Dynamics of Microbial Growth and Coexistence on Variably Saturated Rough Surfaces

Abstract

The high degree of microbial diversity found in soils is attributed to the highly heterogeneous pore space and the dynamic aqueous microenvironments. Previous studies have shown that spatial and temporal variations in aqueous diffusion pathways play an important role in shaping microbial habitats and biological activity in unsaturated porous media. A new modeling framework was developed for the quantitative description of diffusion-dominated microbial interactions focusing on competitive growth of two microbial species inhabiting partially saturated rough surfaces. Surface heterogeneity was represented by patches with different porosities and water retention properties, yielding heterogeneous distribution of water contents that varies with changes in relative humidity or soil matric potential. Nutrient diffusion and microbial growth on the variably hydrated and heterogeneous surface was modeled using a hybrid method that combines a reaction diffusion method for nutrient field with individual based model for microbial growth and expansion. The model elucidated the effects of hydration dynamics and heterogeneity on nutrient fluxes and mobility affecting microbial population growth, expansion, and coexistence at the microscale. In contrast with single species dominance under wet conditions, results demonstrated prolonged coexistence of two competing species under drier conditions where nutrient diffusion and microbial movement were both limited. The uneven distribution of resources and diffusion pathways in heterogeneous surfaces highlighted the importance of position in the landscape for survival that may compensate for competitive disadvantages conferred by physiological traits. Increased motility was beneficial for expansion and survival. Temporal variations in hydration conditions resulted in fluctuations in microbial growth rate and population size. Population growth dynamics of the dominant species under wet–dry cycles were similar to growth under average value of diffusion coefficients for dry and wet conditions, respectively, suggesting that the time-averaged diffusion coefficient could serve as a useful indicator for estimation of microbial activities in a highly dynamic system such as that found in soils.

Appendix

List of symbols

C solute concentration

C0 a constant concentration

D local aqueous diffusion coefficient

D0 solute diffusion coefficient in aqueous phase

De effective diffusion coefficient

$\bar{D}_{\text{e}}$ temporally averaged diffusion coefficient

De,dry effective diffusion coefficient in the dry period

De,wet effective diffusion coefficient in the wet period

DS effective diffusion coefficient in the unsaturated rough surface

Ks half-saturation constant

m an empirical parameter in the van Genuchten model

N concentration of nutrient

n an empirical parameter in the van Genuchten model

R local consumption rate of nutrient

R* nutrient concentration at μ = 0

r cell motility

r radial distance

rm apparent maintenance rate at μ = 0

s substrate concentration

t variable of time

tdry duration of the dry period

twet duration of the wet period

V aqueous volume of the lattice grid

Vmax maximum specific substrate uptake rate

$\overline{{V_{\mu } }}$ median cell volume at μ = 0

v rate of substrate uptake

x cell dry mass of the individual cell

Ymax apparent yield at μmax, corrected for maintenance

α a parameter in the van Genuchten model

ΔM 1 amount of added nutrient at the boundaries to maintain constant concentration

ΔM 2 amount of removed nutrient at the center to maintain constant concentration

Θ effective water content in the van Genuchten model

θ volumetric water content

θr residual water content

θs volumetric water content at saturation

μ specific growth rate

μmax maximum specific growth rate

ρ cell density (based on dry mass)

Φ rough surface porosity

ψm matric potential