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Plant-associated microbiomes promote nutrient turnover in impoverished substrates of a biodiversity hotspot

View ORCID ProfileAntonio P. Camargo, View ORCID ProfileRafael Soares Correa de Souza, View ORCID ProfileJuliana Jose, View ORCID ProfileIsabel R. Gerhardt, View ORCID ProfileRicardo A. Dante, View ORCID ProfileSupratim Mukherjee, View ORCID ProfileMarcel Huntemann, View ORCID ProfileNikos C. Kyrpides, View ORCID ProfileMarcelo F. Carazzolle, View ORCID ProfilePaulo Arruda
doi: https://doi.org/10.1101/2021.07.30.454538
Antonio P. Camargo
1Centro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas (UNICAMP), 13083-875, Campinas, SP, Brazil
2Departamento de Genética e Evolução, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), 13083-970, Campinas, SP, Brazil
3Genomics for Climate Change Research Center (GCCRC), Universidade Estadual de Campinas (UNICAMP), 13083-875, Campinas, SP, Brazil
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Rafael Soares Correa de Souza
1Centro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas (UNICAMP), 13083-875, Campinas, SP, Brazil
3Genomics for Climate Change Research Center (GCCRC), Universidade Estadual de Campinas (UNICAMP), 13083-875, Campinas, SP, Brazil
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  • For correspondence: scs.rafael@gmail.com parruda@unicamp.br
Juliana Jose
2Departamento de Genética e Evolução, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), 13083-970, Campinas, SP, Brazil
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Isabel R. Gerhardt
1Centro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas (UNICAMP), 13083-875, Campinas, SP, Brazil
3Genomics for Climate Change Research Center (GCCRC), Universidade Estadual de Campinas (UNICAMP), 13083-875, Campinas, SP, Brazil
4Embrapa Informática Agropecuária, 13083-886, Campinas, SP, Brazil
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Ricardo A. Dante
1Centro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas (UNICAMP), 13083-875, Campinas, SP, Brazil
3Genomics for Climate Change Research Center (GCCRC), Universidade Estadual de Campinas (UNICAMP), 13083-875, Campinas, SP, Brazil
4Embrapa Informática Agropecuária, 13083-886, Campinas, SP, Brazil
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Supratim Mukherjee
5US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Marcel Huntemann
5US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Nikos C. Kyrpides
5US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
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Marcelo F. Carazzolle
2Departamento de Genética e Evolução, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), 13083-970, Campinas, SP, Brazil
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Paulo Arruda
1Centro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas (UNICAMP), 13083-875, Campinas, SP, Brazil
2Departamento de Genética e Evolução, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), 13083-970, Campinas, SP, Brazil
3Genomics for Climate Change Research Center (GCCRC), Universidade Estadual de Campinas (UNICAMP), 13083-875, Campinas, SP, Brazil
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  • ORCID record for Paulo Arruda
  • For correspondence: scs.rafael@gmail.com parruda@unicamp.br
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Abstract

The substrates of the Brazilian campos rupestres have extremely low concentrations of key nutrients, mainly phosphorus, imposing severe restrictions to plant growth. Regardless, this ecosystem harbors enormous biodiversity which raises the question of how nutrients are cycled and acquired by the biosphere. To uncover the nutrient turnover potential of plant-associated microorganisms in the campos rupestres, we investigated the compositions and functions of microbiomes associated with two species of the Velloziaceae family that grow over distinct substrates (soil and rock). Amplicon, metagenomic, and metagenome-assembled genome sequence data showed that the campos rupestres harbor a novel assemblage of plant-associated prokaryotes and fungi. Compositional analysis revealed that the plant-associated soil and rock communities differed in taxonomic structure but shared a core of highly efficient colonizers that were strongly coupled with nutrient mobilization. Investigation of functional and abundance data revealed that the plant hosts actively recruit communities by exuding organic compounds and that the root-associated microbiomes possess a diverse repertoire of phosphorus turnover mechanisms. We also showed that the microbiomes of both plant species encompass novel populations capable of mobilizing nitrogen and that the substrate strongly influences the dynamics of this cycle. Our results show that the interplay between plants and their microbiomes shapes nutrient turnover in the campos rupestres. We highlight that investigation of microbial diversity is fundamental to understand plant fitness in stressful environments.

Competing Interest Statement

The authors have declared no competing interest.

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Plant-associated microbiomes promote nutrient turnover in impoverished substrates of a biodiversity hotspot
Antonio P. Camargo, Rafael Soares Correa de Souza, Juliana Jose, Isabel R. Gerhardt, Ricardo A. Dante, Supratim Mukherjee, Marcel Huntemann, Nikos C. Kyrpides, Marcelo F. Carazzolle, Paulo Arruda
bioRxiv 2021.07.30.454538; doi: https://doi.org/10.1101/2021.07.30.454538
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Plant-associated microbiomes promote nutrient turnover in impoverished substrates of a biodiversity hotspot
Antonio P. Camargo, Rafael Soares Correa de Souza, Juliana Jose, Isabel R. Gerhardt, Ricardo A. Dante, Supratim Mukherjee, Marcel Huntemann, Nikos C. Kyrpides, Marcelo F. Carazzolle, Paulo Arruda
bioRxiv 2021.07.30.454538; doi: https://doi.org/10.1101/2021.07.30.454538

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