Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot
Abstract
The substrates of the Brazilian campos rupestres, a grassland ecosystem, have extremely low concentrations of phosphorus and nitrogen, imposing restrictions to plant growth. Despite that, this ecosystem harbors almost 15% of the Brazilian plant diversity, raising the question of how plants acquire nutrients in such a harsh environment. Here, we set out to uncover the taxonomic profile, the compositional and functional differences and similarities, and the nutrient turnover potential of microbial communities associated with two plant species of the campos rupestres-dominant family Velloziaceae that grow over distinct substrates (soil and rock). Using amplicon sequencing data, we show that, despite the pronounced composition differentiation, the plant-associated soil and rock communities share a core of highly efficient colonizers that tend to be highly abundant and is enriched in 21 bacterial families. Functional investigation of metagenomes and 522 metagenome-assembled genomes revealed that the microorganisms found associated to plant roots are enriched in genes involved in organic compound intake, and phosphorus and nitrogen turnover. We show that potential for phosphorus transport, mineralization, and solubilization are mostly found within bacterial families of the shared microbiome, such as Xanthobacteraceae and Bryobacteraceae. We also detected the full repertoire of nitrogen cycle-related genes and discovered a lineage ofmore »
- Authors:
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[1];
[2];
[3];
[4];
[4];
[5];
[5];
[5];
[3];
[3]
- Universidade Estadual de Campinas (UNICAMP) (Brazil); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Universidade Estadual de Campinas (UNICAMP) (Brazil); Symbiomics Microbiome Solutions, Florianópolis (Brazil)
- Universidade Estadual de Campinas (UNICAMP) (Brazil)
- Universidade Estadual de Campinas (UNICAMP) (Brazil); Embrapa Agricultura Digital, Campinas (Brazil)
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1983929
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 17; Journal Issue: 3; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Metagenomics; Soil microbiology
Citation Formats
Camargo, Antonio P., de Souza, Rafael S. C., Jose, Juliana, Gerhardt, Isabel R., Dante, Ricardo A., Mukherjee, Supratim, Huntemann, Marcel, Kyrpides, Nikos C., Carazzolle, Marcelo F., and Arruda, Paulo. Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot. United States: N. p., 2022.
Web. doi:10.1038/s41396-022-01345-1.
Camargo, Antonio P., de Souza, Rafael S. C., Jose, Juliana, Gerhardt, Isabel R., Dante, Ricardo A., Mukherjee, Supratim, Huntemann, Marcel, Kyrpides, Nikos C., Carazzolle, Marcelo F., & Arruda, Paulo. Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot. United States. https://doi.org/10.1038/s41396-022-01345-1
Camargo, Antonio P., de Souza, Rafael S. C., Jose, Juliana, Gerhardt, Isabel R., Dante, Ricardo A., Mukherjee, Supratim, Huntemann, Marcel, Kyrpides, Nikos C., Carazzolle, Marcelo F., and Arruda, Paulo. Tue .
"Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot". United States. https://doi.org/10.1038/s41396-022-01345-1. https://www.osti.gov/servlets/purl/1983929.
@article{osti_1983929,
title = {Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot},
author = {Camargo, Antonio P. and de Souza, Rafael S. C. and Jose, Juliana and Gerhardt, Isabel R. and Dante, Ricardo A. and Mukherjee, Supratim and Huntemann, Marcel and Kyrpides, Nikos C. and Carazzolle, Marcelo F. and Arruda, Paulo},
abstractNote = {The substrates of the Brazilian campos rupestres, a grassland ecosystem, have extremely low concentrations of phosphorus and nitrogen, imposing restrictions to plant growth. Despite that, this ecosystem harbors almost 15% of the Brazilian plant diversity, raising the question of how plants acquire nutrients in such a harsh environment. Here, we set out to uncover the taxonomic profile, the compositional and functional differences and similarities, and the nutrient turnover potential of microbial communities associated with two plant species of the campos rupestres-dominant family Velloziaceae that grow over distinct substrates (soil and rock). Using amplicon sequencing data, we show that, despite the pronounced composition differentiation, the plant-associated soil and rock communities share a core of highly efficient colonizers that tend to be highly abundant and is enriched in 21 bacterial families. Functional investigation of metagenomes and 522 metagenome-assembled genomes revealed that the microorganisms found associated to plant roots are enriched in genes involved in organic compound intake, and phosphorus and nitrogen turnover. We show that potential for phosphorus transport, mineralization, and solubilization are mostly found within bacterial families of the shared microbiome, such as Xanthobacteraceae and Bryobacteraceae. We also detected the full repertoire of nitrogen cycle-related genes and discovered a lineage of Isosphaeraceae that acquired nitrogen-fixing potential via horizontal gene transfer and might be also involved in nitrification via a metabolic handoff association with Binataceae. We highlight that plant-associated microbial populations in the campos rupestres harbor a genetic repertoire with potential to increase nutrient availability and that the microbiomes of biodiversity hotspots can reveal novel mechanisms of nutrient turnover.},
doi = {10.1038/s41396-022-01345-1},
journal = {The ISME Journal},
number = 3,
volume = 17,
place = {United States},
year = {Tue Dec 20 00:00:00 EST 2022},
month = {Tue Dec 20 00:00:00 EST 2022}
}
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