Elevated CO₂ decouples bacterial antagonism from wheat take-all suppression while reshaping rhizosphere microbiome responses

Rising atmospheric CO₂ may alter ecosystem dynamics and plant-pathogen interactions, such as those involving Gaeumannomyces graminis var. tritici (Ggt), the causal agent of wheat take-all disease. However, how altered growth chamber CO₂ regimes interact with Ggt and bacteria consortia remains to be fully elucidated. This study evaluated Ggt growth, bacterial consortia performance, and plant-microbiome responses under contrasting incubator and chamber CO₂ conditions.

Two experiments were conducted under contrasting CO₂ environments: (i) in vitro antagonism assays in dedicated incubators to assess bacteria consortia (formed by Bacillus sp., Serratia sp., Acinetobacter sp.) activity against Ggt, and (ii) climate-controlled plant assays in dedicated growth chambers to assess wheat growth, physiology, disease severity, and rhizobiome shifts during Ggt inoculation.

Bacterial treatments inhibited Ggt growth in vitro; early inhibition (day 2) favored aCO₂, whereas eCO₂ enhanced day-6 antagonism for Acinetobacter sp. and the consortium. Under eCO₂, the consortium decreased SOD and chitinase activities, while Acinetobacter sp. tripled chitinase. In growth chambers, eCO₂ enhanced shoot biomass and photosynthesis across treatments (CO₂-fertilization effect), but consortia inoculation failed to significantly suppress take-all disease in planta. Treatment-specific redox shifts occurred, with Ggt + consortia inoculation under eCO₂ exhibiting the highest root lipid peroxidation (TBARS). Rhizosphere analysis linked eCO₂ to increased alpha diversity, enrichment of stress-adapted taxa (Roseomonas, Pseudonocardia), and increased the predicted relative abundance of functional categories associated with cellulolysis and denitrification.

Overall, bacteria consortia exhibited strong in vitro antagonism against Ggt confirming our previous reports. Despite its previously demonstrated antagonistic potential, the bacterial consortium did not significantly suppress take-all disease in plants under the elevated-CO₂ chamber environment. This finding raises the concern that microbial bioinoculants developed under current conditions may not necessarily maintain their effectiveness under future atmospheric scenarios. Consequently, climate robustness should be incorporated as a critical criterion in the development and validation of agricultural bioproducts.