Responses of soil bacterial and fungal communities to extreme desiccation and rewetting

Abstract

The microbial response to summer desiccation reflects adaptation strategies, setting the stage for a large rainfall-induced soil CO2 pulse upon rewetting, an important component of the ecosystem carbon budget. In three California annual grasslands, the present (DNA-based) and potentially active (RNA-based) soil bacterial and fungal communities were tracked over a summer season and in response to controlled rewetting of intact soil cores. Phylogenetic marker genes for bacterial (16S) and fungal (28S) RNA and DNA were sequenced, and the abundances of these genes and transcripts were measured. Although bacterial community composition differed among sites, all sites shared a similar response pattern of the present and potentially active bacterial community to dry-down and wet-up. In contrast, the fungal community was not detectably different among sites, and was largely unaffected by dry-down, showing marked resistance to dessication. The potentially active bacterial community changed significantly as summer dry-down progressed, then returned to pre-dry-down composition within several hours of rewetting, displaying spectacular resilience. Upon rewetting, transcript copies of bacterial rpoB genes increased consistently, reflecting rapid activity resumption. Acidobacteria and Actinobacteria were the most abundant phyla present and potentially active, and showed the largest changes in relative abundance. The relative increase (Actinobacteria) and decrease (Acidobacteria) with dry-down, and the reverse responses to rewetting reflected a differential response, which was conserved at the phylum level and consistent across sites. These contrasting desiccation-related bacterial life-strategies suggest that predicted changes in precipitation patterns may affect soil nutrient and carbon cycling by differentially impacting activity patterns of microbial communities.

Figure 1

Dynamics of water conditions at the Hopland (dots), Sierra (dashes) and Sedgwick (full) experimental sites: cumulative precipitation from September 2009 to September 2010 (a), dynamics of soil water content (b) and potential (c) throughout summer dry-down and controlled wet-up. T0, T1 and T2 indicate field sampling dates, bars indicate ±1s.e. (n=5). Precipitation data source: California Irrigation Management Information System and University of California Santa Barbara Geography Department.

Figure 2

Principal coordinates analysis (PCoA) of the UniFrac pairwise dissimilarity of the relative abundance of bacterial and fungal pyrotag sequences based on 16S rRNA gene (a) and 16S rRNA (b) for bacteria and on 28S rRNA gene (c) and 28S rRNA (d) for fungi, over dry-down and wet-up in the experimental sites (Hopland: black, Sierra: blue, Sedgwick: red). The numbers indicate sampling dates over dry-down, W indicates data acquired 2 h after the end of wet-up.

Figure 3

Dynamics of the 16S rRNA gene-based relative abundance of the main present bacterial groups at the phylum (a) and class (b) levels, sequenced during dry-down and wet-up (grey area, note the difference in x-axis scale) over the three experimental sites. Bars indicate ±1s.e. (n=9).

Figure 4

Dynamics of the 16S rRNA-based relative abundance of the main potentially active bacterial groups at the phylum (a) and class (b) levels, sequenced during dry-down and wet-up (grey area, note the difference in x-axis scale) over the three experimental sites. Bars indicate ±1s.e. (n=9). In the wet-up analysis, Acidobacteriales, Acidobacteria subdiv. 4 and Acidobacteria other subdiv. were grouped into one class due to missing values. The dry-down analysis did not include Acidobacteriales, Acidobacteria other subdiv., Planctomycetacia or Spartobacteria, which were below the abundance threshold.

Figure 5

Dynamics of the 28S rRNA gene-based relative abundance of the main present fungal groups at the phylum (a) and class (b) levels, sequenced during dry-down and wet-up (grey area, note the difference in x-axis scale) over the three experimental sites. Bars indicate ±1s.e. (n=9).

Figure 6

Dynamics of the 28S rRNA-based relative abundance of main potentially active fungal groups at the phylum (a) and class (b) levels, sequenced during dry-down and wet-up (grey area, note the difference in x-axis scale) over the three experimental sites. Bars indicate ±1s.e. (n=9). The dry-down analysis did not include Leotiomycetes or Sordariomycetes, which were below the abundance threshold.

Figure 7

Abundance of selected genes over dry-down (left panels) and RNA transcripts over wet-up (right panels) for the experimental sites (Hopland: dots, Sierra: dashes, Sedgwick: full), obtained by qPCR. Bars indicate ±1s.e. (n=3).