Elsevier

Applied Soil Ecology

Volume 158, February 2021, 103783
Applied Soil Ecology

Plants and microbes' responses to the net nitrification rates of chemical fertilizers in vegetable soils

https://doi.org/10.1016/j.apsoil.2020.103783Get rights and content

Highlights

  • Net nitrification rates (NNRs) were significantly higher in vegetable soils compared with control soils

  • Temperature and pH in the vegetable soils influenced the NNRs

  • Abundance of comammox amoA Nitrospira inopinata was significantly higher in vegetable soils as compared control soils

  • The comammox amoA N. inopinata gene was correlated significantly with the NNRs

Abstract

Various types of chemical fertilizers are used in agricultural production in Bangladesh. However, plants and microbes' responses to the nitrification activity of chemical fertilizers are unknown. The goal of this study was to determine the responses of plants and nitrifying archaea/bacteria and comammox amoA Nitrospira inopinata bacteria to the net nitrification rates (NNRs) of chemical fertilizers in four vegetable soils. The abundance of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB), nitrite-oxidizing bacteria (NOB), and comammox amoA N. inopinata was determined by q-PCR. The NNRs ranged from 2.96 ± 0.39 to 10 ± 1.19 mg kg−1 h−1 and were significantly higher (p < 0.05) in the vegetable soils than in the control soils (uncultivated soils). Temperature and pH influenced the NNRs. The abundance of comammox amoA N. inopinata ranged from 9.34E+05 to 4.55E+06 per gram dry soil in the vegetable soils and represented 28 to 72% of the nitrifying amoA genes. Among the vegetable soils, the highest NNRs and abundance of comammox amoA N. inopinata were found in Phaseolus vulgaris soils. The abundance of AOA, AOB, NOB, and comammox amoA N. inopinata was significantly (p < 0.05) higher in the vegetable soils compared to control soils and was correlated positively and significantly with the NNRs. Principal component analysis (PCA) results confirmed the distinct variation present among the vegetable soils according to their components. Finally, it may be concluded that the plants and nitrifying archaea/bacteria, as well as comammox amoA N. inopinata, can also have indirect/direct effects on the nitrification activity of chemical fertilizer among vegetable soils.

Introduction

Vegetables provide nutrition for human beings by increasing the quality and number of consumed foods (Girard et al., 2012; Chadha et al., 2012; Jaenicke and Virchow, 2013; Weinberger, 2013). However, the amount of vegetable intake in such developing countries as Bangladesh is usually less than the suggested amount of 400 g/day (Keatinge et al., 2011). For some time, local and international non-government organizations (NGOs) have promoted vegetable production in Bangladesh, (Talukder et al., 2000), which could increase the amount of food produced, as well as increase the nutrients provided, such as vitamin A, proteins, carbohydrates, antioxidants, etc. (Bushamuka et al., 2005; Kumar and Quisumbing, 2011; Alcázar-Valle et al., 2020).

Nitrification is one of the most important processes in vegetable plant growth and nutrient production (Zhang et al., 2015). Plants do not absorb atmospheric nitrogen (N2) in the air directly, but instead, use N2 as nitrate, which is highly important for plants' growth and development (Yan et al., 2014). Nitrification is carried out by a two-step procedure in which phylogenetically dissimilar clusters of ammonia-oxidizing archaea (AOA) and/or bacteria (AOB) oxidize ammonia primarily to nitrite (Könneke et al., 2005), and then to nitrate through nitrite-oxidizing bacteria (NOB), which is an essential process in nitrogen cycling (Zhang et al., 2011). Nitrifying bacteria play roles by way of crucial enzymes in the nitrification process such as hydroxylamine oxidoreductase, which oxidizes hydroxylamine to nitric oxide, ammonia monooxygenase, which oxidizes ammonia to hydroxylamine, and nitrite oxidoreductase, which oxidizes nitrite to nitrate (Kuypers et al., 2018). Numerous groups of autotrophic AOA and AOB translate ammonia to nitrite via hydroxylamine (Prosser and Nicol, 2012) and a limited group of Proteobacteria oxidize nitrite to nitrate. Further, soil properties and environmental factors, such as soil pH, influence nitrification. The rates of nitrification depend directly/indirectly on N inputs to the system associated with external factors (Norton and Ouyang, 2019). Fertilizer inputs are direct inputs to the soil mineral N pool and enhanced transfer of N may result from either biological fixation or fertilizer, which will also contribute to N inputs (Maheswari et al., 2017).

Comammox (complete ammonia oxidizers), which oxidize ammonia to nitrate in a single organism, the bacterial genus Nitrospira (van Kessel et al., 2015; Daims et al., 2015), were found previously to comprise only canonical nitrite oxidizers (Lebedeva et al., 2008, Lebedeva et al., 2011; Spieck et al., 2006). It is very important to know how often comammox Nitrospira arises in nitrifying microbial communities, and how important they are for nitrification compared to ammonia-oxidizing archaea (AOA) and bacteria (AOB), and NOB. Nitrospira is distributed globally and represents the most diverse group of NOB known (Daims et al., 2015). Nevertheless, their relative effects on the AOB and AOA in agricultural soils are still undefined (Chen et al., 2008).

The abundance of nitrifying bacteria, as well as that of comammox amoA N. inopinata bacteria, and their effects on the NNR in vegetable soils in Bangladesh remain unknown. Numerous studies have focused on nitrification and related microbes under various fertilization regimes (Wang et al., 2019; Sun et al., 2020). Although soils' bacterial diversity is related to plant biomass, and soil properties and biological processes support microbial diversity's effects on plant biomass (Chen et al., 2020), the responses of plants and microbes to the nitrification activity of chemical fertilizers in vegetable soils are unknown. This work is focused on the responses of plants and microbes, specifically nitrifying archaea/bacteria and comammox amoA N. inopinata bacteria, to the NNRs of chemical fertilizers in four vegetable soils. Consequently, the objectives were to determine the NNRs and the abundance of nitrifying archaea/bacteria and comammox amoA N. inopinata bacteria in vegetable soils in the Kushtia district of Khulna division, Bangladesh. The effect of pH and temperature on the NNRs was also determined.

Section snippets

Sample collection

The study was performed in the Kushtia region in the southwestern region of Bangladesh and covered randomly selected villages, in which we conducted surveys of farmers to collect information about the amount and types of chemical fertilizers they use in their vegetable fields. The experimental location and other information on the soils are detailed in Table 1. The study was conducted in farmers' fields at multiple testing sites in the Kushtia districts. We selected such vegetables as Brinjal (

Local farmers' use of chemical fertilizers in vegetable soils

Vegetables are the crops produced mostly in Bangladesh, and the local farmers indicated in the surveys that they use fertilizers extensively to increase the crop yields. The chemical fertilizers used during cropping and their amount are shown in Table 1. Local farmers in the Kushtia district use different chemical fertilizers, including urea (108 to110 kg−1 h−1 y−1 dm), potassium (58 to 60 kg−1 h−1 y−1 dm), phosphate (105 to 110 kg−1 h−1 y−1 dm), and di-ammonium phosphate (DAP) (58 to 60 kg−1 h

Chemical fertilizers' effects on vegetable soils

Previous studies have found that the use of chemical fertilizers had a distinct effect on the biochemical properties of soil, such as fluctuations in SOC, pH, moisture, and N2 compositions in diverse crops, for example, rice, corn, wheat, and others (Rahman et al., 2020; Rahman et al., 2018; Bnnemann et al., 2006). In this study, the chemical properties of vegetable soils indicated that the concentrations of ammonium, nitrate, SOC total C, and total N were significantly higher in vegetable

Conclusion

Farmers in Bangladesh apply various chemical fertilizers to vegetable field soils. The NNRs were significantly higher (p < 0.05) in vegetable soils, except for L. siceraria plant soils, compared to control soils, and both pH and temperature were found to influence nitrification activity. The abundance of comammox amoA N. inopinata ranged from 9.34E+05 to 4.55E+06 copies per gram dry soil and their distribution was found to be 28 to 72% of the nitrifying (AOB, and NOB) amoA genes. Among the

Declaration of competing interest

All authors declare that they have no conflict of interest.

Acknowledgments

The authors wish to thank Dr. Debra L. Forthman, Professional editor employed by Editor World, for checking the paper's English and grammatical errors. The authors thank the Department of Biotechnology and Genetic Engineering, Islamic University, Kushtia-7003, Bangladesh for the research facilities. They also thank Mr. S. Al-Din of INVENT technology, for helping with the molecular analysis.

Ethical approval

The authors of this study performed no treatments on humans or animals.

References (62)

  • X. Sun et al.

    Soil N transformation rates are not linked to fertilizer N losses in vegetable soils with high N input

    Soil Tillage Res.

    (2020)
  • Z. Wang et al.

    Different ammonia oxidizers are responsible for nitrification in two neutral paddy soils

    Soil Tillage Res.

    (2019)
  • J. Zeng et al.

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

    Soil Biol. Biochem.

    (2016)
  • M. Zhang et al.

    A 2-yr field assessment of the effects of chemical and biological nitrification inhibitors on nitrous oxide emissions and nitrogen use efficiency in an intensively managed vegetable cropping system

    Agric. Ecosyst. Environ.

    (2015)
  • M. Alcázar-Valle et al.

    Bioactive compounds, antioxidant activity, and antinutritional content of legumes: a comparison between four Phaseolus species

    Molecules

    (2020)
  • S. Arai et al.

    Potential N2O emissions from leguminous tree plantation soils in the humid tropics

    Glob. Biogeochem. Cycles

    (2008)
  • E.K. Bnnemann et al.

    Impact of agricultural inputs on soil organisms—a review

    Soil Res.

    (2006)
  • V.N. Bushamuka et al.

    Impact of a homestead gardening program on household food security and empowerment of women in Bangladesh

    Food Nutr. Bull.

    (2005)
  • M.L. Chadha et al.

    Home gardens: an intervention for improved health and nutrition in selected states of India

    Acta Hortic.

    (2012)
  • Y. Chao et al.

    Novel nitrifiers and comammox in a full-scale hybrid biofilm and activated sludge reactor revealed by metagenomics approach

    Appl. Microbiol. Biotechnol.

    (2016)
  • X.P. Chen et al.

    Ammonia-oxidizing archaea: important players in rhizosphere soil?

    Environ. Microbiol.

    (2008)
  • H. Daims et al.

    Complete nitrification by Nitrospira bacteria

    Nature.

    (2015)
  • E.A. Davidson et al.

    Testing a conceptual model of soil emissions of nitrous and nitric oxides: using two functions based on soil nitrogen availability and soil water content, the hole-in-the-pipe model characterizes a large fraction of the observed variation of nitric oxide and nitrous oxide emissions from soils

    BioScience.

    (2000)
  • J. Ehrmann et al.

    Plant: soil interactions in temperate multi-cropping production systems

    Plant Soil

    (2014)
  • H. Erickson et al.

    Former land-use and tree species affect nitrogen oxide emissions from a tropical dry forest

    Oecologia.

    (2002)
  • A.W. Girard et al.

    The effects of household food production strategies on the health and nutrition outcomes of women and young children: a systematic review

    Paediatr. Perinat. Epidemiol.

    (2012)
  • D.W. Graham et al.

    Experimental demonstration of chaotic instability in biological nitrification

    ISME J.

    (2007)
  • J.Z. He et al.

    Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices

    Environ. Microbiol.

    (2007)
  • H. Hu et al.

    Comammox - a newly discovered nitrification process in the terrestrial nitrogen cycle

    J. Soils Sediments

    (2017)
  • S. Ishizuka et al.

    The variation of greenhouse gas emissions from soils of various land-use/cover types in Jambi province, Indonesia

    Nutr. Cycl. Agroecosyst.

    (2005)
  • H. Jaenicke et al.

    Entry points into a nutrition-sensitive agriculture

    Food Secur.

    (2013)
  • Cited by (18)

    • Seasonal dynamics of soil and microbial respiration in the banj oak and chir pine forest of the central Himalaya, India

      2023, Applied Soil Ecology
      Citation Excerpt :

      The soil bulk density (g cm−3) was determined using the known volume of the core cylinder (Okalebo et al., 2002), while soil pH was measured in a 1:2.5 (w/v) soil to solution ratio (Kumar and Garkoti, 2022). Chromic acid wet oxidation was used to estimate soil organic carbon (SOC) (Khanom et al., 2021). Soil total nitrogen (TN) content was measured by using micro-Kjeldahl digestion and distillation unit method (Jackson, 1958).

    • Effect of pesticides on nitrification activity and its interaction with chemical fertilizer and manure in long-term paddy soils

      2022, Chemosphere
      Citation Excerpt :

      Nitrification is the biological ammonia or ammonium oxidation to nitrite followed by two steps oxidation process carried out by nitrifying bacteria (Ali et al., 2021; Sintia et al., 2021; Nahar et al., 2020). It is an important part of the nitrogen cycle as well as considered as ecological and agricultural importance (Khanom et al., 2021; Stefanowicz et al., 2020). Antibiotic resistance genes (ARGs) are recognized as emergent environmental pollutants (Anand et al., 2021; Li et al., 2021; Rahman et al., 2018).

    • Ammonia volatilization and Sporosarcina genus abundance in an Oxisol enriched with urea, compost and biochar

      2022, Applied Soil Ecology
      Citation Excerpt :

      However, the soil NH4+ concentration was lower at 28 days than at 5 days, indicating that NH4+ ions decreased in the soil solution. This decrease in NH4+ ions in soil solution can have occurred due to continuous AV and nitrification processes in soil (Khanom et al., 2021; Pertile et al., 2021). Pertile et al. (2021) reported that urea application in soil increased the abundance of nitrifying archaea/bacteria, oxidizing NH3 and NH4+ forms to nitrite (NO2−) and nitrate (NO3−) steps.

    • Diversity and community composition of nirS-type denitrifying bacteria and ammonia-oxidizing archaea in biofilm samples attached to bio-substrate and abio-substrates in integrated ecological floating bed systems

      2022, Ecological Engineering
      Citation Excerpt :

      Nitrification is carried out by a two-step oxidation procedure, involving the conversion of ammonia to nitrite (i.e., ammonia oxidation) and then nitrite to nitrate (i.e., nitrite oxidation) (Könneke et al., 2005; Prosser and Nicol, 2008; Canfield et al., 2010). Of these two nitrification steps, ammonia oxidation is the first and rate-limiting step, both ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) catalyze this first step (Khanom et al., 2021; Wang et al., 2021a). Previous studies have confirmed that AOA and AOB normally co-exist in various ecosystems (Wang and Gu, 2013; Wang et al., 2021b; Xiao et al., 2021).

    View all citing articles on Scopus
    1

    Equal contribution of both authors as co-first authors.

    View full text