Microbial biomodification of clay minerals

Abstract

Clay minerals are important reactive centers in the soil system. Their interactions with microorganisms are ubiquitous and wide-ranging, affecting growth and function, interactions with other organisms, including plants, biogeochemical processes and the fate of organic and inorganic pollutants. Clay minerals have a large specific surface area and cation exchange capacity (CEC) per unit mass, and are abundant in many soil systems, especially those of agricultural significance. They can adsorb microbial cells, exudates, and enzymes, organic and inorganic chemical species, nutrients, and contaminants, and stabilize soil organic matter. Bacterial modification of clays appears to be primarily due to biochemical mechanisms, while fungi can exhibit both biochemical and biomechanical mechanisms, the latter aided by their exploratory filamentous growth habit. Such interactions between microorganisms and clays regulate many critical environmental processes, such as soil development and transformation, the formation of soil aggregates, and the global cycling of multiple elements. Applications of biomodified clay minerals are of relevance to the fields of both agricultural management and environmental remediation. This review provides an overview of the interactions between bacteria, fungi and clay minerals, considers some important gaps in current knowledge, and indicates perspectives for future research.

Introduction

Clay minerals are ubiquitous weathering and low-temperature hydrothermal alteration products in nature (Evans, 1992). They are also the most abundant types of minerals in terrestrial systems, especially in the pedosphere (Mackenzie & Garrels, 1971). Naturally abundant clay minerals, e.g., montmorillonite, kaolinite, and illite, are a class of layered aluminosilicates that possess strong sorption properties, high cation exchange capacities (CEC) and expansibility (Table 1) (Murray, 2000; Zhang, Zhou, Lin, Tong, & Yu, 2010). They play direct and critical roles in soil and terrestrial ecosystem processes, e.g., the formation and development of soil, stabilization of soil organic carbon, global cycling of the elements, and the sorption of nutrients, enzymes and contaminants (Adamo, Barre, Cozzolino, Di Meo, & Velde, 2016; Barré, Fernandez-Ugalde, Virto, Velde, & Chenu, 2014; Bruun, Elberling, & Christensen, 2010; Burford, Fomina, & Gadd, 2003; Ezzaïm, Turpault, & Ranger, 1999; Stucki & Kostka, 2006).

Mineral surfaces play an integral role in microbial attachment and/or detachment (Claus & Filip, 1990), capable of altering growth, biomass, and metabolite production (Fomina and Gadd, 2002, Fomina and Gadd, 2003; Lunsdorf, Erb, Abraham, & Timmis, 2000; Zhang et al., 2019), and therefore determining energy generation, nutrient acquisition, cell adhesion, and biofilm formation (Brown, Trainor, & Chaka, 2008; Dong, 2010; Gadd, 2007; Stotzky, 1966). Clay minerals are common in low-temperature environments where microorganisms thrive and their high specific surface area provides nutrients and microhabitats (Dong, Jaisi, Kim, & Zhang, 2009). Microorganisms inhabit a wide range of niches in soil environments and therefore have intimate interactions with clay minerals in nature (Dong, 2012; Li, Zhou, Fiore, & Yu, 2019). The size, shape, and structure of fungal mycelial pellets can be significantly affected by clay minerals (bentonite, palygorskite, and kaolinite) (Fomina & Gadd, 2003) while the presence of 2:1 type smectite promoted the rapid formation of bacterial biofilms (Alimova et al., 2006).

Microbial properties, at physiological and genetic levels, can therefore be strongly influenced by clay minerals (Babin et al., 2013; Ma et al., 2017; Marshall, 1975; Zhang et al., 2019). Clay minerals may either stimulate or inhibit microbial growth and function, as revealed by many metabolic indices such as analysis of microbial respiration (Stotzky and Rem, 1966, Stotzky and Rem, 1967; Su et al., 2019; Zhang et al., 2019). Soil microbial community composition can therefore be strongly affected by clay minerals (Carson, Rooney, Gleeson, & Clipson, 2007; Steinbach et al., 2015). Moreover, clay minerals also facilitate horizontal gene transfer between microorganisms (Cuadros, 2017). In particular, the Yoshida Effect has been observed, which describes a novel transformation method based on the inoculation of transforming DNA into bacteria by means of fibrous clay minerals, e.g., sepiolite (Castro-Smirnov et al., 2020; Yoshida, 2007; Yoshida & Ide, 2008).

Increasing attention has been focused on the role of microorganisms in the biomodification of clay minerals. Microorganisms can regulate mineralogical processes as a result of mineral dissolution, mineral formation, and alteration of mineral surface chemistry and reactivity (Hutchens, 2009; Kong et al., 2014; Naimark, Erouschev-Shack, Chizhikova, & Kompantseva, 2009; Sullivan & Gadd, 2019). The main mechanisms include redox transformations (e.g., affecting structural iron) or metabolite excretion, such as chelating compounds (e.g., siderophores), organic acids (e.g., oxalic acid, citric acid) and inorganic acids (e.g., carbonic acid arising from respiratory carbon dioxide (CO₂)) (Dai, Zhao, Dong, Wang, & Huang, 2014; Dong et al., 2009; Gadd, 2007; Hong, Fang, Cheng, Wang, & Churchman, 2016; Kim, Dong, Seabaugh, Newell, & Eberl, 2004; Liu et al., 2012; Müller, 2015). Among the various types of clay minerals that interact with microorganisms, smectite has received significant interest due to its widespread occurrence and pronounced physicochemical properties such as a large surface area, expansibility, and a high cation exchange capacity (Alimova et al., 2009; Kim et al., 2004; Yu et al., 2013; Zhang et al., 2019). Unsurprisingly, it has been reported that microorganisms may also greatly influence the physical and chemical properties of smectite (Kim et al., 2004; Stucki & Kostka, 2006; Stucki, Lee, Zhang, & Larson, 2002; Yang et al., 2016). For example, Kong et al. (2014) observed that more silicon (Si) was released from montmorillonite than from kaolinite and illite at same low molecular weight organic acids (LMWOAs) concentration, and oxalic acid was stronger than citric acid for transformation of montmorillonite. In addition, the compositional and structural characteristics of layered clay minerals allow for a variety of modifications by organic, polymeric or other biological molecules (An, Zhou, Zhuang, Tong, & Yu, 2015; Dumat, Quiquampoix, & Staunton, 2000; Yu et al., 2013). Such modified clay minerals will possess additional functional groups, increased hydrophobicity and adhesion area, and lowered steric hindrance. By using first principles molecular dynamics (FPMD) simulation, several studies have found that isomorphic substitution can influence the edge surface pKa of clay minerals and the surface complexation of toxic metal cations (Liu, Cheng, Sprik, Lu, & Wang, 2014; Liu et al., 2013; Liu, Yao, Han, Zhang, & Banwart, 2017).

A wide range of microorganisms produce extracellular polymeric substances (EPS) which provide an ideal micro-environment or matrix for chemical reactions, e.g., bioprecipitation, nutrient and particulate entrapment, and protection against environmental stress (e.g., salinity and desiccation) as well as toxicants such as antibiotics and toxic metals (Comte, Guibaud, & Baudu, 2008; Costa, Raaijmakers, & Kuramae, 2018; Decho & Gutierrez, 2017; Fang et al., 2010; Gadd, 2010; Shi et al., 2016; Wang et al., 2018). EPS can be considered as a critical micro-zone linking the biosphere and pedosphere. It is well known that bacterial biofilms and activated EPS may significantly affect clay interlayer expansion (Alimova et al., 2009). However, different types of microorganism can possess different mechanisms of mineral formation and/or dissolution. Therefore, it is important to understand the mechanisms of interaction between different species of microorganisms and clay minerals.

Bacterial and fungal interactions with clay minerals have been widely investigated. This article reviews the research progress on the interactions between bacteria and fungi and clay minerals. We highlight the importance of different types of microorganisms to soil ecological processes, as well as the relevance and application of these interactions to soil development and management and/or environmental remediation.