Background Microbial-driven decomposition of plant residues is integral to carbon sequestration in terrestrial ecosystems. Actinobacteria, one of the most widely distributed bacterial phyla in soils, are known for their ability to degrade plant residues in vitro. However, their in situ importance and specific activity across contrasting ecological environments are not known. Here, we conducted three field experiments with buried straw in combination with microcosm experiments with 13C-straw in paddy soils under different soil fertility levels to reveal the ecophysiological roles of Actinobacteria in plant residue decomposition. Results While accounting for only 4.6% of the total bacterial abundance, the Actinobacteria encoded 16% of total abundance of carbohydrate-active enzymes (CAZymes). The taxonomic and functional compositions of the Actinobacteria were, surprisingly, relatively stable during straw decomposition. Slopes of linear regression models between straw chemical composition and Actinobacterial traits were flatter than those for other taxonomic groups at both local and regional scales due to holding genes encoding for full set of CAZymes, nitrogenases, and antibiotic synthetases. Ecological co-occurrence network and 13C-based metagenomic analyses both indicated that their importance for straw degradation increased in less fertile soils, as both links between Actinobacteria and other community members and relative abundances of their functional genes increased with decreasing soil fertility. Conclusions This study provided DNA-based evidence that non-dominant Actinobacteria plays a key ecophysiological role in plant residue decomposition as their members possess high proportions of CAZymes and as a group maintain a relatively stable presence during plant residue decomposition both in terms of taxonomic composition and functional roles. Their importance for decomposition was more pronounced in less fertile soils where their possession functional genes and interspecies interactions stood out more. Our work provides new ecophysiological angles for the understanding of the importance of Actinobacteria in global carbon cycling.

Straw, mainly dry stalks of crops, is an agricultural byproduct. Its incorporation to soils via microbial redistribution is an environment-friendly way to increase fertility. Fertilization influences soil microorganisms and straw degradation. However, our up to date knowledge on the responses of the straw decomposers to fertilization remains elusive. To this end, inoculated with paddy soils with 26-year applications of chemical fertilizers, organic amendments or controls without fertilization, microcosms were anoxically incubated with 13C-labelled rice straw amendment. DNA-based stable isotope probing and molecular ecological network analysis were conducted to unravel how straw degrading bacterial species shift in responses to fertilizations, as well as evaluate what their roles/links in the microbiome are. It was found that only a small percentage of the community ecotypes was participating into straw degradation under both fertilizations. Fertilization, especially with organic amendments decreased the predominance of Firmicutes- and Acidobacteria-like straw decomposers but increased those of the copiotrophs, such as β-Proteobacteria and Bacteroidetes due to increased soil fertility. For the same reason, fertilization shifted the hub species towards those of high degrading potential and created a more stable and efficient microbial consortium. These findings indicate that fertilization shapes a well-organized community of decomposers for accelerated straw degradation.