Key role of microbial necromass and iron minerals in retaining micronutrients and facilitating biological nitrogen fixation in paddy soils

Abstract

Paddy fields, as the largest anthropogenic wetlands on Earth, face a high risk of micronutrient loss through surface runoff and leaching due to their frequent irrigation-drainage cycles, as well as removal with crop harvest. While micronutrient's losses largely impede biological nitrogen fixation (BNF) in soils, agricultural practices and mechanisms that retain micronutrients and thus increase BNF in paddy soils remain underexplored. Here we showed that the long-term (40 years) application of fertilizers increased the contents of microbial necromass in paddy soils by 20%-43% compared to the unfertilized control. In particular, long-term organic fertilizations increased poorly crystalline minerals through intensifying mineral weathering, which further contributed to the increased stable carbon burials in paddy soils. Synchrotron radiation based spectromicroscopy analysis provided direct evidence demonstrating a differential control of mineral hydroxyl on C functional groups at the submicron scale in paddy soils. Notably, microbial necromass and short-range ordered minerals had a strong correlation with the content and bioavailability of micronutrients in paddy soils, indicating their key roles in the retention of micronutrients. Metagenomic sequencing analysis further indicated that the content and bioavailability of micronutrients were strongly correlated with the abundance of the key N-fixing genera (i.e., Azospirillum and Bradyrhizobium). Unexpectedly, structural equation modeling (SEM) identified that microbial necromass exerted the strongest control on N-fixing genera, highlighting an underappreciated role of microbial necromass as a reservoir of micronutrients. Based on micronutrient's bioavailability and metagenomic sequencing, we conclude that micronutrients are the key factor for BNF in paddy soils, offering significant implications for managing BNF in paddy soils.