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The microbiome of Riccia liverworts is an important reservoir for microbial diversity in temporary agricultural crusts

BACKGROUND: The microbiota of liverworts provides an interesting model for plant symbioses; however, their microbiome assembly is not yet understood. Here, we assessed specific factors that shape microbial communities associated with Riccia temporary agricultural crusts in harvested fields by invest...

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Autores principales: Wicaksono, Wisnu Adi, Semler, Bettina, Pöltl, Martina, Berg, Christian, Berg, Gabriele, Cernava, Tomislav
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10233997/
https://www.ncbi.nlm.nih.gov/pubmed/37264474
http://dx.doi.org/10.1186/s40793-023-00501-0
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author Wicaksono, Wisnu Adi
Semler, Bettina
Pöltl, Martina
Berg, Christian
Berg, Gabriele
Cernava, Tomislav
author_facet Wicaksono, Wisnu Adi
Semler, Bettina
Pöltl, Martina
Berg, Christian
Berg, Gabriele
Cernava, Tomislav
author_sort Wicaksono, Wisnu Adi
collection PubMed
description BACKGROUND: The microbiota of liverworts provides an interesting model for plant symbioses; however, their microbiome assembly is not yet understood. Here, we assessed specific factors that shape microbial communities associated with Riccia temporary agricultural crusts in harvested fields by investigating bacterial, fungal and archaeal communities in thalli and adhering soil from different field sites in Styria and Burgenland, Austria combining qPCR analyses, amplicon sequencing and advanced microscopy. RESULTS: Riccia spec. div. was colonized by a very high abundance of bacteria (10(10) 16S rRNA gene copies per g of thallus) as well as archaea and fungi (10(8) ITS copies per g of thallus). Each Riccia thallus contain approx. 1000 prokaryotic and fungal ASVs. The field type was the main driver for the enrichment of fungal taxa, likely due to an imprint on soil microbiomes by the cultivated crop plants. This was shown by a higher fungal richness and different fungal community compositions comparing liverwort samples collected from pumpkin fields, with those from corn fields. In contrast, bacterial communities linked to liverworts are highly specialized and the soil attached to them is not a significant source of these bacteria. Specifically, enriched Cyanobacteria, Bacteroidetes and Methylobacteria suggest a symbiotic interaction. Intriguingly, compared to the surrounding soil, the thallus samples were shown to enrich several well-known bacterial and fungal phytopathogens indicating an undescribed role of liverworts as potential reservoirs of crop pathogens. CONCLUSIONS: Our results provide evidence that a stable bacterial community but varying fungal communities are colonizing liverwort thalli. Post-harvest, temporary agricultural biocrusts are important reservoirs for microbial biodiversity but they have to be considered as potential reservoirs for pathogens as well. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00501-0.
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spelling pubmed-102339972023-06-02 The microbiome of Riccia liverworts is an important reservoir for microbial diversity in temporary agricultural crusts Wicaksono, Wisnu Adi Semler, Bettina Pöltl, Martina Berg, Christian Berg, Gabriele Cernava, Tomislav Environ Microbiome Research BACKGROUND: The microbiota of liverworts provides an interesting model for plant symbioses; however, their microbiome assembly is not yet understood. Here, we assessed specific factors that shape microbial communities associated with Riccia temporary agricultural crusts in harvested fields by investigating bacterial, fungal and archaeal communities in thalli and adhering soil from different field sites in Styria and Burgenland, Austria combining qPCR analyses, amplicon sequencing and advanced microscopy. RESULTS: Riccia spec. div. was colonized by a very high abundance of bacteria (10(10) 16S rRNA gene copies per g of thallus) as well as archaea and fungi (10(8) ITS copies per g of thallus). Each Riccia thallus contain approx. 1000 prokaryotic and fungal ASVs. The field type was the main driver for the enrichment of fungal taxa, likely due to an imprint on soil microbiomes by the cultivated crop plants. This was shown by a higher fungal richness and different fungal community compositions comparing liverwort samples collected from pumpkin fields, with those from corn fields. In contrast, bacterial communities linked to liverworts are highly specialized and the soil attached to them is not a significant source of these bacteria. Specifically, enriched Cyanobacteria, Bacteroidetes and Methylobacteria suggest a symbiotic interaction. Intriguingly, compared to the surrounding soil, the thallus samples were shown to enrich several well-known bacterial and fungal phytopathogens indicating an undescribed role of liverworts as potential reservoirs of crop pathogens. CONCLUSIONS: Our results provide evidence that a stable bacterial community but varying fungal communities are colonizing liverwort thalli. Post-harvest, temporary agricultural biocrusts are important reservoirs for microbial biodiversity but they have to be considered as potential reservoirs for pathogens as well. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00501-0. BioMed Central 2023-06-01 /pmc/articles/PMC10233997/ /pubmed/37264474 http://dx.doi.org/10.1186/s40793-023-00501-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Wicaksono, Wisnu Adi
Semler, Bettina
Pöltl, Martina
Berg, Christian
Berg, Gabriele
Cernava, Tomislav
The microbiome of Riccia liverworts is an important reservoir for microbial diversity in temporary agricultural crusts
title The microbiome of Riccia liverworts is an important reservoir for microbial diversity in temporary agricultural crusts
title_full The microbiome of Riccia liverworts is an important reservoir for microbial diversity in temporary agricultural crusts
title_fullStr The microbiome of Riccia liverworts is an important reservoir for microbial diversity in temporary agricultural crusts
title_full_unstemmed The microbiome of Riccia liverworts is an important reservoir for microbial diversity in temporary agricultural crusts
title_short The microbiome of Riccia liverworts is an important reservoir for microbial diversity in temporary agricultural crusts
title_sort microbiome of riccia liverworts is an important reservoir for microbial diversity in temporary agricultural crusts
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10233997/
https://www.ncbi.nlm.nih.gov/pubmed/37264474
http://dx.doi.org/10.1186/s40793-023-00501-0
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