Cadmium adsorption to clay-microbe aggregates: Implications for marine heavy metals cycling

Abstract

Interactions between microorganisms and clay minerals influence the transport and cycling of metal contaminants in both marine and terrestrial environments. The present study was conducted to quantify the adsorption of dissolved cadmium, Cd(II), under seawater-like conditions to the marine cyanobacterium Synechococcus sp. PCC 7002, three common clay minerals (kaolinite, montmorillonite and illite), as well as cell-clay aggregates. We show here that the Synechococcus-only experiments removed the most Cd above pH 5.5, followed in decreasing order by aggregates of 50% cells:50% individual clays, aggregates of cells and all 3 clays, and individual clays. Electron microscope imaging showed that clays associated in a tangential edge-on orientation to the cells in Synechococcus-clay mineral aggregates. A non-electrostatic surface complexation modeling approach was used to fit Cd adsorption onto Synechococcus cells and individual clay minerals. The resulting Cd binding constants were then used in consort with surface functional group pKa values and site concentrations to accurately predict the extent of Cd adsorption onto the Synechococcus-clay mineral aggregates using the component additivity (CA) approach. We observed that the addition of cyanobacterial cells to clay mineral suspensions led to significantly larger mean aggregate sizes of clay minerals, enhancing the clay sedimentation rate. Although specifically focused on Cd, our study indicates that the ratio of bacterial plankton to clay minerals is an important determinant in terms of understanding the rate with which metals are transferred from the water column to the seafloor.

Introduction

Microorganisms and clay minerals rarely exist alone in the natural environment (Ledin, 2000, Zhou and Huang, 2001, Zeng et al., 2020). Rather, microorganisms are generally adsorbed to solid surfaces, including clay minerals, as a consequence of attractive van der Waals interactions, hydrogen bonding, hydrophobicity, surface roughness, surface tension and ion bridging (Ledin et al., 1999, Huang et al., 2000, Yee et al., 2000, Huang et al., 2005, Krause et al., 2019, Li et al., 2019). The surface properties of these aggregates differ dramatically from pure bacterial or mineral surfaces, particularly in terms of surface area and charge, hydrophobicity, double-layer properties, numbers of reactive sites, and potential metal-binding affinity (Neihof and Loeb, 1972, Walker et al., 1989, Huang et al., 2005, Chen et al., 2009, Putnis and Ruiz-Agudo, 2013, Martinez et al., 2016, Hirst et al., 2017, Zhou, 2017). Indeed, the presence of microbial coatings can alter the reactivity of the underlying mineral surface through masking of high-energy surface sites, providing a variety of new sites for metal binding and/or modifying the electrical properties of the mineral-water interface (Neihof and Loeb, 1972, Templeton et al., 2001, Templeton et al., 2003, Phoenix et al., 2002, Wigginton, 2014, Kikuchi et al., 2019, Zeng et al., 2020). It is, therefore, important to consider bacteria-mineral aggregates as a geochemically reactive solids and to quantify their metal scavenging ability as mixed adsorbent systems.

In the past decade, the database pertaining to proton and metals adsorption onto microbial cells and clay minerals has expanded considerably, which when combined with surface complexation modelling (SCM), has allowing for improved predictions of their heavy metal scavenging ability in aquatic environments (Fein et al., 1997, Ueshima et al., 2008, Gu et al., 2010, Mishra et al., 2010, Liu et al., 2015, Liu et al., 2018). Other studies have examined the role of bacteria-clay mineral aggregates in terms of their metal binding. For instance, Walker et al. (1989) observed that Bacillus subtilis cell wall-clay and Escherichia coli cell wall-clay mixtures bound 20–90% less metal than equal amounts of the individual components did. Transmission electron microscopy and energy-dispersive X-ray spectroscopy confirmed that the adsorption of cells to clay resulted in the masking or neutralization of chemically reactive adsorption sites normally available to metal ions. Huang et al. (2000) reported that the presence of Rhizobium fredii increased the Cd adsorption affinity of kaolin (116.5%). Templeton et al., 2001, Templeton et al., 2003 showed that at least 50% of the total bound Pb(II) was associated with the Burkholderia cepacian biofilm component at pH < 5.5, and goethite became dominant (70% adsorption) above pH 6.0 in systems exposed to solutions of Pb(II). Kuang et al. (2019) reported that a combination of extracellular polymeric substances (EPS) secreted from Microcystis aeruginosa with kaolinite created new adsorption sites, which increased Cu(II) adsorption. The above studies suggest that heavy metals adsorption onto microbe-clay minerals aggregates is not only different than those of the individual constituent components, but aggregation leads to a more complex surface for metal adsorption reactions. Furthermore, the surface reactivity of microbe-clay mineral aggregates is influenced by bacterial species (especially the functionality and composition of cell wall envelopes) and the clay mineral type.

It has been demonstrated that a significant fraction of primary production in the oceans may be attributed to the growth of planktonic cyanobacteria (Fisher, 1985, Flombaum et al., 2013), with some genera, such as Synechococcus, reaching densities on the order of 10⁴-10⁶ cells/mL in the photic zone (Waterbury et al., 1979). Clay minerals are also widely distributed in marginal marine settings; the total suspended sediment delivered by all rivers to the oceans annually is estimated to be 13.5 × 10⁹ tons (Milliman and Meade, 1983), of which 10–25% is clay (Manheim et al., 1970, Schroeder et al., 2015). These clays can serve as significant scavengers for heavy metals, and transport and deposit heavy metals in rivers and estuaries (Liu et al., 2018, Hao et al., 2020). When considering aggregates of cyanobacterial cells and clay minerals as biosorbents for metal binding (Kikuchi et al., 2019), it is important to mimic closely the chemical conditions of seawater. However, such studies are limited to date.

In the present work, we investigated Cd(II) adsorption by mixtures of the marine cyanobacterium Synechococcus sp. PCC 7002 (henceforth referred to as Synechococcus) and three types of clay minerals: kaolinite, montmorillonite, and illite. We focused on this system because clay minerals and planktonic microorganisms are ubiquitous suspended particulate matter in the oceans, the three clay minerals encompass the range of structural compositions found in nature (1:1 of kaolinite, 2:1 of montmorillonite and illite), and the surface reactivities of the adsorbents have been characterized previously (Liu et al., 2015, Liu et al., 2018). We hypothesized that in systems where a clay mineral and planktonic Synechococcus cells were mixed, aggregation would occur to an extent where surface functional group site blockage would lower the observed extent of Cd adsorption versus component additivity (CA) model predictions of sorption, which do not consider site blockage. Further, we hypothesized that the extent of site blockage and reduced Cd adsorption would be considerable at the high ionic strength tested (0.56 M), where clay mineral – bacterial cell aggregation is enhanced, versus previous experiments that used far lower ionic strengths (e.g., Alessi and Fein, 2010). Our systems necessarily have bacterial cells, clay minerals, and Cd concentrations that are higher than expected ones in freshwater, estuarine, or marine conditions; however, aggregation of cells and clay minerals is enhanced at higher sorbent concentrations, allowing us to test whether site blockage is an important factor in reducing Cd sorption to the aggregates. To test the two hypotheses above, there were three aims in this study: (1) determining the morphology and size distribution of the cell-clay mineral aggregates; (2) observing Cd adsorption onto the Synechococcus-clay mineral composites; and (3) testing the ability of the CA surface complexation modeling approach to predict Cd adsorption behaviors in various Synechococcus-clay mineral aggregates and compare those predictions to observed Cd removal from aqueous solution.