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The Ignavibacteria are ubiquitously abundant in paddy soils, but their functional role is poorly known. Here, we applied a targeted meta-genomic/transcriptomic approach to elucidate genetic potential and functional activity of the Ignavibacteria in straw-amended paddy soils from Italy. Eight high-quality metagenome-assembled genomes (MAGs) were recovered, being the largest ones (∅ 4.8 Mbp) among all known Ignavibacteria genomes (∅ 3.7 Mbp). Functional annotation revealed that the Ignavibacteria in Italian paddy soil are facultative anaerobes, represent a novel lineage in the Ignavibacteriae phylum, and have the ability for aerobic-hybrid phenylacetate degradation. Their putative functional roles under anoxic and micro-oxic conditions were assessed by mapping environmental mRNA onto the MAGs. Transcript analysis showed that primary fermentation of sugars to acetate and hydrogen is a major energy-yielding pathway under anoxic conditions. Although the phenylacetate degradation pathway is widely distributed among taxonomically diverse paddy soil bacteria, Ignavibacteria almost exclusively expressed this pathway under micro-oxic conditions. In particular, the transcript level of the paaABCDE gene cluster increased significantly. It encodes a monooxygenase, which is the key enzyme of phenylacetate degradation. This was linked to a significant decrease in transcripts encoding fermentation pathways and oxygen-sensitive hydrogenases, but increase in transcripts encoding TCA cycle, respiratory chain, and proteins involved in oxygen stress response (SOD1, AhpC, Bfr). More than half of the carbohydrate-active enzymes (CAZymes) expressed under anoxic and micro-oxic conditions possessed signal peptides, thereby indicating that Ignavibacteria contribute to the decomposition of complex polymers, such as cellulose, hemicellulose, and chitin. In summary, the Ignavibacteria in rice field soil are metabolically versatile and particularly adapted to the varying oxygen conditions in this ecosystem. • Multi-omics was used to characterize yet uncultured Ignavibacteria in rice field soil. • High-quality MAGs revealed greatest metabolic versatility among known Ignavibacteria. • Primary fermentation was the major activity under anoxic paddy soil conditions. • Phenylacetate degradation was specifically induced under micro-oxic conditions. • Contribution to polymer hydrolysis occurred regardless of oxygen conditions. [ABSTRACT FROM AUTHOR]