Plant nickel-exclusion versus hyperaccumulation: a microbial perspective.

Background: In New Caledonia, nearly 2000 plant species grow on ultramafic substrates, which contain prominent levels of heavy metals and are deficient in essential plant nutrients. To colonize these habitats, such plants, known as metallophytes, have developed various adaptive behaviors towards metals (exclusion, tolerance, or hyperaccumulation). Ultramafic substrates also host many unique microorganisms, which are adapted to metallic environments and capable of boosting plant growth while assisting plants in acquiring essential micronutrients. Hence, plant-microbiota interactions play a key role in adapting to environmental stress. Here, we hypothesised that microbial associations in the different aboveground and underground compartments of metallophytes could be associated to their metal hyperaccumulation or exclusion phenotypes. This hypothesis was tested using a systematic comparative metabarcoding approach on the different compartments of two New Caledonian metallophytes belonging to the same genus and living in sympatry on ultramafic substrates: Psychotria gabriellae, a nickel-hyperaccumulator (Ni-HA), and Psychotria semperflorens, the related non-accumulator (nA) species.

Results: The study of the diversity and specificity of fungal amplicon sequence variants (ASVs) reveals a structuring of fungal communities at both the plant phenotype and compartment levels. In contrast, the structure of bacterial communities was primarily shaped by the belowground compartments. Additionally, we observed a lower diversity in the bacterial communities of the aboveground compartments of each species. For each plant species, we highlighted a distinct global microbial signature (biomarkers), as well as compartment-specific microbial associations.

Conclusion: To our knowledge, this study is the first to systematically compare the microbiomes associated with different compartments of New Caledonian metallophyte species growing on the same substrate and under identical environmental conditions but exhibiting different adaptive phenotypes. Our results reveal distinct microbial biomarkers between the Ni-hyperaccumulator and non-accumulator Psychotria species. Most of the highlighted biomarkers are abundant in various plants under metal stress and may contribute to improving the phytoextraction or phytostabilization processes. They are also known to tolerate heavy metals and enhance metal stress tolerance in plants. The present findings highlight that the microbial perspective is essential for better understanding the mechanisms of hyperaccumulation and exclusion at the whole-plant level. Video Abstract.