Soil parameters affect the functional diversity of the symbiotic microbiota of Hymenaea courbaril L., a Neotropical fruit tree

Abstract

There is considerable evidence that abiotic factors have an important influence on the microbial diversity of natural ecosystems. In the present study, we tested the hypothesis that rhizospheric and endophytic micro-organisms isolated from the roots of Hymenaea courbaril L. in two biomes with distinct ecological characteristics – the Pantanal wetland and the Cerrado savanna – present distinct functional traits. We also evaluated the functional diversity (H′) of the microbiota and the potential effects of soil parameters, such as Organic Material (OM), cation exchange capacity (CEC), and nutrient concentrations, on the relative abundance of the micro-organisms with functional traits such as the solubilization of phosphates (CaHPO4, AlPO4, and FePO4), the synthesis of indole-3-acetic acid (IAA) and the ACC deaminase enzyme, and antibiosis to the phytopathogens Fusarium sp., Sclerotinia sclerotiorum, and Rhizoctonia sp. A higher percentage of the micro-organisms from the Pantanal (in comparison with the Cerrado) presented intense or very intense function in the synthesis of IAA and antibiosis, with a higher degree of specialization (reduced functional diversity) in the former trait (H’ = 0.73) and a lower degree in the latter (H’ = 0.91 for antibiosis to Fusarium sp.; H’ = 0.97 for S. sclerotiorum, and H’ = 0.80 for Rhizoctonia sp.). The micro-organisms of the Cerrado were more effective in the solubilization of phosphates, and the mean concentrations of P solubilized by these micro-organisms were higher than those observed in the isolates from the Pantanal, when the sources were AlPO4 and FePO4, which indicates a potential relationship between the high concentrations of Al and Fe found naturally in the soils of the Cerrado and the functional traits of its endemic microbiota. We also observed high levels of diversity in the functional traits of the Cerrado micro-organisms involved in solubilization (H’ = 1.09 for CaHPO4, H’ = 1.05 for AlPO4, and H’ = 1.09 for FePO4). All the isolates from both biomes synthetized ACC deaminase very intensively. In the Pantanal, soil parameters such as pH, OM, CEC, and the levels of Mn and Fe, as well as the Fe concentrations in the root and aerial portion of the plant affected the relative abundance of the micro-organisms that had efficient functional traits. In the Cerrado soil, the parameters pH, CEC, and the Mn, Mg, and Fe concentrations, as well as the level of Fe in the aerial part of the plant all affected the relative abundance. We proved our hypothesis on the specialization of the micro-organisms for specific functional traits, and also that the functionality of the symbiotic microbiota is influenced by environmental parameters. The present study provides important insights into the interactions between the soil and the endophytic root and rhizospheric micro-organisms isolated from H. courbaril L. in the Pantanal and Cerrado biomes. These findings will support future studies that will better define the environmental factors that influence the expression of different functional traits by the micro-organisms in the microbiome.