Rare bacterial and fungal taxa respond strongly to combined inorganic and organic fertilization under short-term conditions

Soil microbial communities play a crucial role in driving multiple ecosystem functions. Although numerous studies have investigated the effects of fertilization on the entire soil microbial community, the responses of abundant (relative abundance ≥ 1 % in all samples, or ≥ 1 % in some samples but never < 0.01 % in any samples) and rare (relative abundance < 0.01% in all samples, or < 0.01% in some samples but never≥ 1% in any samples) microbial taxa, as along with their relative contributions to ecosystem functions in agricultural soils under combined organic and inorganic fertilization, have been less explored. Here, a field experiment revealed that rare bacterial and fungal taxa were more sensitive to short-term fertilization than abundant taxa. The combined application of inorganic and organic fertilizers maintained the alpha-diversity of rare bacterial taxa and enhanced the alpha-diversity of rare fungal taxa. The significant impact of fertilization on the bacterial community was primarily induced by alterations in soil pH (decreased from 6.01 to 5.46), total phosphorus (0.32 – 0.37 g/kg), available phosphorus (1.24 – 4.76 mg/kg), and available potassium (41.11 – 58.78 mg/kg), whereas the fungal community was less influenced by fertilization. The dissimilarity of both abundant (Mantel r = 0.38, P = 0.001) and rare (Mantel r = 0.26, P = 0.014) bacterial taxa exhibited positive relationships with ecosystem multifunctionality. Additionally, ecosystem multifunctionality was positively associated with the relative abundance of specific genera and keystone species, particularly rare bacterial taxa (e.g., Melioribacter, Aquisphaera, Sunxiuqinia, Methylobacterium, and Thermosporothrix), the abundant fungal genus Achroiostachys, and rare fungal taxa (e.g., Paraphelidium, Pseudallescheria, Scutellinia, Niesslia, Tilletia, Coprinopsis, Poaceascoma, Entrophospora sp., Acremonium persicinum, Hydropisphaera erubescens, and Rozellomycota sp.) (ρ = 0.52–0.75, P < 0.05). A partial least-squares path model indicated that soil nutrients (path coefficient = 0.83, p = 0.001) and microbial beta-diversity (path coefficient = 0.18, p = 0.049) exerted primary direct and positive effects on ecosystem multifunctionality, with soil nutrients also indirectly influencing ecosystem multifunctionality through microbial beta-diversity. Collectively, these findings underscore the significant response of rare, rather than abundant, microbial taxa and their contributions to ecosystem multifunctionality. This highlights the potential of appropriately combined inorganic and organic fertilizers, which promote rare microbial taxa, to enhance the multifunctionality of agricultural ecosystems.