Drought suppresses rhizosphere carbon inputs and losses with cascading effects on soil microbial communities in a pine forest

Severe drought impacts soil organic carbon (SOC) cycling. Yet, there is limited understanding of drought effects on rhizosphere C allocation and its fate in the soil, since belowground C contributes to new SOC formation while fueling soil microbial communities and SOC mineralization. Here, we quantified rhizosphere C inputs and losses in a 17-year long irrigation experiment in a dry Scots pine forest using 13C-enriched soil ingrowth bags with different mesh sizes. Fungal and bacterial communities inside the ingrowth bags and in adjacent soils were analyzed by Illumina MiSeq sequencing. After two years, net new SOC accumulation was 5 times greater in root-accessible vs root-exclusion bags (1000- vs 20-μm mesh). Irrigation stimulated new SOC formation in the first year as compared to natural drought both in root-accessible (+26%) and root-exclusion bags (+47%). Losses of “old” 13C-enriched SOC increased under irrigation in root-accessible (+88%) and root-exclusion bags (+32%), resulting in an overall balanced effect of irrigation on SOC. After two years, irrigation showed a limited effect on net new SOC formation both in root-accessible and root-exclusion bags despite a 70% greater root ingrowth under irrigation. We attribute the lacking irrigation effect on rhizosphere-derived SOC to higher respiratory losses of new soil C, which is in line with +55% old C losses by irrigation in root-accessible bags after two years. These findings indicate a faster C cycling in the rhizosphere under irrigation with enhanced C inputs, which were however rapidly mineralized, resulting in negligible net effects. The increased belowground C allocation and increased C turnover in the rhizosphere under irrigation were paralleled by shifts in fungal and bacterial communities in ingrowth bags as well as in adjacent soils. Fungal and bacterial community structures were also shaped by the presence of roots in the bags. Overall, our results in this long-term irrigation experiment imply that naturally dry conditions slow SOC cycling, suppressing both rhizosphere C inputs and losses. The reduced supply of belowground C leads to cascading effects on soil microbial community composition under drought.