Inoculation of Bacillus spp. Modulate the soil bacterial communities and available nutrients in the rhizosphere of vetiver plant irrigated with acid mine drainage

doi:10.1016/j.chemosphere.2020.128345

Chemosphere

Volume 263, January 2021, 128345

https://doi.org/10.1016/j.chemosphere.2020.128345 Get rights and content

Highlights

•
AMD inhibited plant growth and shifted microbial community structure.
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Bacillus spp. showed P-solubilization, IAA and siderophore production.
•
Bacillus spp. enhanced vetiver adaptability and biomass in AMD-impacted soils.
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Bacillus spp. diluted AMD impacts by improving soil P, N, & microbial communities.

Abstract

Acid mine drainage (AMD) is one of an important pollution sources associated with mining activities and often inhibits plant growth. Plant growth promoting bacteria has received extensive attention for enhancing adaptability of plants growing in AMD polluted soils. The present study investigated the effect of plant growth promoting Bacillus spp. (strains UM5, UM10, UM13, UM15 and UM20) to improve vetiver (Chrysopogon zizanioides L.) adaptability in a soil irrigated with 50% AMD. Bacillus spp. exhibited P-solubilization, IAA and siderophore production. The Bacillus spp. strains UM10 and UM13 significantly increased shoot (4.2–2.5%) and root (3.4–1.9%) biomass in normal and AMD-impacted soil, respectively. Bacillus sp. strain UM20 significantly increased soil AP (379.93 mg/kg) while strain UM13 increased TN (1501.69 mg/kg) and WEON (114.44 mg/kg) than control. Proteobacteria, Chloroflexi, Acidobacteria and Bacteroidetes are the dominant phyla, of which Acidobacteria (12%) and Bacteroidetes (8.5%) were dominated in soil inoculated with Bacillus sp. strain UM20 while Proteobacteria (70%) in AMD soil only. However, the Chao1 and evenness indices were significantly increased in soil inoculated with Bacillus sp. strain UM13. Soil pH, AP and N fractions were positively correlated with the inoculation of bacterial strains UM13 and UM20. Plant growth promoting Bacillus spp. strains UM13 and UM20 were the main contributors to the variations in the rhizosphere bacterial community structure, improving soil available P, TN, WEON, NO₃⁻-N thus could be a best option to promote C. zizanioides adaptability in AMD-impacted soils.

Graphical abstract

Introduction

The exposure of coal and pyrite minerals to atmospheric oxygen and water resultant into production of highly acidic water, which is known as acid mine drainage (AMD) (RoyChowdhury et al., 2015; Aguinaga et al., 2018). It is mainly characterized by low pH, high salinity, heavy metals, metalloids and sulphate contents (Kefeni et al., 2017). Therefore, untreated AMD can impair the surrounding ecosystems such as soil, surface and ground water and thus harm the health of human and other biotic species (Hallberg, 2010). The United Nations has recently recognized AMD as the second biggest global issue after global warming (Tuffnell et al., 2017) revealing the importance of this environmental challenge. AMD is common in resource rich countries such as China, Brazil, Australia, Canada, Chile, Romania, South Africa and USA. For example, more than 557,000 abandoned AMD sites the USA, 90,000 legacy mine sites in Australia and many sites in Korea and South Africa are producing AMD wastewater (RoyChowdhury et al., 2019; Kefeni et al., 2018). Unfortunately, in China, some farmland that is nearby mining areas has been severely contaminated by AMD (Li, 2017). China has about 5383 abandoned mines, Dabaoshan mines (Shaoguan City, Guangdong Province), are known to have high cancer rates (Chen et al., 2015). In 2015, there were almost 63,433 mines in China mainly producing AMD wastewater (Liu et al., 2015), for instance Tongling (Cu) mine wastewater has pH value ranged from 2.1 to 3.5 and sulphate contents varied from 833 to 6272 mg L⁻¹ (Hua and Li, 2018). The AMD problem in Shanxi province, China, has also received much attention in recent years (Sun et al., 2013) because almost quarter of Chinese coal resources are present in this province. Hence, the AMD is not only in China but also it is a common emerging problem of many leading countries of the world.

AMD could have consequences when drained into soil and water bodies. AMD can change the soil pH, reduce soil organic carbon and impact the soil microbial community and as a result may cause severe effect on the nutrient uptake and plant growth (Quadros et al., 2016). Moreover, due to its low pH, it increases solubility and toxicity of various metals such as Cu, Cd and Zn that compete with essential nutrients of soil (Dong et al., 2018). A few studies highlighted the negative impacts of AMD in plants, for example, it can induce oxidative stress that can cause cellular damage and disrupt morphological and physiological attributes of plant (Gardea-Torresdey et al., 2005). It may also lower the soil pH, which causes deficiency of essential nutrients like N and P to plants (Dean et al., 2019) and consequently, the breakdown of organic matter has reduced due to low microbial activity (Simate and Ndlovu, 2014). Recently, Dong et al. (2018) investigated that AMD (10 mL/g soil) had decreased the available soil P and K up to 63% and 97%, respectively. To overcome, the problems of AMD-impacted soils, recently, vetiver system has been employed. The vetiver (Chrysopogon zizanioides L.) is a comparatively new energy crop, cost effective and eco-friendly technology for the reclamation of AMD-impacted soils. Vetiver has a huge and complex adventitious root system; its unique morphological and physiological attributes has also been considered as a suitable option for management of nutrient deficient AMD-impacted soil (Roongtanakiat et al., 2008). Moreover, vetiver grass is not only growing very well in acidic soil, but also improving its health (Danh et al., 2009). The variations in microbial community structure with the variant of AMD and chemical parameters in natural wetland have recently been reported by Aguinaga et al. (2018). However, little is known about the microbial communities residing in the rhizosphere of vetiver grass, nitrogen and phosphorus dynamics in AMD-impacted soil. Therefore, it is important to characterize soil microbial communities associated to vetiver rhizosphere and compare with soil physico-chemical properties.

The exogenous application of bacteria is another technique to improve establishment of vetiver grass in AMD-impacted soil. Plant growth-promoting bacteria (PGPR) are residing in close association with roots and can play a key role to transform the unavailable form of nutrients into available form for plant through oxidation, nitrification, ammonification, nitrogen fixation and other nutrient cycling processes (Vasquez et al., 2008). Plant growth-promoting Bacillus spp. can improve plant adaptability through colonization, phosphorus solubilization, siderophore and IAA production (Ahmad et al., 2018). The Bacillus spp. are capable of producing exopolysaccharide substances and siderophore that enable them to form biofilms and survive under harsh environments that can improve plant adaptability (Ahmad et al., 2018). In nutrient-deficient AMD environment (Yang et al., 2019), inoculation of Bacillus spp. results in the proliferation of free-living microorganisms which have the ability to mobilize and mineralize unavailable organic P (Nash et al., 2014). Bacillus can also stimulate the breakdown and mineralization of toxic pollutant because they can play a significant role in providing nutrients and carbon source as a result have a potential to restore and maintain AMD-impacted soil (Bastida et al., 2015). In this study, some selected Bacillus spp. strains would be characterized for IAA and production of siderophore and P-solubilization in vitro as well as in vivo and would be correlated with available P, TN, WEON, NO₃⁻-N, and rhizosphere microbial community structure in AMD-impacted soil. A little information is available regarding performance of vetiver plant grown in AMD-impacted soil particularly, when inoculated with different strains of Bacillus spp.. It is, however, highly important to mitigate the AMD stress by manipulation of plant growth-promoting Bacillus spp. to improve soil physicochemical properties, growth and adaptability of vetiver grass. The objectives of this study were to: i) study the effect of AMD on microbial community structures and nutrients (N, P) availability in soil, ii) characterize Bacillus spp. for various growth promoting activities, mineralization of P, and soil N fractions (total N, mineral N: NH₄⁺-N, NO₃⁻-N, microbial biomass N, water extractable organic N), and iii) evaluate the effect of selected Bacillus spp. on the growth indices of vetiver plant and rhizospheric microbial communities in AMD-impacted soil.

Section snippets

Rhizosphere sampling and processing

Soil samples were collected from the rhizosphere of plants growing on the shuimuchong (30° 55′ N, 117° 50^' E) copper mine tailings disposal site which is located approximately 3 km northeast of Tongling City, Anhui Province, Southeast China. The roots of the plants were uprooted gently and soil intact with roots was collected by manual shaking in sterilized sealed plastic bags and stored at 4 °C for further analysis.

Isolation of rhizobacteria

Isolation of heterotrophic bacteria were done on growth media formulated with

Isolation and functional attributes of rhizobacteria

A total of 29 different colonies were isolated and identified from the “the rhizosphere of plants growing on mine tailings” (SFig.1). Of the 29 isolates, following 5 Bacillus spp. strains (UM5, UM10, UM20, UM13 and UM15) were selected for further study based on their robust growth and different plant growth promoting attributes (Table 1). Among 5 bacterial strains, UM5 and UM13 were produced IAA by 23.24–30.33 and 37.42–43.23 mg L⁻¹, respectively in the gradient of 0–5% AMD (Table 1). While

Discussion

The rhizosphere is a prime niche of diverse microbial communities (Venturi and Keel, 2016) and few of them have exhibited plant growth promoting attributes (Ahmad et al., 2018; Tahir et al., 2019). These interactions are important to study particularly in stress conditions. About 29 bacterial isolates were isolated from the rhizosphere of plants grown in an AMD-impacted soil (mine tailings). Most of the strains have identified as Bacillus species and exhibited IAA, P-solubilization and

Conclusion

AMD is a worldwide environmental problem with serious negative impact on plant growth and their adaptability. Based on our results, the inoculation of Bacillus spp. strains UM13 and UM20 could be a best option to reduce deleterious impact of AMD and promote Chrysopogon zizanioides adaptability by increasing heterotrophic soil microbial communities, soil available P, TN, WEON and NO₃–N in AMD-impacted soils. The augmentation of AMD-tolerant and PGP-Bacillus spp. is an innovative approach for the

Credit author statement

Umar Daraz: Conceptualization, Data curation, Experimental work, Writing - original draft, Investigation, Formal analysis; Qingye Sun: Methodology, Supervision, Writing - review & editing; Li Yang: Methodolgy, Investigation, Writing - review & editing; Mingzhu Zhang: Software; Iftikhar Ahmad: Writing - review & editing.

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.

Acknowledgments

This study was funded by the National Natural Science Foundation of China (31800456) and the Key Research and Development Projects in Anhui Province (201904a020027). The authors also thank Zhaojun Wu and Dandan Zhao for their assistance with maintenance of the bacterial isolate collection.

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Inoculation of Bacillus spp. Modulate the soil bacterial communities and available nutrients in the rhizosphere of vetiver plant irrigated with acid mine drainage

Highlights

Abstract

Graphical abstract

Introduction

Section snippets

Rhizosphere sampling and processing

Isolation of rhizobacteria

Isolation and functional attributes of rhizobacteria

Discussion

Conclusion

Credit author statement

Declaration of competing interest

Acknowledgments

Ecotoxicol. Environ. Saf.

J. Environ. Manag.

Soil Biol. Biochem.

Chemosphere

Microbiol.

Sci. Total Environ.

Soil Biol. Biochem.

Coord. Chem. Rev.

Hydrometallurgy

Microbiol. Res.

Soil Biol. Biochem.

Ecotoxicol. Environ. Saf.

J. Clean. Prod.

J. Environ. Chem. Eng.

Agric. Ecosyst. Environ.

Geoderma

Appl. Soil Ecol.

Appl. Soil Ecol.

Field Crop. Res.

Anal. Biochem.

J. Environ. Chem. Eng.

Ann. Agric. Sci.

Sci. Total Environ.

Chemosphere

Ecotoxicol. Environ. Saf.

Trends Plant Sci.

Agric. Ecosyst. Environ.

Geoderma

J. Hazard Mater.

Geoderma

Microbial community shifts in response to acid mine drainage pollution within a natural wetland ecosystem

Front. Microbiol.

The role of root exudates in rhizosphere interactions with plants and other organisms

Annu. Rev. Plant Biol.

The role of root exudates in rhizosphere interactions with plants and other organisms

Annu. Rev. Plant Biol.

Soil restoration with organic amendments: linking cellular functionality and ecosystem processes

Sci. Rep.

Structure and functions of the bacterial microbiota of plants

Annu. Rev. Plant Biol.

Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts

Soil Sci. Soc. Am. J.