Keystone ecological cluster rather than the whole community of phoD-encoding bacteria driving ecological function and the improvement of yield under long-term organic regime in greenhouse

Abstract

The phoD-encoding bacteria play a crucial role in mediating agricultural soil organic phosphorus mineralization and altering the bioavailability of phosphorus. Clarifying the effect of the phoD-encoding bacterial ecological functional characteristic and their contribution to soil multifunctionality response to different fertilization is essential for improving sustainable agricultural productivity in the intensive greenhouse. Therefore, we investigated the response of the phoD-encoding bacterial community to soil organic phosphorus pools and physiochemical features under eight long-term fertilization treatments, spanning both organic and inorganic regimes, and their subsequent impact on tomato yield. The results revealed total organic phosphorus (TPo) content tended to accumulate in moderately labile Po (MLPo) and fulvic acid-associated Po (FAPo) pools under organic regime compared to inorganic regime. Notably, nitrogen-phosphorus chemical fertilizers plus organic manure (MNP) significantly reduced the content of available P (AP), labile Po (LPo), and total inorganic P (TPi) pools compared to the phosphorus chemical fertilizer plus organic manure (MP) treatment, while enhancing the long-term supply of organic phosphorus availability by promoting its accumulation in the MLPo pool. Alkaline phosphomonoesterase (ALP) activity, which was significantly reduced by nitrogen fertilizer under inorganic regime, was significantly recovered and enhanced in organic regime. The phoD-encoding bacterial community was strongly influenced by organic regime, followed by phosphorus and nitrogen fertilizers, with soil organic matter (SOM) being a key determinant. Long-term fertilizers and regimes led to the formation of five keystone ecological clusters within the phoD-encoding bacterial community. SEM revealed that the increased cumulative relative abundance (CPM) of module #1 under organic manure physiologically regulated ALP activity. Additionally, the increased multibiodiversity of module #1 enhanced soil multifunctionality indirectly contributing to higher tomato yields. Collectively, long-term organic regime facilitated the formation of a keystone ecological cluster of phoD-encoding bacteria, which effectively mitigated the inhibitory effect of nitrogen fertilizer on ALP activity, thereby enhancing soil multifunctionality in increasing yield.