Cadmium adsorption to clay-microbe aggregates: Implications for marine heavy metals cycling
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.
Section snippets
Preparation of bacterial cells
Cyanobacterial strain Synechococcus sp. PCC 7002 was grown and harvested in a manner similar to that described by Liu et al. (2015). The bacteria were inoculated in media A (Stevens and Van Baalen 1973) supplemented with 0.01 M NaNO3 (designated A+ media; Stevens and Porter 1980) and buffered with 1 M Tris at pH 8.2. Stock bacteria were cultured on A+ agar plates at 30 °C. Once a suitable colony developed on the plate, cells were transferred into 50 mL of A+ media using an inoculation loop to
Zeta potential and particle size distribution
The zeta potentials of Synechococcus cells, individual clay minerals, and the composite of Synechococcus and clay minerals are plotted against pH in Fig. 1. In terms of individual zeta potentials, Synechococcus demonstrated a continuous increase in net negative surface charge from pH 4.0 to 6.0, and above which the surface charge remains constant. Kaolinite, montmorillonite and illite also exhibited an increasingly negative surface charge with increasing pH, with montmorillonite being the most
Discussion
In seawater, microorganisms and clay particles commonly exist in the form of aggregates (Avnimelech et al., 1982, Verspagen et al., 2006, Kennedy et al., 2014). Microbial cells provide abundant reactive ligands which can deprotonate over a wide range of pH (Beveridge and Graham, 1991, Fein et al., 1997, Cox et al., 1999, Lalonde et al., 2008, Liu et al., 2015). These ligands are capable of binding metal cations and serving as nucleation sites for mineral authigenesis (Konhauser et al., 1994,
Conclusion
In this study, we observed that Synechococcus cells accumulate on clay mineral surfaces, promoting the development of larger microaggregates. In Synechococcus-clay mineral mixture systems, Cd preferably adsorbs to the Synechococcus surface relative to the sites on the clay mineral surfaces. Using Cd stability constants calculated for each sorbent, the CA surface complexation modelling approach provides reasonable predictions of Cd adsorption onto Synechococcus-clay composites. Future studies
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.
Acknowledgements
This work was financially supported by the National Natural Science Foundation of China as a general project (grant No. 21677080) and a Shandong joint project (grant No. U1906222), the Ministry of Education, People’s Republic of China as a 111 program (grant No. T2017002), and the Fundamental Research Funds for the Central Universities (ZX20180412). This work was also supported by NSERC Discovery Grants to KOK (RGPIN-165831) and DSA (RGPIN-04134).
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