Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer

Abstract

Viruses are the most abundant biological entity on Earth and their interactions with microbial communities are recognized to influence microbial ecology and impact biogeochemical cycling in various ecosystems. While the factors that control the distribution of viruses in surface aquatic environments are well-characterized, the abundance and distribution of continental subsurface viruses with respect to microbial abundance and biogeochemical parameters have not yet been established. In order to begin to understand the factors governing virus distribution in subsurface environments, we assessed microbial cell and virus abundance in groundwater concurrent with groundwater chemistry in a uranium impacted alluvial aquifer adjoining the Colorado River near Rifle, CO. Virus abundance ranged from 8.0 × 10⁴ to 1.0 × 10⁶ mL^-1 and exceeded cell abundance in all samples (cell abundance ranged from 5.8 × 10⁴ to 6.1 × 10⁵ mL^-1). The virus to microbial cell ratio ranged from 1.1 to 8.1 and averaged 3.0 ± 1.6 with virus abundance most strongly correlated to cell abundance (Spearman's ρ = 0.73, p < 0.001). Both viruses and cells were positively correlated to dissolved organic carbon (DOC) with cells having a slightly stronger correlation (Spearman's ρ = 0.46, p < 0.05 and ρ = 0.54, p < 0.05; respectively). Groundwater uranium was also strongly correlated with DOC and virus and cell abundance (Spearman's ρ = 0.62, p < 0.05; ρ = 0.46, p < 0.05; and ρ = 0.50, p < 0.05; respectively). Together the data indicate that microbial cell and virus abundance are correlated to the geochemical conditions in the aquifer. As such local geochemical conditions likely control microbial host cell abundance which in turn controls viral abundance. Given the potential impacts of viral-mediated cell lysis such as liberation of labile organic matter from lysed cells and changes in microbial community structure, viral interactions with the microbiota should be considered in an effort to understand subsurface biogeochemical cycling and contaminant mobility.

Keywords: aquifer; bacteriophage; dissolved organic carbon; groundwater; subsurface; uranium; virus.

Figure 1

Location of monitoring wells within a uranium contaminated alluvial aquifer located 0.3 miles east of Rifle, Colorado (USA) and adjoining the Colorado River (Well 309 39.52842, −107.774426 and Well SY07 39.529335, −107.770864). Monitoring wells located inside the contaminant plume are denoted with red stars whereas monitoring wells located outside of the contaminant plume are denoted as black boxes. Groundwater virus abundance (A), cell abundance (B), and virus-to-microbial cell ratio (VMR) (C) data collected from monitoring wells across the alluvial aquifer. Error bars denoted standard error of measure for duplicate samples. Spatial interpolation of groundwater viruses (D), cells (E), and virus-to-microbial cell ratio (F) data collected from monitoring wells in the alluvial aquifer depicting spatial distribution. Color gradient from high (red) to low (blue) denotes interpolated values.

Figure 2

Spearman's rank correlations between DOC and abundances of cells (A) and viruses (B). Spearman's rank correlation between viruses and cells (C) in groundwater samples. Error bars represent the standard deviation of the mean of duplicate measurements. Error bars not visible are smaller than the symbol. Dashed lines represent the 95% confidence interval for the lines of regression presented in the figure.

Figure 3

Spatial interpolation of groundwater DOC (A), uranium (B), nitrate (C), sulfate (D), and DIC (E) data collected from monitoring wells in the alluvial aquifer depicting spatial distribution. Color gradient from high (red) to low (blue) denotes interpolated concentrations.