From community structure to function: Metagenomics-enabled predictive understanding of microbial communities to climate warming at the temperate grassland ecosystems in Oklahoma

Background/Question/Methods

Feedback between terrestrial carbon (C) and climate warming is one of the major uncertainties in projecting future climate warming. Most carbon-climate modeling studies predict a positive feedback in that warming leads to a decrease in ecosystem C storage due to a warming-induced increase in soil C release through respiration. Results from various experimental studies on the effects of climate warming on ecosystem C storage, however, are controversial and contradictory. Such controversy is partially due to the lack of mechanistic understanding of the feedback responses of belowground microbial communities to climate warming because most of those experiments have primarily focused on plant communities. Although microorganisms catalyse most biosphere processes related to fluxes of greenhouse gases, little is known about the microbial role in regulating future climate change. Here, we used integrated metagenomics, GeoChip and Illumina Hi-Seq2000 platform (2 X 100 paired end), to determine the feedback responses of microbial community structure and functions to climate warming in a tall grass prairie ecosystem in Central Oklahoma. Moreover, the dynamics of belowground net primary productivity (BNPP) and the fraction of BNPP to NPP (f_BNPP), which are of fundamental importance in understanding carbon allocation and storage in grasslands, were examined as well.

Results/Conclusions

Warming increased BNPP by 42-67% with a significant increase in wet years, while f_BNPP was increased more in dry years, suggesting that water availability dominated their interannual variability and responses to warming. Mainly discovered by GeoChip, microorganisms play crucial roles in regulating soil C dynamics through (i) shifting microbial community composition, most likely led to the reduced temperature sensitivity of heterotrophic soil respiration, (ii) differentially stimulating genes for degrading labile but not recalcitrant C so as to maintain long-term soil C stability, and (iii) enhancing nutrient cycling processes to promote plant nutrient use efficiency and hence plant growth. All these mechanisms would weaken the positive feedback between the terrestrial C cycle and climate warming. For metagenomics sequencing, more than 90% genes and organisms did not differ in abundance by warming, while a higher abundance of genes under warming was related to sporulation. Significant differences were among the top four most abundant phyla (Proteobacteria, Acidobacteria, Planctomycetes, and Bacteriodetes). Several metabolic pathways were increased under warming, including those for greenhouse gas emissions, nitrogen cycling, and organic C utilization. Overall, all these results elucidating the complexity of ecosystem responses to climate warming and microbially mediated feedbacks is fundamental to understanding these responses.