Loess Plateau, China
2023, Agriculture, Ecosystems and Environment
Citation Excerpt :
In recent years, PGPR – as exogenous bacteria – have been inoculated into soil, resulting in increases, decreases, or no impact on native microbial activity (Li et al., 2018a). In this study, The impact on soil microbes was not obvious after PGPR application (Fig. 5), possibly due to some strains not playing an effective role in terms of survival and competition under low soil moisture conditions (Wang et al., 2021). Moreover, PGPR may release/fix/solubilize certain chemicals that hinder microbial growth (Gupta et al., 2014), which is why PGPR addition had little influence on soil microbes.
Soil amendments are commonly used to reduce greenhouse gas (GHG) emissions by altering the physical, biological, and chemical qualities of soil, but the mechanism by which this is achieved still vague. This two-year study surveyed the influences of biochar (BC), Bacillus mucilaginosus (BM), and Bacillus subtilis (BS) on the physical, enzyme activities, soil microbial and GHG emissions. Results indicated that soil amendment addition decreased the activities of β-glucosidase (BG), cellobiohydrolase (CBH), β-xylosidase (BX), sucrase, cellulase by 8.81%, 8.99%, 22.08%, 59.46%, 74.61%, respectively, and increased N-acetylglucosaminidase (NAG) activity by 155.00%. Soil amendments had little effect on soil microbes, apart from those related to the C and N cycles, such as Proteobacteria, Mortierellomycota and Acidobacteriota. In addition, BC, BM, and BS amendments decreased mean cumulative CO₂ emissions by 38.43%, 11.83%, and 38.54%, respectively. Cumulative N₂O emissions from the BC treatment increased by 28.17% in 2019 and decreased by 37.22% in 2020. For the BM and BS treatments, cumulative N₂O emissions did not significantly change in 2019 but decreased by 4.93% and 57.85% in 2020, respectively. Generally, soil amendments decreased the greenhouse emission intensity (GHGI) and global warming potential (GWP). Moreover, a structural equation model (SEM) revealed factors that directly or indirectly controlled GHG emissions, including NAG, BX, CBH, Proteobacteria, Mortierellomycota and Acidobacteriota. These factors were limited mainly by soil C and N substrates, such as ammonium-nitrogen (NH₄⁺-N), available phosphorus (AP), and soil organic matter (SOM). Overall, soil amendments can reduce GHG emissions in the long term, but they are affected by many factors.However, soil amendments alone have limited effects on reducing GHG emissions on the Loess Plateau. Suggesting combining and applying biochar and plant growth-promoting rhizobacteria (PGPR) may enhance soil quality and alleviate GHG emissions.
The combined action of biochar and nitrogen-fixing bacteria on microbial and enzymatic activities of soil N cycling
2023, Environmental Pollution
Citation Excerpt :
Thus, improving the efficiency of N fertilizer and capacity of soil N retention are the key measures to achieve a sustainable agriculture and environmental protection (Battye et al., 2017). The addition of exogenous nitrogen-fixing bacteria during agricultural production is both green and effective for N retention in soil (Wang et al., 2021). Nitrogen-fixing bacteria are capable of transforming N2 from the atmosphere into ammonia (NH4+) (Rosenblueth et al., 2018) and nitrogenases (NIT) are enzymes used by bacteria to complete the process.
This study aims to investigate the positive effects of the combined use of Enterobacter cloacae and biochar on improving nitrogen (N) utilization. The greenhouse pots experimental results showed the synergy of biochar and E. cloacae increased soil total N content and plant N uptake by 33.54% and 15.1%, respectively. Soil nitrogenase (NIT) activity increased by 253.02%. Ammonia monooxygenase (AMO) and nitrate reductase (NR) activity associated with nitrification and denitrification decreased by 10.94% and 29.09%, respectively. The relative abundance of N fixing microorganisms like Burkholderia and Bradyrhizobium significantly increased. Sphingomonas and Ottowia, two bacteria involved in the nitrification and denitrification processes, were found to be in lower numbers. The E. cloacae's ability to fix N₂ and promote the growth of plants allow the retention of N in soil and make more N available for plant development. Biochar served as a reservoir of N for plants by adsorbing N from the soil and providing a shelter for E. cloacae. Thus, biochar and E. cloacae form a synergy for the management of agricultural N and the mitigation of negative impacts of pollution caused by excessive use of N fertilizer.

View all citing articles on Scopus

View full text

Effect of biochar applied with plant growth-promoting rhizobacteria (PGPR) on soil microbial community composition and nitrogen utilization in tomato

Abstract

Methods Enzymol

Soil Biol Biochem

Adv Agron

Soil Biol Biochem

Field Crops Res

Appl Soil Ecol

Sci Total Environ

Soil Biol Biochem

Soil Biol Biochem

Soil Biol Biochem

Soil Biol Biochem

Geoderma

Agric Ecosyst Environ

Ecol Eng

Pedosphere

Deep Sea Res Part I

Pedosphere

Soil Biol Biochem

Methods Enzymol

Pedosphere

Complete nitrification by Nitrospira bacteria

Nature

Oxidative environment and redox homeostasis in plants: Dissecting out significant contribution of major cellular organelles

Front Environ Sci

Spectrophotometric determination of chlorophyll-A, B and total carotenoid contents of some algae species using different solvents

Turk J Bot

Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB

Appl Environ Microbiol