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

Detalhes bibliográficos
Autor(a) principal: CAMARGO, A. P.
Data de Publicação: 2023
Outros Autores: 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.
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice)
Texto Completo: http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151181
https://doi.org/10.1038/s41396-022-01345-1
Resumo: 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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spelling Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.Ecossistema de pastagensCampos rupestresMicrobioma vegetalSequenciamento de dadosPlant microbiomesSoil microbesData sequencingGenomaNitrogênioBactériaVelloziaceaeGenomeNitrogenThe 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.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. deJOSE, J.GERHARDT, I. R.DANTE, R. A.MUKHERJEE, S.HUNTEMANN, M.KYRPIDES, N. C.CARAZZOLLE, M. F.ARRUDA, P.2023-01-24T12:01:32Z2023-01-24T12:01:32Z2023-01-242023info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleThe ISME Journal, v. 17, n. 3, p. 354-370, Mar. 2023.http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151181https://doi.org/10.1038/s41396-022-01345-1enginfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice)instname:Empresa Brasileira de Pesquisa Agropecuária (Embrapa)instacron:EMBRAPA2023-01-24T12:01:32Zoai:www.alice.cnptia.embrapa.br:doc/1151181Repositório InstitucionalPUBhttps://www.alice.cnptia.embrapa.br/oai/requestopendoar:21542023-01-24T12:01:32falseRepositório InstitucionalPUBhttps://www.alice.cnptia.embrapa.br/oai/requestcg-riaa@embrapa.bropendoar:21542023-01-24T12:01:32Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice) - Empresa Brasileira de Pesquisa Agropecuária (Embrapa)false
dc.title.none.fl_str_mv Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.
title Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.
spellingShingle Plant microbiomes harbor potential to promote nutrient turnover in impoverished substrates of a Brazilian biodiversity hotspot.
CAMARGO, A. P.
Ecossistema de pastagens
Campos rupestres
Microbioma vegetal
Sequenciamento de dados
Plant microbiomes
Soil microbes
Data sequencing
Genoma
Nitrogênio
Bactéria
Velloziaceae
Genome
Nitrogen
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.
author CAMARGO, A. P.
author_facet 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_role author
author2 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.
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv 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.
dc.contributor.author.fl_str_mv 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.
dc.subject.por.fl_str_mv Ecossistema de pastagens
Campos rupestres
Microbioma vegetal
Sequenciamento de dados
Plant microbiomes
Soil microbes
Data sequencing
Genoma
Nitrogênio
Bactéria
Velloziaceae
Genome
Nitrogen
topic Ecossistema de pastagens
Campos rupestres
Microbioma vegetal
Sequenciamento de dados
Plant microbiomes
Soil microbes
Data sequencing
Genoma
Nitrogênio
Bactéria
Velloziaceae
Genome
Nitrogen
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.
publishDate 2023
dc.date.none.fl_str_mv 2023-01-24T12:01:32Z
2023-01-24T12:01:32Z
2023-01-24
2023
dc.type.driver.fl_str_mv info:eu-repo/semantics/publishedVersion
info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv The ISME Journal, v. 17, n. 3, p. 354-370, Mar. 2023.
http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151181
https://doi.org/10.1038/s41396-022-01345-1
identifier_str_mv The ISME Journal, v. 17, n. 3, p. 354-370, Mar. 2023.
url http://www.alice.cnptia.embrapa.br/alice/handle/doc/1151181
https://doi.org/10.1038/s41396-022-01345-1
dc.language.iso.fl_str_mv eng
language eng
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv reponame:Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice)
instname:Empresa Brasileira de Pesquisa Agropecuária (Embrapa)
instacron:EMBRAPA
instname_str Empresa Brasileira de Pesquisa Agropecuária (Embrapa)
instacron_str EMBRAPA
institution EMBRAPA
reponame_str Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice)
collection Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice)
repository.name.fl_str_mv Repositório Institucional da EMBRAPA (Repository Open Access to Scientific Information from EMBRAPA - Alice) - Empresa Brasileira de Pesquisa Agropecuária (Embrapa)
repository.mail.fl_str_mv cg-riaa@embrapa.br
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