Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.

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.

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Main Authors: CAMARGO, A. P., SOUZA, R. S. C. de, JOSE, J., GERHARDT, I. R., DANTE, R. A., MUKHERJEE, S., HUNTEMANN, M., KYRPIDES, N. C., CARAZZOLLE, M. F., ARRUDA, P.
Other Authors: ANTONIO P. CAMARGO, UNIVERSIDADE ESTADUAL DE CAMPINAS; RAFAEL S. C. DE SOUZA, UNIVERSIDADE ESTADUAL DE CAMPINAS, SYMBIOMICS MICROBIOME SOLUTIONS; JULIANA JOSE, UNIVERSIDADE ESTADUAL DE CAMPINAS; ISABEL RODRIGUES GERHARDT, CNPTIA; RICARDO AUGUSTO DANTE, CNPTIA; SUPRATIM MUKHERJEE, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; MARCEL HUNTEMANN, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; NIKOS C. KYRPIDES, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; MARCELO F. CARAZZOLLE, UNIVERSIDADE ESTADUAL DE CAMPINAS; PAULO ARRUDA, UNIVERSIDADE ESTADUAL DE CAMPINAS.
Format: Artigo de periódico biblioteca
Language:Ingles
English
Published: The ISME Journal, 2022. 2023-01-24
Subjects:Ecossistema de pastagens, Campos rupestres, Microbioma vegetal, Sequenciamento de dados, Plant microbiomes, Soil microbes, Data sequencing, Genoma, Nitrogênio, Bactéria, Velloziaceae, Genome, Nitrogen,
Online Access:http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151181
https://doi.org/10.1038/s41396-022-01345-1
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spelling dig-alice-doc-11511812023-01-24T12:01:32Z Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot. CAMARGO, A. P. SOUZA, R. S. C. de JOSE, J. GERHARDT, I. R. DANTE, R. A. MUKHERJEE, S. HUNTEMANN, M. KYRPIDES, N. C. CARAZZOLLE, M. F. ARRUDA, P. ANTONIO P. CAMARGO, UNIVERSIDADE ESTADUAL DE CAMPINAS; RAFAEL S. C. DE SOUZA, UNIVERSIDADE ESTADUAL DE CAMPINAS, SYMBIOMICS MICROBIOME SOLUTIONS; JULIANA JOSE, UNIVERSIDADE ESTADUAL DE CAMPINAS; ISABEL RODRIGUES GERHARDT, CNPTIA; RICARDO AUGUSTO DANTE, CNPTIA; SUPRATIM MUKHERJEE, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; MARCEL HUNTEMANN, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; NIKOS C. KYRPIDES, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; MARCELO F. CARAZZOLLE, UNIVERSIDADE ESTADUAL DE CAMPINAS; PAULO ARRUDA, UNIVERSIDADE ESTADUAL DE CAMPINAS. Ecossistema de pastagens Campos rupestres Microbioma vegetal Sequenciamento de dados Plant microbiomes Soil microbes Data sequencing Genoma Nitrogênio Bactéria Velloziaceae Genome Nitrogen 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. Online first. 2023-01-24T12:01:32Z 2023-01-24T12:01:32Z 2023-01-24 2022 Artigo de periódico http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151181 https://doi.org/10.1038/s41396-022-01345-1 Ingles en openAccess The ISME Journal, 2022.
institution EMBRAPA
collection DSpace
country Brasil
countrycode BR
component Bibliográfico
access En linea
databasecode dig-alice
tag biblioteca
region America del Sur
libraryname Sistema de bibliotecas de EMBRAPA
language Ingles
English
topic Ecossistema de pastagens
Campos rupestres
Microbioma vegetal
Sequenciamento de dados
Plant microbiomes
Soil microbes
Data sequencing
Genoma
Nitrogênio
Bactéria
Velloziaceae
Genome
Nitrogen
Ecossistema de pastagens
Campos rupestres
Microbioma vegetal
Sequenciamento de dados
Plant microbiomes
Soil microbes
Data sequencing
Genoma
Nitrogênio
Bactéria
Velloziaceae
Genome
Nitrogen
spellingShingle Ecossistema de pastagens
Campos rupestres
Microbioma vegetal
Sequenciamento de dados
Plant microbiomes
Soil microbes
Data sequencing
Genoma
Nitrogênio
Bactéria
Velloziaceae
Genome
Nitrogen
Ecossistema de pastagens
Campos rupestres
Microbioma vegetal
Sequenciamento de dados
Plant microbiomes
Soil microbes
Data sequencing
Genoma
Nitrogênio
Bactéria
Velloziaceae
Genome
Nitrogen
CAMARGO, A. P.
SOUZA, R. S. C. de
JOSE, J.
GERHARDT, I. R.
DANTE, R. A.
MUKHERJEE, S.
HUNTEMANN, M.
KYRPIDES, N. C.
CARAZZOLLE, M. F.
ARRUDA, P.
Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.
description 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.
author2 ANTONIO P. CAMARGO, UNIVERSIDADE ESTADUAL DE CAMPINAS; RAFAEL S. C. DE SOUZA, UNIVERSIDADE ESTADUAL DE CAMPINAS, SYMBIOMICS MICROBIOME SOLUTIONS; JULIANA JOSE, UNIVERSIDADE ESTADUAL DE CAMPINAS; ISABEL RODRIGUES GERHARDT, CNPTIA; RICARDO AUGUSTO DANTE, CNPTIA; SUPRATIM MUKHERJEE, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; MARCEL HUNTEMANN, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; NIKOS C. KYRPIDES, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; MARCELO F. CARAZZOLLE, UNIVERSIDADE ESTADUAL DE CAMPINAS; PAULO ARRUDA, UNIVERSIDADE ESTADUAL DE CAMPINAS.
author_facet ANTONIO P. CAMARGO, UNIVERSIDADE ESTADUAL DE CAMPINAS; RAFAEL S. C. DE SOUZA, UNIVERSIDADE ESTADUAL DE CAMPINAS, SYMBIOMICS MICROBIOME SOLUTIONS; JULIANA JOSE, UNIVERSIDADE ESTADUAL DE CAMPINAS; ISABEL RODRIGUES GERHARDT, CNPTIA; RICARDO AUGUSTO DANTE, CNPTIA; SUPRATIM MUKHERJEE, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; MARCEL HUNTEMANN, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; NIKOS C. KYRPIDES, DEPARTMENT OF ENERGY JOINT GENOME INSTITUTE; MARCELO F. CARAZZOLLE, UNIVERSIDADE ESTADUAL DE CAMPINAS; PAULO ARRUDA, UNIVERSIDADE ESTADUAL DE CAMPINAS.
CAMARGO, A. P.
SOUZA, R. S. C. de
JOSE, J.
GERHARDT, I. R.
DANTE, R. A.
MUKHERJEE, S.
HUNTEMANN, M.
KYRPIDES, N. C.
CARAZZOLLE, M. F.
ARRUDA, P.
format Artigo de periódico
topic_facet Ecossistema de pastagens
Campos rupestres
Microbioma vegetal
Sequenciamento de dados
Plant microbiomes
Soil microbes
Data sequencing
Genoma
Nitrogênio
Bactéria
Velloziaceae
Genome
Nitrogen
author CAMARGO, A. P.
SOUZA, R. S. C. de
JOSE, J.
GERHARDT, I. R.
DANTE, R. A.
MUKHERJEE, S.
HUNTEMANN, M.
KYRPIDES, N. C.
CARAZZOLLE, M. F.
ARRUDA, P.
author_sort CAMARGO, A. P.
title Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.
title_short Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.
title_full Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.
title_fullStr Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.
title_full_unstemmed Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.
title_sort plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a brazilian biodiversity hotspot.
publisher The ISME Journal, 2022.
publishDate 2023-01-24
url http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151181
https://doi.org/10.1038/s41396-022-01345-1
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