The mechanism for inhibiting acidification of variable charge soils by adhered Pseudomonas fluorescens☆
Graphical abstract
Introduction
The plant rhizosphere hosts a number of bacteria which could be both beneficial and harmful to the plant (Li et al., 2013). Bacteria have the ability to degrade organic pollutants as well as to reduce the toxic effects of heavy metals on plants. As plant growth-promoting agents, rhizobacteria produce special phytohormones such as gibberellins, auxins, and cytokines to promote root elongation and flowering. They can also increase the solubility of soil phosphorus (Gamalero et al., 2009; De Souza et al., 2015; Prasad et al., 2015). The promotion of plant growth by rhizobacteria is achieved either through facilitating adsorption of nutrients such as nitrates, phosphates, and essential minerals, or regulating the adverse effects of pathogens on plant growth (Aloo et al., 2019). For instance, Whipps (2001) demonstrated that bacteria produced substances that degraded the virulence factor or the cell walls of phytopathogens thereby protecting plants from their harmful effects. The presence of bacteria in soils have also been shown to enhance the cation retention ability (Liu et al., 2015; Ren et al., 2019), with their extracellular polymeric substances (EPS) playing a vital role in heavy metal immobilization in variable charge soils (Nkoh et al., 2019a, b).
The percentage of acid soils in the world is fast increasing due to a rapid increase in soil acidification (Von Uexkull and Mutert, 1995). Soil acidification leads to soil infertility, increase in Al and Mn toxicities, and the deficiency of P, Mo, Ca, and Mg, and thus decrease in crop production (Bowman et al., 2008; Singh et al., 2017). The natural acidification process in soils is fast changing from a slow and steady process to a huge challenge due to anthropogenic activities such as acid deposition and increasing use of nitrogenous fertilizers (Zhang et al., 2008; Guo et al., 2010; Xie et al., 2019). In acidic soils, Al toxicity is regarded as the main factor limiting plant growth by inhibiting root elongation (Yamamoto, 2019), and it was predicted that the concentration of active Al in acidic soils increased remarkably with decreasing pH (Kochian et al., 2005). Another adverse effect of soil acidification is the reduction in plant biodiversity (Bowman et al., 2008). During acidification, soils experience different ranges of buffering and this is often associated with the release of different cations in soil solution (Shi et al., 2018a, b). Al concentration in soil solution is controlled by the dissolution equilibrium of different Al-containing minerals, which also depends largely on soil pH (Sposito, 1989). At pH below 4.5, it was reported that the concentration of Al3+ in soil solutions increased to toxic levels as more Al3+ was released from soil solid (Bowman et al., 2008). Therefore, it is of significance to retard soil acidification.
Soils rich in particles with amphoteric surface properties in the Oxisols, Ultisols, Alfisols, Spodosols, and Andisols orders are considered to be variable charge soils. They have developed under intensive weathering in subtropical and tropical regions or from volcanic ash parent material (Van Ranst et al., 2017). There are huge areas of variable charge soils in tropical and subtropical regions of China, which are rich in iron (Fe) and aluminum (Al) oxides due to intensive weathering and leaching under hot and humid climatic conditions (Xu et al., 2016). These soils are generally acidic and easy to acidify.
Soil acidification rate depends on both acid inputs and soil pH buffering capacity (pHBC). Soil pHBC is a measure of the soil’s ability to resist acidification and retard the decline in pH (Xu et al., 2012). For soils in the tropics and subtropics, the cation exchange capacity (CEC) plays a vital role in determining their pHBC (Aitken, 1992; Nelson and Su, 2010; Xu et al., 2012; Yang et al., 2020). The clay mineral content of these soils also influence their pHBC. The contribution made by the 2:1 type clay minerals (e.g. vermiculite) towards enhancing the pHBC is greater than the contribution made by the 1:1 type minerals (e.g. kaolinite) (Xu et al., 2012; Yang et al., 2020). Also, the soil organic matter is made up of functional groups (e.g. –COOH or –OH) attached to organic chains which are liable to deprotonation or protonation as solution pH changes (Sposito, 1989; Shi et al., 2017). These weakly acidic functional groups and their corresponding organic anions construct pH buffering systems. Therefore, materials which can increase soil organic matter content will help to enhance soil pHBC.
The amendment of soils with crop residues in the form of biochars has received considerable attention recently, and their ability to enhance the pHBC of variable charge soils was investigated (Xu et al., 2012; Shi et al., 2017, 2018a, b). In one of such studies (Shi et al., 2017), the authors observed that cations were released into solution during protonation of carboxyl groups on the biochar surface. This confirmed that biochar enhanced soil pHBC through the association of organic anions on the biochar with H+ to form neutral molecules. Similar to soil organic matter and biochars, there are abundant functional groups on the bacteria surface, which explains why variable charge soils have great adhesion capacity for bacteria (Liu et al., 2015; Ren et al., 2018a). We hypothesize that rhizobacteria adhered on variable charge soils will inhibit the acidification of the soils. This study was designed with the aim to (a) investigate the effect of Pseudomonas fluorescens (P. fluorescens) on the acidification of two Ultisols, (b) evaluate the different forms of Al in these soils after acidification in the presence of bacteria, (c) discover the mechanisms for the inhibition of soil acidification by the bacteria.
Section snippets
Determination of the basic properties of the soils
The Ultisols were collected from Liuzhou, Guangxi Province and from Yingtan, Jiangxi Province of China. They were air-dried and ground to pass a 60-mesh sieve (250 μm). The basic properties of the soils are given in Table 1. Soil pH was determined in distilled deionized water at a ratio of 1:2.5 with an Orion A211 pH meter. Soil organic matter was determined using the dichromate method. Soil CEC was determined by the ammonium acetate method at pH 7.0 (Pansu and Gautheyrou, 2006). Soil clay
The effect of P. fluorescens on the Ultisol’s ability to resist changes in pH caused by acid or alkali
The CEC of the soils was low and 4.5 and 6.3 cmol kg−1 for Ultisol-Liuzhou and Ultisol-Yingtan, respectively (Table 1). For these soils, the mineral composition affects their CEC, as well as their pHBC (Xu et al., 2012; Yang et al., 2020). Specifically, the content of 1:1 type mineral of kaolinite was larger than the 2:1 type mineral of vermiculite (Table S1), with the contribution of the former towards enhancing soil CEC being inferior. Thus, it was expected that the pHBC of the soils was low.
Conclusions
The adhesion of P. fluorescens on variable charge soils enhanced the ability of the soils to resist the decline in pH and decreased the production of soluble Al and exchangeable Al3+ during soil acidification. The association of organic anions on the bacteria with H+ to form neutral molecular groups was the main mechanism for the inhibition of the bacteria on soil acidification. ATR-FTIR analyses and the change of the zeta potential of the bacteria with pH confirmed the protonation of organic
Main findings
Pseudomonas fluorescens adhered on variable charge soils inhibited the acidification of the soils and the production of soil soluble Al and exchangeable Al. Association of organic anions on the bacteria with H+ to form neutral molecular groups was mainly responsible for the inhibition of soil acidification by the bacteria.
CRediT authorship contribution statement
Jackson Nkoh Nkoh: Conceptualization, Methodology, Writing - original draft. Jing Yan: Methodology. Ren-Kou Xu: Conceptualization, Methodology, Writing - review & editing, Supervision.
Acknowledgements
This study was supported by the National Natural Science Foundation of China (Grant No. 41571233). We also acknowledge the CAS-TWAS President’s Fellowship for international Ph. D students in China.
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