Distinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes

Abstract

ABSTRACT It is a central ecological goal to explore the effects of global change factors on soil microbial communities. The vast functional gene repertoire of soil microbial communities is composed of both core and accessory genes, which may be governed by distinct drivers. This intuitive hypothesis, however, remains largely unexplored. We conducted a 5-year nitrogen and water addition experiment in the Eurasian steppe and quantified microbial gene diversity via shotgun metagenomics. Nitrogen addition led to an 11-fold increase in the abundance (based on quantitative PCR [qPCR]) of ammonia-oxidizing bacteria, which have mainly core community genes and few accessory community genes. Thus, nitrogen addition substantially increased the relative abundance of many core genes at the whole-community level. Water addition stimulated both plant diversity and microbial respiration; however, increased carbon/energy resources from plants did not counteract increased respiration, so soil carbon/energy resources became more limited. Thus, water addition selected for microorganisms with genes responsible for degrading recalcitrant soil organic matter. Accordingly, many other microorganisms without these genes (but likely with other accessory community genes due to relatively stable average microbial genome size) were selected against, leading to the decrease in the diversity of accessory community genes. In summary, nitrogen addition primarily affected core community genes through nitrogen-cycling processes, and water addition primarily regulated accessory community genes through carbon-cycling processes. Although both gene components may significantly respond as the intensity of nitrogen/water addition increases, our results demonstrated how these common global change factors distinctly impact each component. IMPORTANCE Our results demonstrated increased ecosystem nitrogen and water content as the primary drivers of the core and accessory components of soil microbial community functional diversity, respectively. Our findings suggested that more attention should be paid to certain components of community functional diversity under specific global change conditions. Our findings also indicated that microbial communities have adapted to nitrogen addition by strengthening the function of ammonia oxidization to deplete the excess nitrogen, thus maintaining ecosystem homeostasis. Because community gene richness is primarily determined by the presence/absence of accessory community genes, our findings further implied that strategies such as maintaining the amount of soil organic matter could be adopted to effectively improve the functional gene diversity of soil microbial communities subject to global change factors.

Keywords

• accessory community gene
• core community gene
• grassland
• increased precipitation
• microbial diversity
• nitrogen deposition