Cargando…

Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host

BACKGROUND: The rhizosheath-root system is an adaptive trait of sandy-desert speargrasses in response to unfavourable moisture and nutritional conditions. Under the deserts’ polyextreme conditions, plants interact with edaphic microorganisms that positively affect their fitness and resistance. Howev...

Descripción completa

Detalles Bibliográficos
Autores principales: Marasco, Ramona, Mosqueira, María J., Fusi, Marco, Ramond, Jean-Baptiste, Merlino, Giuseppe, Booth, Jenny M., Maggs-Kölling, Gillian, Cowan, Don A., Daffonchio, Daniele
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6280439/
https://www.ncbi.nlm.nih.gov/pubmed/30514367
http://dx.doi.org/10.1186/s40168-018-0597-y
_version_ 1783378673021222912
author Marasco, Ramona
Mosqueira, María J.
Fusi, Marco
Ramond, Jean-Baptiste
Merlino, Giuseppe
Booth, Jenny M.
Maggs-Kölling, Gillian
Cowan, Don A.
Daffonchio, Daniele
author_facet Marasco, Ramona
Mosqueira, María J.
Fusi, Marco
Ramond, Jean-Baptiste
Merlino, Giuseppe
Booth, Jenny M.
Maggs-Kölling, Gillian
Cowan, Don A.
Daffonchio, Daniele
author_sort Marasco, Ramona
collection PubMed
description BACKGROUND: The rhizosheath-root system is an adaptive trait of sandy-desert speargrasses in response to unfavourable moisture and nutritional conditions. Under the deserts’ polyextreme conditions, plants interact with edaphic microorganisms that positively affect their fitness and resistance. However, the trophic simplicity and environmental harshness of desert ecosystems have previously been shown to strongly influence soil microbial community assembly. We hypothesize that sand-driven ecological filtering constrains the microbial recruitment processes in the speargrass rhizosheath-root niche, prevailing over the plant-induced selection. METHODS: Bacterial and fungal communities from the rhizosheath-root compartments (endosphere root tissues, rhizosheath and rhizosphere) of three Namib Desert speargrass species (Stipagrostis sabulicola, S. seelyae and Cladoraphis spinosa) along with bulk sand have been studied to test our hypothesis. To minimize the variability determined by edaphic and climatic factors, plants living in a single dune were studied. We assessed the role of plant species vs the sandy substrate on the recruitment and selection, phylogenetic diversity and co-occurrence microbial networks of the rhizosheath-root system microbial communities. RESULTS: Microorganisms associated with the speargrass rhizosheath-root system were recruited from the surrounding bulk sand population and were significantly enriched in the rhizosheath compartments (10(5) and 10(4) of bacterial 16S rRNA and fungal ITS copies per gram of sand to up to 10(8) and 10(7) copies per gram, respectively). Furthermore, each rhizosheath-root system compartment hosted a specific microbial community demonstrating strong niche-partitioning. The rhizosheath-root systems of the three speargrass species studied were dominated by desert-adapted Actinobacteria and Alphaproteobacteria (e.g. Lechevalieria, Streptomyces and Microvirga) as well as saprophytic Ascomycota fungi (e.g. Curvularia, Aspergillus and Thielavia). Our results clearly showed a random phylogenetic turnover of rhizosheath-root system associated microbial communities, independent of the plant species, where stochastic factors drive neutral assembly. Co-occurrence network analyses also indicated that the bacterial and fungal community members of the rhizosheath-root systems established a higher number of interactions than those in the barren bulk sand, suggesting that the former are more stable and functional than the latter. CONCLUSION: Our study demonstrates that the rhizosheath-root system microbial communities of desert dune speargrasses are stochastically assembled and host-independent. This finding supports the concept that the selection determined by the desert sand prevails over that imposed by the genotype of the different plant species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0597-y) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6280439
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-62804392018-12-10 Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host Marasco, Ramona Mosqueira, María J. Fusi, Marco Ramond, Jean-Baptiste Merlino, Giuseppe Booth, Jenny M. Maggs-Kölling, Gillian Cowan, Don A. Daffonchio, Daniele Microbiome Research BACKGROUND: The rhizosheath-root system is an adaptive trait of sandy-desert speargrasses in response to unfavourable moisture and nutritional conditions. Under the deserts’ polyextreme conditions, plants interact with edaphic microorganisms that positively affect their fitness and resistance. However, the trophic simplicity and environmental harshness of desert ecosystems have previously been shown to strongly influence soil microbial community assembly. We hypothesize that sand-driven ecological filtering constrains the microbial recruitment processes in the speargrass rhizosheath-root niche, prevailing over the plant-induced selection. METHODS: Bacterial and fungal communities from the rhizosheath-root compartments (endosphere root tissues, rhizosheath and rhizosphere) of three Namib Desert speargrass species (Stipagrostis sabulicola, S. seelyae and Cladoraphis spinosa) along with bulk sand have been studied to test our hypothesis. To minimize the variability determined by edaphic and climatic factors, plants living in a single dune were studied. We assessed the role of plant species vs the sandy substrate on the recruitment and selection, phylogenetic diversity and co-occurrence microbial networks of the rhizosheath-root system microbial communities. RESULTS: Microorganisms associated with the speargrass rhizosheath-root system were recruited from the surrounding bulk sand population and were significantly enriched in the rhizosheath compartments (10(5) and 10(4) of bacterial 16S rRNA and fungal ITS copies per gram of sand to up to 10(8) and 10(7) copies per gram, respectively). Furthermore, each rhizosheath-root system compartment hosted a specific microbial community demonstrating strong niche-partitioning. The rhizosheath-root systems of the three speargrass species studied were dominated by desert-adapted Actinobacteria and Alphaproteobacteria (e.g. Lechevalieria, Streptomyces and Microvirga) as well as saprophytic Ascomycota fungi (e.g. Curvularia, Aspergillus and Thielavia). Our results clearly showed a random phylogenetic turnover of rhizosheath-root system associated microbial communities, independent of the plant species, where stochastic factors drive neutral assembly. Co-occurrence network analyses also indicated that the bacterial and fungal community members of the rhizosheath-root systems established a higher number of interactions than those in the barren bulk sand, suggesting that the former are more stable and functional than the latter. CONCLUSION: Our study demonstrates that the rhizosheath-root system microbial communities of desert dune speargrasses are stochastically assembled and host-independent. This finding supports the concept that the selection determined by the desert sand prevails over that imposed by the genotype of the different plant species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0597-y) contains supplementary material, which is available to authorized users. BioMed Central 2018-12-04 /pmc/articles/PMC6280439/ /pubmed/30514367 http://dx.doi.org/10.1186/s40168-018-0597-y Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Marasco, Ramona
Mosqueira, María J.
Fusi, Marco
Ramond, Jean-Baptiste
Merlino, Giuseppe
Booth, Jenny M.
Maggs-Kölling, Gillian
Cowan, Don A.
Daffonchio, Daniele
Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host
title Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host
title_full Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host
title_fullStr Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host
title_full_unstemmed Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host
title_short Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host
title_sort rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6280439/
https://www.ncbi.nlm.nih.gov/pubmed/30514367
http://dx.doi.org/10.1186/s40168-018-0597-y
work_keys_str_mv AT marascoramona rhizosheathmicrobialcommunityassemblyofsympatricdesertspeargrassesisindependentoftheplanthost
AT mosqueiramariaj rhizosheathmicrobialcommunityassemblyofsympatricdesertspeargrassesisindependentoftheplanthost
AT fusimarco rhizosheathmicrobialcommunityassemblyofsympatricdesertspeargrassesisindependentoftheplanthost
AT ramondjeanbaptiste rhizosheathmicrobialcommunityassemblyofsympatricdesertspeargrassesisindependentoftheplanthost
AT merlinogiuseppe rhizosheathmicrobialcommunityassemblyofsympatricdesertspeargrassesisindependentoftheplanthost
AT boothjennym rhizosheathmicrobialcommunityassemblyofsympatricdesertspeargrassesisindependentoftheplanthost
AT maggskollinggillian rhizosheathmicrobialcommunityassemblyofsympatricdesertspeargrassesisindependentoftheplanthost
AT cowandona rhizosheathmicrobialcommunityassemblyofsympatricdesertspeargrassesisindependentoftheplanthost
AT daffonchiodaniele rhizosheathmicrobialcommunityassemblyofsympatricdesertspeargrassesisindependentoftheplanthost