Elsevier

Chemical Geology

Volume 212, Issues 3–4, 1 December 2004, Pages 313-327
Chemical Geology

Inhibition and enhancement of microbial surface colonization: the role of silicate composition

https://doi.org/10.1016/j.chemgeo.2004.08.021Get rights and content

Abstract

Classical treatment of cell attachment by models of filtration or coulombic attraction assumes that attachment of cells to mineral surfaces would be controlled by factors such as response to predation, collision efficiency, or coulombic attraction between the charged groups at the mineral and cell surfaces. In the study reported here, the passive model of attachment was investigated using a native microbial consortium and a variety of Al- and Fe-bearing silicates and oxides to determine if other controls, such as mineral composition, also influence the interaction between cells and surfaces. Results from in situ colonization studies in an anaerobic groundwater at pH 6.8 combined with most probable number analyses (MPN) of surface-adherent cells demonstrate that electrostatic effects dominate microbial colonization on positively charged oxide surfaces regardless of mineral composition. In contrast, on negatively charged silicate minerals and glasses, the solid phase composition is a factor in determining the extent of microbial colonization, as well as the diversity of the attached community. In particular, silicates containing more than 1.2% Al exhibit less biomass than Al-poor silicates and MPN suggests a shift in community diversity, possibly indicating Al toxicity on these surfaces. When Fe is present in the silicate, however, this trend is reversed and abundant colonization of the surface is observed. Here, microorganisms preferentially colonize those silicate surfaces that offer beneficial nutrients and avoid those that contain potentially toxic elements.

Introduction

The subsurface microbial community can be grossly divided into two distinct but related populations: free-floating or planktonic microorganisms usually assumed to be the smaller fraction, and attached or sessile organisms, which are the more populous fraction in most aquifers (Hazen et al., 1991). Each habitat offers distinct advantages and disadvantages to a population, and there is a rich literature on the mechanisms and tactics for microbial attachment to mineral surfaces (e.g., Fletcher and Murphy, 2001), and the transport of pathogenic microorganisms in soils and aquifers (Harvey and Harms, 2001, Harvey and Harms, 2002). Microbial attachment and growth can influence flow through small pore spaces, and may alter the nature of the mineral surface or change mineral water reaction equilibria. Microbial attachment to mineral surfaces is a selection mechanism for the microbial community, a component of the porewater geochemistry and can even influence the hydraulic character of the aquifer. The basis for microbial attachment and subsequent colonization of mineral surfaces, therefore, is integral to understanding the biogeochemistry of groundwater habitats.

Models of microbial attachment to and growth on mineral surfaces in aquifers assumes that the initial cell attachment is a passive or random interaction. Often cells are approximated as charged colloids and mineral surfaces as uniform charged surfaces with the primary interaction by passive filtration and columbic attraction (e.g., van Loosdrecht et al., 1989). Most importantly, minerals are treated as surfaces with only the property of charge actively influencing microbial attraction, while passive properties such as hydration forces, hydrophobic or steric interactions, and polymer bridging all influence microbial attachment to some degree but are difficult to separate and quantify (Elimelech et al., 1995). Currently, there are several models used to describe microbial attachment to mineral surfaces, including Derjaguin–Ladau–Verwey–Overbeek (DLVO), extended DLVO (Hermansson, 1999) and surface complexation models (SCM; Fein et al., 1997, Fowle and Fein, 1999, Martinez and Ferris, 2001, Yee et al., 2004). These models are particularly useful in modeling short-term laboratory experiments, as well as microbial transport in porous media where cell attraction and initial attachment occurs over short time periods. Surface complexation models, for example, describe the reactivity of the microbial cell wall by employing acid–base titrations that are used to quantify and assign surface functional groups (e.g., carboxyl, phosphoryl, amino). Equilibrium constants for the deprotonation of these functional groups (pKa) can then be utilized to model the microbial electric field under specific solution pH and ionic strength conditions. Though often dilute, most groundwaters still contain common major cations (Ca2+, Mg2+, K+, etc.) and therefore both microbial and mineral surface functional groups are likely complexed, potentially leading to a reduction in the electrostatic repulsion between negatively charged bacteria and silicate surfaces such as feldspars, at near-neutral pH (Fowle et al., 2004, Yee et al., 2004).

Significant changes in attachment behavior have been documented as a function of solution pH and ionic strength. Although these parameters have been shown as primary controls on initial surface attachment (Kinoshita et al., 1993, Yee et al., 2000), changes in other matrix properties have profound effects. In particular, the concentration and flux of nutrient and carbon sources has been shown to impact microbial attachment in laboratory settings (Bonet et al., 1993, Knox et al., 1985, McEldowney and Fletcher, 1986, Molin et al., 1982). Field observations suggest that the number of planktonic organisms increases within plumes of carbon contamination (Godsy et al., 1992, Harvey et al., 1984), and Murphy and Ginn (1996) found that initially attached organisms detached to the aqueous phase under non-nutrient-limited conditions, but reattached as one or more nutrients became limiting. Attachment may serve as a means to avoid predation by grazers (protazoan; Harvey, 1997) or may benefit microorganisms because nutrient availability may be greater due to surface-associated organic matter (Davis and McFeters, 1988, Lechevallier and McFeters, 1990, Mueller, 1996) and nutrients. Recent studies have demonstrated that some dissimilatory iron-reducing bacteria use specialized flagella to detect and attach to iron oxide minerals (Caccavo and Das, 2002, Childers et al., 2002, Lower et al., 2001). This type of chemotactic behavior may account for differential colonization of mineral surfaces with similar surface charge but different compositions and may play a role in establishing surface-associated microbial communities.

Over longer time periods, however, other factors must be considered and colonization by microorganisms rather than reversible attachment or detachment may occur. Growth of individual cells on a mineral surface may result in the formation of complex interdependent microbial communities, where the cells in contact with the solution are not in contact with the mineral surface, and the surface charge is immaterial to individual cells comprising the layered biofilm. Mineral surfaces can become fouled with exopolysaccarides (EPS) or other organic polymers changing the surface charge, while exoenzymes may sorb to exposed mineral surfaces. Minerals can dissolve or precipitate due to the presence of viable microorganisms, resulting in a complex and reactive chemical environment around the attached cell that may interfere or potentially enhance basic cell functions associated with metabolism and growth. The longer a cell is attached, the greater the opportunity to directly interact with the mineral surface, and the nature of that interaction will become increasingly important to the success of that population on that habitat (i.e. mineral surface).

The research presented here examines microbial colonization (a steady-state observation of the sum of attachment, detachment, growth and death of surface adherent microbes) of silicate mineral, oxide phases, and glass surfaces in nature over relatively long time periods (months) as a function of both surface charge and detailed composition. The role of silicate-bound metals and nutrients on microbial colonization was investigated and these results were compared to pure silica and simple glass surfaces using both specific coulombic attraction models and broader compositional influences. Microbial colonization on mineral surfaces, as opposed to initial microbial attachment, is strongly influenced by the composition of the mineral, with both negative and positive influences offered by silicate bound metals and nutrients. A compositional model of microbial colonization suggests that all mineral surfaces are not created equally, and a more complete understanding of microbial–mineral surface association requires more than a description of surface charge.

Section snippets

Methods

The influence of basic silicate composition on microbial colonization was examined using a variety of iron (Fe)- and aluminum (Al)-bearing minerals and glasses in field colonization experiments. Fe and Al were chosen because both metals have similar electron valence and charge and occur naturally in silicate minerals with silica and charge balancing cations. Microorganisms use Fe as a micronutrient, and in anaerobic systems, as a terminal electron acceptor while Al is known to be inhibitory to

Surface colonization of silicate minerals and glasses

Minerals and glasses were placed into the native groundwater using in situ microcosms and left undisturbed to interact with groundwater, colloids and planktonic organisms for periods up to 1 year. All of the minerals and glasses examined had varying degrees of colonization by microorganisms. The extent of colonization and diversity of organisms differed not only with the composition of the solid phase but also its surface properties.

Previous results of similar experiments using other silicate

Discussion

In this study, the influence of major-element composition of silicate minerals on microbial colonization was investigated using silicate minerals and glasses containing these metals. It is proposed here that both mineral surface charge and mineral composition influence microbial colonization. Our results suggest, however, that these two controls dominate attachment and subsequent colonization under different conditions. When the mineral surface is uniformly positively charged, negatively

Summary and conclusions

This study demonstrates two modes of microbial colonization of minerals in circum-neutral pH, anaerobic groundwater. Fig. 8 is a schematic summarizing these findings. On mineral surfaces such as the iron and aluminum oxides investigated in this study, we observe a largely passive interaction dominated by electrostatic interactions between the positively charged mineral surfaces and negatively charged microorganisms shown as the shaded area left of the line in Fig. 8. In contrast, on silicate

Acknowledgments

The author gratefully acknowledges the assistance and contributions of P. Bennett, G. Delin, D. Siegel, P. Glaser, and F. Hiebert. The author would also like to thank the editors of this volume as well as two anonymous reviewers, A. Engel, and D. Fowle for their thoughtful reviews. This research was supported by the NSF (EAR-0230204), ACS-PRF (38868-G2), the USGS Toxic Hydrology Program and the Geology Associates of the University of Kansas. [LW]

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