Elsevier

Journal of Hydrology

Volume 558, March 2018, Pages 72-89
Journal of Hydrology

Research papers
Preferential flow in the vadose zone and interface dynamics: Impact of microbial exudates

https://doi.org/10.1016/j.jhydrol.2017.12.065Get rights and content

Highlights

  • Microbial exudates exert a significant effect on the wettability of fluids.

  • Catechol solutions reduce contact angle while riboflavin solutions increase it.

  • Microbial exudates impact wetting front instability and fingered flow.

  • Increase in microbial exudate concentrations increases water saturation at fingertip.

  • Light transmission method allows visualization of preferential flow in porous media.

Abstract

In the hydrological cycle, the infiltration process is a critical component in the distribution of water into the soil and in the groundwater system. The nonlinear dynamics of the soil infiltration process yield preferential flow which affects the water distribution in soil. Preferential flow is influenced by the interactions between water, soil, plants, and microorganisms. Although the relationship among the plant roots, their rhizodeposits and water transport in soil has been the subject of extensive study, the effect of microbial exudates has been studied in only a few cases. Here the authors investigated the influence of two artificial microbial exudates–catechol and riboflavin–on the infiltration process, particularly unstable fingered flow, one form of preferential flow. Flow experiments investigating the effects of types and concentrations of microbial exudates on unstable fingered flow were conducted in a two-dimensional tank that was filled with ASTM C778 graded silica sand. The light transmission method (LTM) which is based on capturing the light intensity transmitted through a sand-water system and then converting it into degree of water saturation was used to visualize and characterize the flow of water in porous media as well as to image and measure the spatial and temporal distribution of water in porous media. Flow patterns, vertical and horizontal profiles of the degree of water saturation of the fingers, as well as measurements of the fingers dimension (width), number, and velocity were determined using the light transmission method. Interfacial experiments exploring the influence of microbial exudates on the wettability behavior of water were performed by measuring the contact angle and the interfacial tension of the (solid)-gas-microbial exudate solution systems. Unstable wetting front generating fingered flow was observed in all infiltration experiments. The experimental results showed that the microbial exudate addition affected the infiltration process, as the measurements of the degree of saturation profiles and widths of the fingers differed from those of the control NaCl solution. These differences may be due to an improved water holding capacity in the presence of the microbial exudates. The lowest catechol solution concentration (10 μM) produced the largest finger width (9.69 cm) among the tested catechol solution concentrations and all the other solutions including the control solution (7.24 cm). Moreover, the wettability of the medium for the catechol solution increased with an increase in concentration. The highest riboflavin solution concentration (1000 μM) generated the highest finger width (7.75 cm) among the tested riboflavin solution concentrations. However, the wettability of the medium for the riboflavin solution decreased with an increase in concentration. Our study demonstrated that the microbial exudates which are biochemical compounds produced and released by microbes in the environment are capable of influencing the soil infiltration process. The results of this study also demonstrated that the influence of the contact angle expressed as (cosθ)1/2 should be integrated in the scaling of the finger dimension, i.e., finger width, when the Miller and Miller (1956) scaling theory is applied for the hydrodynamic scaling in porous media.

Introduction

The infiltration process is an extremely important factor within the hydrological cycle as it filters water from both the atmosphere and the ground surface into the soil, which in turn revives the underground ecosystem through a recharged ground water table to ensure the continuity of the cycle. A combination of gravity and capillarity forces acts upon the water and upon entry into the soil pores with gravity always acting vertically and with the capillary forces channeling the water in all directions (Gray and Norum, 1967). Derived in 1931 by Lorenzo A. Richards, the Richards equation is used to determine water flow in the vadose zone under constant temperature from Darcy’s law and the conservation of mass. It is expressed as:θt=ZK(θ)dψ(θ)dθθz-K(θ)z=zD(θ)θz-K(θ)zwhere θ represents the volumetric water content in soil, t the time, z the vertical axis pointing downward indicating positive, K the soil hydraulic conductivity, Ψ the soil water potential, and D the soil water diffusivity. This highly nonlinear problem makes analytical and numerical solutions to the Richards equation typically non-unique (Celia et al., 1990). The theory of infiltration and solutions to elucidate the question of flow in porous media have been the focus of extensive research, most particularly through the seminal work of Jean-Yves Parlange (Parlange, 1973, Parlange, 1975, Parlange and Aylor, 1972, Parlange, 1971a, Parlange, 1971b, Parlange, 1971c, Parlange, 1972a, Parlange, 1972b, Parlange, 1972c, Parlange, 1972d, Parlange, J.Y.,1972e). Analytical and quasi-analytical solutions of the equation of flow in porous media have been formulated through time expansion (Philip, 1969, Philip, 1975a, Philip, 1975b), integral approaches (Parlange, 1971b, Parlange, J.Y.,1972e) and the nonmonotonic traveling wave (DiCarlo et al., 2008). Many simplifications and approximations to the Richards equation have been proposed (e.g. Bras, 1990, Smith et al., 1993, Waechter and Philip, 1985).

Water flow during the infiltration process in soil systems is either uniform, with wetting fronts flowing in parallel to the soil surface level; or non-uniform, with wetting fronts flowing irregularly (Green and Ampt, 1911). In a non-uniform flow, water movement in some areas of the unsaturated subsurface is faster and more intense than in others. Preferential flow in the form of macropore flow, unstable fingered flow, and funnel flow are a few of the characteristic non-uniform flows that may occur. Preferential flow refers to the movement of water in addition to the solutes in a non-uniform flow and is independent from common conditions that characterize soils in various locations (Andreini and Steenhuis, 1990, Baveye et al., 1998, Dekker and Ritsema, 1996, Doerr et al., 2007, Doerr et al., 2006). The occurrence of finger flows, one form of preferential flow that frequently occurs in homogeneous porous media, may appear due to (i) entrapment of air during the movement of the wetting front, (ii) flow through water-repellent soils, (iii) the process of continuous non-ponding infiltration, and (iv) flow through layered materials having different textures (Baker and Hillel, 1990, Diment and Watson, 1985, Du et al., 2001, Glass et al., 1991, Glass et al., 1990, Glass et al., 1989a, Glass et al., 1989b, Glass et al., 1989c, Hill and Parlange, 1972, Hillel and Baker, 1988, Parlange and Hill, 1976, Philip, 1975a, Philip, 1975b, Raats, 1973, Selker et al., 1992, Tamai et al., 1987, Yao and Hendrickx, 1996, Yao and Hendrickx, 2001). Surface tension and contact angle are the two interfacial parameters most commonly examined in the infiltration process (Yuan and Lee, 2013). Additional details on wetting front instability and gravity-driven flow in porous media can be obtained in extensive reviews (Assouline, 2013, Glass and Nicholl, 1996, De Rooij, 2000, DiCarlo, 2013, Xiong, 2014).

The formation of preferential flow may be influenced either directly or indirectly from various biological factors. Although plant root zones induce water into the soil, microorganisms and their secreted compounds can change hydraulic conductivity by modifying soil porosity and inducing water repellency, which then forms preferential flow paths (Morales et al., 2010). These preferential flow paths of a soil profile can then form a saturated distribution zone with fingering flow paths (Kim et al., 2005, Steenhuis et al., 1994). These unstable wetting fronts then split the original horizontal profiles into fingering flow paths that may cause a leaching of contaminants via the soil into the groundwater (Bauters et al., 2000, Darnault et al., 2003, Darnault et al., 2004, Doerr et al., 2007, Hendrickx and Flury, 2001, Uyusur et al., 2010, Uyusur et al., 2015, Wang et al., 2000). In addition, unexpected dry and wet soil patches from fingering flow paths can negatively affect microbial populations and plant growth (Morales et al., 2010). For example, the agrochemicals and wetting agents (surfactants) regularly applied to golf course greens can rapidly move through the subsurface by preferential flow (Kostka, 2000, Morales et al., 2010).

Soil moisture is an integral component concerning the support of biogeochemical processes as nutrient cycles, and a catalyst for microbial and plant activities (Wang et al., 2015). Soil modification by microorganisms and plant roots creates preferential flow, which in turn facilitates the microbial and plant activity by supplying more oxygen, moisture content, available nutrients, and different dissolved substrates along the wetted flow path. The soil-water dynamics are complex due to the heterogeneity in soil media from the nonuniform spatial distribution of microorganisms and plant roots, different soil structures, numerous interrelated biogeochemical reactions, spatial and temporal variability, and the scaling factor for hydrological processes (Ettema and Wardle, 2002, Morales et al., 2010).

Microorganisms growing in the soil tend to accumulate low molecular weight organic molecules, also known as osmolytes. The semi-permeability of membranes of these microorganisms causes a release of the intracellular solutes as exudates, which in turn preserve their osmotic potential with the surrounding medium. Although the exudate production varies among microorganisms, this microbial response is a useful strategy to prevent cell lysis and death caused by changes in soil water content (Boot et al., 2013, Griffin, 1981, Halverson et al., 2000, Kieft et al., 1987, Potts, 1994, Wang et al., 2015). It has been determined that plant exudates released by roots can function as surfactants and change surface tension of soil solutions, which in turn alters the hydraulic conductivity and water flow around the rhizosphere (Passioura, 1988, Read et al., 2003, Read and Gregory, 1997). As surface-active organic compounds, surfactants can alter both surface tension of liquids and contact angle at the solid-liquid interface, which can further influence both the water flow and the potential transport of contaminants in the vadose zone (Bashir et al., 2008, Karagunduz et al., 2015). However, little research has been undertaken to examine the influence of different microbial exudates on water infiltration processes into the vadose zone. Catechol is one compound produced by certain bacteria (e.g., Escherichia coli) that can be synthesized by feeding those microbes on glucose and as intermediates during the biodegradation processes of aromatic compounds (e.g., phenol) (Draths and Frost, 1995, Li et al., 2005, Nair et al., 2008). Riboflavin (or vitamin B2), which is naturally produced by many microorganisms, including Candida famata, Bacillus subtilis, and lactic acid bacteria, is a second compound that can be treated as a microbial exudate (Bacher et al., 2001, Perkins et al., 1999, Perkins and Pero, 1993, Schallmey et al., 2004, Stahmann et al., 2000, Thakur et al., 2016).

First used by Hoa in 1981 to measure water content in two-dimensional unsaturated sandy porous media, the Light Transmission Method (LTM) is ideal for studying the infiltration process without disturbing the porous media system. This non-invasive imaging technique is inexpensive and fast responding, and provides high resolution with a mininum of acquisition time (Darnault et al., 1998, Werth et al., 2010). In order to acquire available data, a transparent (thin enough to be two dimensional) system that enables visible light to transmit through is needed. A charge-coupled device (CCD) camera is commonly used for data capture in the light transmission method, as the resolution is acceptable (Werth et al., 2010). The light intensity data separated from the original RGB image can be converted to the percentage of water saturation based on the calibration equation. As a result, profiles of water distribution of wetting front and fingered flow during the infiltration process can be obtained and then analyzed for flow characteristics.

Very little study has been undertaken to examine the infiltration process in porous media using the light transmission method, and even less to elucidate the influence of microbial exudate on the flow process. Although plant exudates act as surfactants to influence water flow, the effect of microbial exudates upon the infiltration process is unknown. Therefore, a random rain event, rather than point source, was simulated to mimic natural conditions, and to use the light transmission method to investigate the effect of these microbial exudates on preferential flow with different concentrations which relate to different concentrations of biomass when applying real microbes.

The primary objective of this research entailed an investigation of how different microbial exudates with varying concentrations alter the infiltration process in an unsaturated sand system and the distribution of the soil moisture content. Specifically, the microbial exudates catechol and riboflavin were examined to determine any influence on flow in porous media. The surface tension and the contact angle were dynamically monitored to obtain the interfacial properties of exudate solutions, and the infiltration experiments were conducted in a homogeneous and initially dry porous media in a two-dimensional (2D) tank. A light transmission method with high spatial and temporal resolution was used to construct the flow patterns and to visualize the water saturation distribution followed by the use of MATLAB to process the imaging and data analyses.

Section snippets

Microbial exudates solution preparation

Two solutions of microbial exudate were simulated using catechol and riboflavin, the molar concentrations of which were 10, 100, 500, and 1000 μM, respectively. For the catechol (≥99.5%, Sigma-Aldrich, St. Louis, MO) solution, 1.10, 11.01, 55.05, and 110.10 mg of catechol powder were mixed with 0.01 M of BDH ACS Grade NaCl (VWR International, Radnor, PA) solution. For the riboflavin (≥98%, Sigma-Aldrich, St. Louis, MO) solution, 3.76, 37.64, 188.18, and 376.36 mg of riboflavin powder were mixed

Catechol

The contact angles for the catechol solutions are shown in Fig. 3. The lowest concentration of 10 μM catechol solution with 0.01 M NaCl exhibited the highest contact angle among the four concentrations. An increase in the catechol concentration from 10 μM to 1000 μM reduced the contact angle from 75 ± 2.82° to 69 ± 3.52° at time 0 min successively. At approximately 10 min, all contact angles decreased and slowly plateaued. The initial contact angle of 76.7 ± 1.61° in the 0.01 M NaCl control

Discussion

Microbial exudate, as the first step in the simulation of a microbial effect, does affect the infiltration process, particularly preferential flow through porous media. In this research, catechol and riboflavin in particular were studied, as were the interfacial characteristics of contact angle and surface tension which played an important role in the analysis of the fingering flow process.

The study of interfacial characteristics of catechol and riboflavin provided the basic information for

Conclusion

The important findings of this 2D tank microbial exudate flow study are summarized below:

  • The light transmission method is a unique tool allowing the investigation of the synergistic influence of solution chemistry and porous media characteristics on the infiltration process, including the unstable fingered flow phenomenon, with a high spatial and temporal resolution.

  • Microbial exudates affected the preferential flow during the infiltration process by forming two zones in the vertical water

Acknowledgments

This material is based upon work supported by the U.S. Department of Energy Office of Science, Office of Basic Energy Sciences and Office of Biological and Environmental Research under Award Number DE-SC-00012530. The authors thank Peter Kitanidis, Editor-in-Chief of Journal of Hydrology; Jirka Simunek, Associate Editor of Journal of Hydrology; and the two reviewers for their useful comments. The authors are especially grateful to Tammo Steenhuis for his very valuable insights. We also wish to

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