Warming Alters Expressions of Microbial Functional Genes Important to Ecosystem Functioning

Abstract

Soil microbial communities play critical roles in ecosystem functioning and are likely altered by climate warming. However, so far, little is known about effects of warming on microbial functional gene expressions. Here, we applied functional gene array (GeoChip 3.0) to analyze cDNA reversely transcribed from total RNA to assess expressed functional genes in active soil microbial communities after nine years of experimental warming in a tallgrass prairie. Our results showed that warming significantly altered the community wide gene expressions. Specifically, expressed genes for degrading more recalcitrant carbon were stimulated by warming, likely linked to the plant community shift toward more C4 species under warming and to decrease the long-term soil carbon stability. In addition, warming changed expressed genes in labile C degradation and N cycling in different directions (increase and decrease), possibly reflecting the dynamics of labile C and available N pools during sampling. However, the average abundances of expressed genes in phosphorus and sulfur cycling were all increased by warming, implying a stable trend of accelerated P and S processes which might be a mechanism to sustain higher plant growth. Furthermore, the expressed gene composition was closely related to both dynamic (e.g., soil moisture) and stable environmental attributes (e.g., C4 leaf C or N content), indicating that RNA analyses could also capture certain stable trends in the long-term treatment. Overall, this study revealed the importance of elucidating functional gene expressions of soil microbial community in enhancing our understanding of ecosystem responses to warming.

Keywords: GeoChip; RNA; functional gene expression; global climate change; warming.

FIGURE 1

Detrended correspondence analysis (DCA) of microbial community composition in control and warming treatments based on expressed functional genes.

FIGURE 2

Difference of normalized signal intensity between warming and control for expressed functional genes involved in carbon (C) degradation. The complexity of carbon is presented in order from labile to recalcitrant from left to right. Error bars represent standard error. Significance according to two tailed paired t-test were labeled by ^∗∗∗p ≤ 0.01, ^∗∗p ≤ 0.05, ^∗p ≤ 0.10; while red and blue colors represent increases and decreases caused by warming.

FIGURE 3

Percentage change of normalized signal intensity from expressed functional genes involved in nitrogen (N) cycling to warming. Significance according to two tailed paired t-test were labeled by ^∗∗∗p ≤ 0.01, ^∗∗p ≤ 0.05, ^∗p ≤ 0.10. Red and blue colors represent increases and decreases caused by warming; while gray color means that the expressed genes were not present on the version of GeoChip used, or were undetected.

FIGURE 4

Difference of normalized signal intensity between warming and control for expressed functional genes involved in phosphorus (P) and sulfur (S) cycling. Error bars represent standard error. Significance according to two tailed paired t-test were labeled by ^∗∗∗p ≤ 0.01, ^∗∗p ≤ 0.05, ^∗p ≤ 0.10; while red and blue colors represent increases and decreases caused by warming.

FIGURE 5

Canonical correspondence analysis (CCA) of microbial community composition based on expressed functional genes with selected environmental variables. The table presents results from partial CCA and variation partitioning analysis (VPA). The selected environmental variables include soil moisture (Soil M), soil temperature (Soil T), leaf C:N ratio in C₄ species (C₄ leaf C:N), and below-ground net primary productivity (BNPP).

FIGURE 6

Conceptual model of warming impacts on grassland ecosystem processes based on results from this study. Greenhouse gas pool of CO₂ is represented by square frames in green color, material pools are represented by square frames in yellow color, and biological processes are represented by punched tape frames in blue color. Material flows are represented by thicker rows in black color. Impacts of environmental attributes (e.g., soil temperature) and microbial community are represented by narrow rows in red (increase), blue (decrease) or black (different directions) colors.