Spatial and resource factors influencing high microbial diversity in soil

Abstract

To begin defining the key determinants that drive microbial community structure in soil, we examined 29 soil samples from four geographically distinct locations taken from the surface, vadose zone, and saturated subsurface using a small-subunit rRNA-based cloning approach. While microbial communities in low-carbon, saturated, subsurface soils showed dominance, microbial communities in low-carbon surface soils showed remarkably uniform distributions, and all species were equally abundant. Two diversity indices, the reciprocal of Simpson's index (1/D) and the log series index, effectively distinguished between the dominant and uniform diversity patterns. For example, the uniform profiles characteristic of the surface communities had diversity index values that were 2 to 3 orders of magnitude greater than those for the high-dominance, saturated, subsurface communities. In a site richer in organic carbon, microbial communities consistently exhibited the uniform distribution pattern regardless of soil water content and depth. The uniform distribution implies that competition does not shape the structure of these microbial communities. Theoretical studies based on mathematical modeling suggested that spatial isolation could limit competition in surface soils, thereby supporting the high diversity and a uniform community structure. Carbon resource heterogeneity may explain the uniform diversity patterns observed in the high-carbon samples even in the saturated zone. Very high levels of chromium contamination (e.g., >20%) in the high-organic-matter soils did not greatly reduce the diversity. Understanding mechanisms that may control community structure, such as spatial isolation, has important implications for preservation of biodiversity, management of microbial communities for bioremediation, biocontrol of root diseases, and improved soil fertility.

FIG. 1.

Representative microbial community diversity patterns based on OTU abundance in surface, vadose, and saturated soils from low- and high-carbon sites. The values in boxes are community diversity values based on the reciprocal of Simpson’s index.

FIG. 2.

Plots of the reciprocal of Simpson’s index (1/D) versus the log series index for the microbial communities at different soil depths from low-carbon (A) and high-carbon (B) sites. The values in the box are index values that indicate dominance in community structure.

FIG. 3.

Comparison of microbial community diversity (based on Simpson’s index) and chromium levels at the high-carbon Cannelton site.

FIG. 4.

Conceptual model of two soil particles showing the relationships between microbial biomass (M) and nutrient (R) exchanges. Although a small sample of soil would contain a large number of similar particle systems, this minimal representation suffices for our purposes. cR₁ and dR₂, nutrient fluxes between soil particles through water film, which also permits migration of microorganisms between particles (albeit slow); I, nutrient input from rainfall; eR₁ and eR₂ nutrient fluxes that become unavailable for microbial uptake, either because of gravitational loss or because of immobilization in compounds that the organisms cannot metabolize.

FIG. 5.

Effects of spatial isolation on population dynamics. (A) No spatial isolation with unequal uptake and loss coefficients. When I = 5, a₁ = 0.2, a₂ = b₁ = b₂ = d = e = 0.1, c = 0.2, K = 10, and R₁ = R₂ = 25, M₁ approaches 1.428 while M₂ remains 0.714 at equilibrium. Thus, two populations cannot be equally abundant, and hence noncompetitive patterns cannot be achieved. (B) Spatial isolation. The results are similar to those described above, except that when I = c = d = 0.0, M₁ = 0.129 and M₂ = 0.112 after 100 time intervals; that is, initially, M₁ has a slightly faster growth rate. However, M₁ = M₂ = 0.021 after 500 time intervals. The initial growth advantage of M₁ is temporary since it uses up its isolated supply of nutrients more rapidly. Thus, the sizes of the isolated populations become nearly identical, as seen in the noncompetitive pattern, even if the populations differ in terms of their growth dynamics.