Growth kinetic and transport of mixed microbial cultures in subsurface environments

Highlights

• Monod equation may fail to estimate microbial community kinetics.

• Microbial community kinetics can be expressed by an equivalent strain.

• Proposed a procedure to calibrate the equivalent strain.

• Equivalent strain can characterize microbial community in reactive transport.

• Equivalent strain efficiency depends on substrate availability.

Abstract

Subsurface porous environments harbor various microbial communities that control ecosystem functions such as geochemical cycling, bioremediation and ore formation. To simulate bioprocesses derived by microbial communities, Monod equation and cardinal models are utilized to model growth kinetics dependency on substrate concentration and temperature, respectively. In this work, we illustrate that Monod equation with constant parameters cannot characterize community derived microbial processes. Additionally, the growth-temperature dependency of a community of microorganisms does not follow a specific mathematical model. We suggest an equivalent strain model that can estimate the rate of community-derived metabolisms (RCDM) in non-isothermal reactive transport processes. We consider a one-dimensional flow system with four different simulation scenarios of immobile biomass-limited electron donor, mobile biomass-limited electron donor, immobile biomass-unlimited electron donor and mobile biomass-unlimited electron donor. We illustrate that the equivalent strain can efficiently characterize (with absolute normalized deviation (AND)<4%) the behavior of the test community when electron donor availability is limited. In contrast to the limited electron donor availability cases, we show that the equivalent strain is not capable of characterizing the test community when electron donor is abundant, leading to a maximum AND of 70%. The deviation of the equivalent strain from the test community is due to the inability of the equivalent strain to represent the effects of community evolution on RCDM and biomass deactivation that happens due to temperature variations.

Introduction

Almost all underground environments experience numerous reactive processes that are influenced by microbial activities. Soils, deep geothermal aquifers, marine sediments and petroleum reservoirs are some examples of such environments. Microbially-derived processes, for example, control ground water quality, or the concentrations of toxins in soils by breaking down harmful materials to nontoxic compounds. In hydrocarbon reservoirs, microorganisms can act as friends and foes. While microorganisms can increase oil recovery through a process called microbial enhanced oil recovery (Ke et al., 2018; Veshareh and Ayatollahi, 2020; Veshareh et al., 2018), they can cause environmental and economical damage by producing the toxic, corrosive H₂S gas through the reservoir souring process (Hubert et al., 2003; Prajapat et al., 2018). These are a few reasons why understanding the dynamics of microbial processes is crucial.

Underground environments harbor a vast range of microorganisms in great abundance. Torsvik and Øvreås (2002) estimated that one gram of soil hosts about 10 billion microorganisms from numerous type of species. However, since biochemical pathways are finite, many microorganisms contribute and compete in a common process. Even though a group of microorganisms may derive the same metabolism, their activity at a given environmental condition (temperature, substrate concentration, etc.) can be significantly different. Isolation of major contributing microorganisms in a community and studying their kinetic dependency is, however, time consuming and economically expensive. A single Monod equation has been able to fit experimental data obtained from batch processes governed by multiple strains such as anaerobic treatment of domestic and industrial wastewaters (Donoso-Bravo and Fdz-Polanco, 2010; Sosnowski et al., 2008; Sötemann et al., 2005). In many studies, the Monod equation (with parameters obtained by fitting batch experiments) has been used to simulate reactive transport processes (Cheng et al., 2016; Haghshenas et al., 2012; Veshareh et al., 2020; Veshareh and Nick, 2019). Stolpovsky (2012) illustrated that two Monod equations are required for accurate modeling of isothermal reactive flow and transport in porous media representing biodegradation derived by 100 strains. He showed that the Monod equation parameters for the two equations are equal to the minimum and maximum of Monod parameters of the 100 strains. For sulfate-reduction metabolism derived by 25 sulfate-reducing microorganisms, in a non-isothermal flow system, Cheng et al. (2018) found that considering one Monod equation underestimates the metabolism rate and at least 9 Monod equations have to be considered. Monod equation parameters of the 9 strains was obtained by dividing the original 25 strains into three groups of mesophiles, thermophiles and hyperthermophiles and then choosing three key microorganisms in each regime.

Temperature is one of the main environmental factors that influences microbial growth. In subsurface environments, temperature can be highly heterogeneous in space and time. For example, in the processes of cooled geothermal fluid or seawater injection into a geothermal or an oil reservoir, respectively, locations close to injection wells are cooled down, while zones close to production wells are warmer (Willems and Nick, 2019; Ziabakhsh-Ganji et al., 2018). Temperature effect on growth has been investigated by many researchers due to its significance in fundamental research (e.g., taxonomy, microbial metabolism) and in applied research (e.g., control of bioprocesses in safe handling of goods, agriculture and food industries). As a result, many mathematical models have been developed to express microbial growth dependency on temperature (Esener et al., 1981; Hinshelwood, 1946; Mohr and Krawiec, 1980; Ratkowsky et al., 1983; Schoolfield et al., 1981). Among these models, the model introduced by Rosso et al. (1995) has been used in non-isothermal bioreactive transport simulations (Cheng et al., 2018; Hosseininoosheri et al., 2017). It is important to note that these models have been developed for a single microorganism. Thus, it is not clear if such models can express the temperature dependency of a community of microorganisms in a reactive transport model.

Here, we aim to answer the following main questions:

• For an isothermal system, can a single Monod equation with constant parameters predict the rate of a community-derived metabolism (RCDM)?

• Can a distinct mathematical model, developed for growth-temperature dependency of a single strain, characterize the temperature dependency of a community of microorganisms?

• Can an equivalent strain characterize RCDM? What is the error associated with employing such an equivalent strain?

To this aim, we first undertake a theoretical approach by writing a mathematical model that represents a community derived metabolism rate and then reformulating it to the Monod kinetic equation form. From this reformulation we illustrate whether a single Monod equation and a single temperature model with constant model parameters as explained in Burger et al. (2005) and Rosso et al. (1995) can reflect RCDM. Furthermore, we suggest an equivalent strain characterized by a Monod equation with variable parameters to estimate RCDM. A guideline is proposed to measure the equivalent strains kinetic parameters using batch experiments. Next, we use a community of 25 sulfate-reducing microorganisms introduced by Cheng et al. (2018) to corroborate what we conclude using the theoretical approach. Additionally, we evaluate whether or not the proposed equivalent strain model can characterize RCDM. We then describe the conditions under which our proposed equivalent strain model for a given reactive transport problem is applicable.