Metagenomic investigation of the microbiomes of plants adapted tonutritional limitation

Author(s)

Antônio Pedro Camargo

• Document type: Doctoral Thesis
• Press: Campinas, SP.
• Institution: Universidade Estadual de Campinas (UNICAMP). Instituto de Biologia
• Defense date: 2021-02-18

Examining board members

Marcelo Falsarella Carazzolle; Diego Mauricio Riaño Pachón; Gabriela Felix Persinoti; Valeria Maia de Oliveira

• Advisor: Marcelo Falsarella Carazzolle; Paulo Arruda

Abstract

The seasonally dry and nutrient-impoverished soils of the Brazilian campos rupestres impose severe growth-limiting conditions on plants. Species of a dominant plant family, Velloziaceae, are highly specialized to scarce resources of this environment. Despite plant-microbe associations playing critical roles in stressful ecosystems, the contribution of these interactions in the campos rupestres remains obscure. Here, we undertook metagenomic analyses to investigate the composition, dynamics, and functions of microbiomes associated with two Velloziaceae species that thrive in contrasting substrates of the campos rupestres: Vellozia epidendroides, which occupies shallow patches of soil, and Barbacenia macrantha, that grows over exposed rocks. We show that the microbial communities associated with these plants are diverse and taxonomically novel. We also demonstrate that there is a significant and phylogenetically structured differentiation between the communities associated with these two plants and that, despite this extensive contrast, an abundant core microbiome was found to be shared between the two species. Through the investigation of the metabolic potential of a diverse set of bacterial genomes recovered from the substrate and rhizosphere metagenomes, we were able to determine that the rock-associated bacterial communities are markedly enriched in functions related to autotrophy and carbon assimilation, which are likely important to sustain the microbial communities in such carbon-depleted substrate. We also found that this carbon-impoverishment of the rock substrates likely influences the nitrogen fixation dynamics in B. macrantha as our results indicate that the diazotrophs associated with this plant are all endophytic, while in V. epidendroides we also identified free-living nitrogen-fixing bacteria, including a family that received this metabolic genotype via horizontal gene transfer. In addition, we propose a novel model for nitrification where nitrite synthesis is not performed by a single cell and depends on a metabolic handoff interaction between two populations. Regarding phosphorus (P) nutrition, we found that taxa comprising the core microbiome are the major populations involved in P-mobilization and that P-scavenging mechanisms that complement those used by the plants are likely being selected in these communities. Finally, we also investigated the biosynthetic potential of the studied microbiomes and found a major differentiation regarding the products of their secondary metabolism, which could be mostly attributed to divergent taxonomic profiles and likely influence the plant-microbiome association dynamics. Taken together, our results show that the campos rupestres harbor an untapped microbial diversity that has the potential to uncover new forms of plant-microbiome interactions that could increase plant fitness in stressful conditions. (AU)

• FAPESP's process: 18/04240-0 - Metagenomic investigation of the microbiomes of plants adapted to phosphorus nutritional limitation
• Grantee: Antônio Pedro de Castello Branco da Rocha Camargo
• Support Opportunities: Scholarships in Brazil - Doctorate