Elsevier

European Journal of Soil Biology

Volume 106, September–October 2021, 103350
European Journal of Soil Biology

Biochar interaction with chemical fertilizer regulates soil organic carbon mineralization and the abundance of key C-cycling-related bacteria in rhizosphere soil

https://doi.org/10.1016/j.ejsobi.2021.103350Get rights and content

Highlights

  • Functional groups on biochar and not C content regulate the mineralization of SOC.

  • Biochar + Fertilizer (BF) decreased the abundance of C-cycling bacteria to regulate C-cycling.

  • C-cycling was regulated by competition for C sources with N-cycling bacteria under BF.

  • BF did not reduce the activities of some hydrocarbon-degrading bacteria.

Abstract

Biochar amendment in soils has been proposed as an important strategy to improve soil C retention. However, while the exact roles of different biochar types on soil organic carbon (SOC) dynamics are not clear, the effect of their interactions with chemical fertilization on SOC, the dynamics of C-cycling enzyme activities and key C-cycling-related bacteria in rhizosphere soil remain unexplored. Therefore, biochars derived from rice straw, bamboo, cow, and pig manure were applied with/without chemical fertilizer to study soil C dynamics, the activities, diversity, and abundance of different C-cycling-related bacteria in the plant-soil system. Biochar + fertilizer (BF), irrespective of biochar source, induced an initial increase in dissolved organic and inorganic C (DOC and DIC) that were subsequently reduced compared to biochar over 15-weeks. Higher intensities of C-containing functional groups rather than the total C content of biochar induced the mineralization of SOC. Also, higher nutrient uptake, biomass, and CO2 concentration in plants under BF had an insignificant influence on SOC. Similarly, the reduction in mineral-associated organic C, DOC, DIC, and invertase activity in BF soils was associated with a decrease in the relative abundance of some key C-cycling related bacterial orders: Gemmmatimonadales, Myxococcales, Nitrosomonadales, and Acidimicrobiales, while the hydrocarbon-degrading taxa (Sphingmonadales and Xanthomonadales), and N-cycling bacteria were stimulated. Hence, BF amendment could exert varied influences on C-cycling-related bacteria and on global C-cycling. The use of BF limited C-cycling and its loss by providing more N-substrates for N-cycling organisms, which also competed with most C-cycling-related bacteria for organic C to regulate C mineralization and its associated loss.

Introduction

The soil carbon (C), made up of organic and inorganic fractions, is the largest C pool in the terrestrial ecosystem [1]. It is approximately 3.3 times that of the atmospheric C pool [2]. It makes up approximately two-thirds of all C in the terrestrial ecosystems and is actively exchanged with the atmosphere [3]. As a key factor used to assess soil quality and plant productivity, soil organic C (SOC) plays a crucial role in improving soil physicochemical properties, soil nutrient cycling, photosynthesis in plant leaves, and soil biological properties [4]. However, various human activities, such as intense land use and excessive long-term use of N-based chemical fertilizers, could increase soil carbon loss and increase its release as carbon dioxide (CO2) into the atmosphere. CO2, along with nitrous oxide (N2O) and methane (CH4), contributes to over 90% of global climate warming from anthropogenic activities [5]. Due to the inevitability of increasing plant yields to meet food demand, the use of N fertilizers has increased drastically, accounting for 72% of soil N input in China [6] and 77.8% in the US in 2018 [7]. Given the tight connections between C and N cycles in the terrestrial ecosystem, the increasing use of chemical N fertilizers could alter the ecosystem's C cycles [8]. Therefore, exploring management practices that could reduce the mineralization and loss of labile C fractions remains a major concern in soil management and global environmental health.

Biochar is an aromatic C-rich solid byproduct obtained when biomass is pyrolyzed in an oxygen-limited environment [9]. It has gained attention in agriculture for its role in improving soil physical, chemical, and biological properties [10]. As a C-rich material, the application of biochar can increase the availability of recalcitrant and labile C compounds that can undergo degradation after their incorporation into the soil [11]. Published reports have shown that biochar could exert either positive, negative, or no effects on soil fertility and C storage potential [[12], [13], [14]]. Labile organic C inputs contained in straw and litter, for example, can increase not only SOC concentration and nutrient availability but could also stimulate microbial activity [15,16]. However, most practical soil applications of biochar are made along with inorganic fertilizers to improve N retention and optimize crop production [9]. While biochar could increase SOC stocks, its interaction with chemical fertilizers could alter soil C dynamics by modifying C cycling enzyme activity and soil microbial communities involved in SOC degradation. Similarly, inorganic N addition to soils could affect soil physicochemical properties [17,18], soil microbial community composition and function [19,20], and soil organic matter stability [21]. Notably, soil C degrading organisms are the biotic controlling factors for SOC turnover, thereby significantly regulating soil C-cycling and CO2 emission [22]. Some taxa possess higher C-cycling abilities among the soil bacteria via increased decomposition of organic C sources in the soil, which they incorporate into their biomass and respire as CO2 [23]. They possess the RuBisCO form II enzyme gene (cbbM), which enables them to utilize C more efficiently [24]. Since these bacteria have great control over soil C cycling and act as the primary regulators of C exchange in the soil-atmosphere system [25,26], their regulatory activities can shift under altered environmental conditions and soil management practices [27].

With the varying effect of sole biochar and inorganic fertilizer on soil properties and bacterial distribution, predicting the identities of C-cycling-related 16S rRNA genes when biochar is co-applied with chemical fertilizers in the soil systems is of utmost importance. The co-application of biochar and fertilizers has become a common practice, but their effect on C-cycling and the abundance of major C-cycling-related 16S rRNA genes has not been adequately documented in soil-plant systems. Therefore, the changes in soil C fractions over time and how they regulate the distribution of different key C-cycling-related bacterial communities in rhizosphere soil under biochar + fertilizer interactions require adequate understanding. The use of rhizosphere soil in our study is important because it differs from the bulk soil due to changes in its biogeochemistry, which are influenced by root exudates containing labile C that supports microbial activity [28,29]. Therefore, this study will provide the needed insight into C-cycling in practical agricultural soils, unlike the numerous available reports without the effect of plant rhizosphere. Hence, this study could contribute to ecosystem models for predicting the C budget of terrestrial ecosystems in soil-plant systems.

We hypothesize that: Compared to sole biochar, combined biochar and fertilizer would reduce the mineralization of SOC, with variation among biochar types. Also, N fertilization in BF would provide substrates for N-cycling-related bacteria, which may compete for dominance and C sources with the C-cycling-related bacteria to regulate C-cycling. Similarly, the expected increase in root exudates associated with increased plant nutrition, biomass, and photosynthesis under BF could influence the abundance of rhizosphere C-cycling related bacterial groups.

Therefore, this study's objectives were to understand the effects of different biochar + fertilizer interactions on the mechanisms regulating the dynamic relationship between soil C fractions, C-cycling enzyme activity, the diversity, and functional abundance of key bacterial communities regulating C cycling in the plant-soil system. These interactions on plant photosynthetic CO2, nutrient concentration and biomass of maize would also be observed.

Section snippets

Production and characterization of biochar

The biochars used for this study were produced from bamboo, rice straw, cow manure, and pig manure. The raw feedstocks were air-dried, crushed, and pyrolyzed at 500 °C ± 10 °C (at a holding time of 2 h). Slow pyrolysis of the biomasses was carried out using a bench-scale pyrolysis unit (SSBP-50004, Jiangsu, China.) under oxygen-limited conditions. The internal oxygen was purged out from the reactor by introducing a stream of nitrogen gas at 0.5 L min−1 for 2 min prior to pyrolysis. After

Properties of biochar and the effects of biochar/biochar and fertilizer interactions on soil chemical properties

Higher contents of total N and P were observed in the pig manure biochar (PMB) compared to cow manure biochar (CMB), rice straw biochar (RSB), and bamboo biochar (BB) (Table S1). The CMB had the highest pH content, while the BB had the highest total C content and specific surface area. In addition to the high ash content in RSB, this biochar also had higher peaks of C and O-containing functional groups (Fig. 1). Despite its high C content, the bamboo biochar had the weakest peaks/intensities of

Influence of biochar + fertilizer interactions on soil C fractions and C-cycling enzyme activity

The DOC pool is regarded as the primary form of labile C and a significant indicator of the lability of SOC [37]. The initial increase in DOC and DIC in BF relative to biochar could be attributed to an increase in soil nutrients provided by the added fertilizers, which stimulated microbial activities' for the degradation of the introduced labile C in biochar. Increases in soil nutrients after fertilization and the provision of suitable habitats for microbial growth and protection from predators

Conclusion

The use of biochar sources containing higher intensities of C-containing functional groups (as in CMB, PMB, and RSB) rather than their total C (as in BB) content regulated their influence on the mineralization of SOC. Combined biochar and fertilizer (BF) increased plant nutrient uptake, biomass, and photosynthesis. However, the assumed deposition of the plant photosynthetic CO2 as roots exudates were insignificant in altering the abundance of rhizosphere C-cycling-related bacterial community.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgment

This work was funded by the Fujian Forestry Science and Technology Promotion Project (2020TG17) and the University-Industry Cooperation Project of Fujian Provincial Department of Science and Technology (2016N5005).

References (77)

  • M.M. Ibrahim et al.

    De-ashed biochar enhances nitrogen retention in manured soil and changes soil microbial dynamics

    Geoderma

    (2020)
  • F. Eivazi et al.

    Glucosidases and galactosidases in soils

    Soil Biol. Biochem.

    (1988)
  • L. Han et al.

    Biochar's stability and effect on the content, composition and turnover of soil organic carbon

    Geoderma

    (2020)
  • D.D. Warnock et al.

    Influences of non-herbaceous biochar on arbuscular mycorrhizal fungal abundances in roots and soils: results from growth-chamber and field experiments

    Appl. Soil Ecol.

    (2010)
  • J. Lehmann et al.

    Biochar effects on soil biota – a review

    Soil Biol. Biochem.

    (2011)
  • D. Wu et al.

    Effect of biochar origin and soil pH on greenhouse gas emissions from sandy and clay soils

    Appl. Soil Ecol.

    (2018)
  • Z. Yan et al.

    Co-occurrence patterns of the microbial community in polycyclic aromatic hydrocarbon-contaminated riverine sediments

    J. Hazard Mater.

    (2019)
  • E.J. Foster et al.

    Biochar and manure amendments impact soil nutrients and microbial enzymatic activities in a semi-arid irrigated maize cropping system

    Agric. Ecosyst. Environ.

    (2016)
  • J. Tian et al.

    Biochar affects soil organic matter cycling and microbial functions but does not alter microbial community structure in a paddy soil

    Sci. Total Environ.

    (2016)
  • D. Ameur et al.

    Activated biochar alters activities of carbon and nitrogen acquiring soil enzymes

    Pedobiologia

    (2018)
  • H.M. El Sharkawi et al.

    Biochar-ammonium phosphate as an uncoated-slow release fertilizer in sandy soil

    Biomass Bioenergy

    (2018)
  • W. Wang et al.

    Predatory Myxococcales are widely distributed in and closely correlated with the bacterial community structure of agricultural land

    Appl. Soil Ecol.

    (2020)
  • C. Kramer et al.

    Soil organic matter in soil depth profiles: distinct carbon preferences of microbial groups during carbon transformation

    Soil Biol. Biochem.

    (2008)
  • C. Ai et al.

    Reduced dependence of rhizosphere microbiome on plant-derived carbon in 32-year long-term inorganic and organic fertilized soils

    Soil Biol. Biochem.

    (2015)
  • S. Wang et al.

    Soil aggregate-associated bacterial metabolic activity and community structure in different aged tea plantations

    Sci. Total Environ.

    (2019)
  • R. Sun et al.

    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.

    (2015)
  • J. Mao et al.

    Bioremediation of polycyclic aromatic hydrocarbon-contaminated soil by a bacterial consortium and associated microbial community changes

    Int. Biodeterior. Biodegrad.

    (2012)
  • J. Zeng et al.

    Effects of carbon sources on the removal of ammonium, nitrite and nitrate nitrogen by the red yeast Sporidiobolus pararoseus Y1

    Bioresour. Technol.

    (2020)
  • J. Zeng et al.

    Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition

    Soil Biol. Biochem.

    (2016)
  • A.K.A. Suleiman et al.

    Organic amendment strengthens interkingdom associations in the soil and rhizosphhere of barley (Hordeum vulgare)

    Sci. Total Environ.

    (2019)
  • R. Chen et al.

    Fertilization decreases compositional variation of paddy bacterial community across geographical gradient

    Soil Biol. Biochem.

    (2017)
  • S. Yan et al.

    Influence of soil organic carbon on the aroma of tobacco leaves and the structure of microbial communities

    Curr. Microbiol.

    (2020)
  • Z. Sun et al.

    Priming of soil organic carbon decomposition induced by exogenous organic carbon input: a meta-analysis

    Plant Soil

    (2019)
  • S. Yan et al.

    Biochar application on paddy and purple soils in southern China: soil carbon and biotic activity

    Roy. Soc. Open Sci.

    (2019)
  • J. Hansen et al.

    Global warming in the twenty-first century: an alternative scenario

    Proc. Natl. Acad. Sci. U.S.A.

    (2000)
  • W.F. Zhang et al.

    The development and contribution of nitrogenous fertilizer in China and challenges faced by the country

    Sci. Agric. Sin.

    (2013)
  • EPA

    Greenhouse Gas Emissions: Overview of Greenhouse Gases

    (2020)
  • Е. Blagodatskaya et al.

    Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review

    Biol. Fertil. Soils

    (2008)
  • Cited by (28)

    View all citing articles on Scopus
    View full text