Low pore connectivity increases bacterial diversity in soil

Abstract

One of soil microbiology's most intriguing puzzles is how so many different bacterial species can coexist in small volumes of soil when competition theory predicts that less competitive species should decline and eventually disappear. We provide evidence supporting the theory that low pore connectivity caused by low water potential (and therefore low water content) increases the diversity of a complex bacterial community in soil. We altered the pore connectivity of a soil by decreasing water potential and increasing the content of silt- and clay-sized particles. Two textures were created, without altering the chemical properties or mineral composition of the soil, by adding silt- and clay-sized particles of quartz to a quartz-based sandy soil at rates of 0% (sand) or 10% (silt+clay). Both textures were incubated at several water potentials, and the effect on the active bacterial communities was measured using terminal restriction fragment length polymorphism (TRFLP) of bacterial 16S rRNA. Bacterial richness and diversity increased as water potential decreased and soil became drier (P < 0.012), but they were not affected by texture (P > 0.553). Bacterial diversity increased at water potentials of <or=2.5 kPa in sand and <or=4.0 kPa in silt+clay, equivalent to <or=56% water-filled pore space (WFPS) in both textures. The bacterial community structure in soil was affected by both water potential and texture (P < 0.001) and was correlated with WFPS (sum of squared correlations [delta(2)] = 0.88, P < 0.001). These findings suggest that low pore connectivity is commonly experienced by soil bacteria under field conditions and that the theory of pore connectivity may provide a fundamental principle to explain the high diversity of bacteria in soil.

FIG. 1.

Fitted water release curves (a) and pore size distributions (b) for sand (▪ and black bars) and silt+clay (□ and white bars). Water release curves show the water-filled pore space at each water potential. Pore size distributions show the percentage of total pore volume occupied by each pore size class. At a given water potential, pores in the corresponding size class and all smaller pores contain water.

FIG. 2.

Back-scattered scanning electron micrographs demonstrating the variation in particle and pore size in sand (left) and silt+clay (right). Sand-sized quartz particles (sp) are visible in both treatments, while ground quartz particles (indicated with an asterisk) are only present within the resin (r)-infiltrated pore spaces in silt+clay. Scale bars = 100 μm.

FIG. 3.

Distance-based redundancy analysis (dbRDA) of bacterial communities incubated in either sand (black symbols) or silt+clay (gray symbols, separated by straight line) at the water potentials (cm) shown by the values. Circles surround data for bacterial communities that did not differ from each other (P > 0.05). The curved line separates data for bacterial communities incubated in wet and dry soils (water-filled pore space more than or less than 56%, respectively). All pairwise comparisons across the curved line were significantly different (P < 0.05), except for silt+clay at −1.5 and −5.5 kPa, which did not differ. The soil variables used to generate the dbRDA were water-filled pore space (% total pore volume), silt+clay content (% [wt/wt]), porosity (cm³ cm⁻³), largest water-filled pore, and the volume of water in pore size classes 68 to 77 μm, 77 to 88 μm, 88 to 102 μm, 102 to 122 μm, 122 to 153 μm, and 153 to 204 μm. The values in parentheses indicate the percentages of the fitted and total variations explained by each axis.