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High-resolution metagenomic reconstruction of the freshwater spring bloom

BACKGROUND: The phytoplankton spring bloom in freshwater habitats is a complex, recurring, and dynamic ecological spectacle that unfolds at multiple biological scales. Although enormous taxonomic shifts in microbial assemblages during and after the bloom have been reported, genomic information on th...

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Autores principales: Kavagutti, Vinicius S., Bulzu, Paul-Adrian, Chiriac, Cecilia M., Salcher, Michaela M., Mukherjee, Indranil, Shabarova, Tanja, Grujčić, Vesna, Mehrshad, Maliheh, Kasalický, Vojtěch, Andrei, Adrian-Stefan, Jezberová, Jitka, Seďa, Jaromir, Rychtecký, Pavel, Znachor, Petr, Šimek, Karel, Ghai, Rohit
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9878933/
https://www.ncbi.nlm.nih.gov/pubmed/36698172
http://dx.doi.org/10.1186/s40168-022-01451-4
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author Kavagutti, Vinicius S.
Bulzu, Paul-Adrian
Chiriac, Cecilia M.
Salcher, Michaela M.
Mukherjee, Indranil
Shabarova, Tanja
Grujčić, Vesna
Mehrshad, Maliheh
Kasalický, Vojtěch
Andrei, Adrian-Stefan
Jezberová, Jitka
Seďa, Jaromir
Rychtecký, Pavel
Znachor, Petr
Šimek, Karel
Ghai, Rohit
author_facet Kavagutti, Vinicius S.
Bulzu, Paul-Adrian
Chiriac, Cecilia M.
Salcher, Michaela M.
Mukherjee, Indranil
Shabarova, Tanja
Grujčić, Vesna
Mehrshad, Maliheh
Kasalický, Vojtěch
Andrei, Adrian-Stefan
Jezberová, Jitka
Seďa, Jaromir
Rychtecký, Pavel
Znachor, Petr
Šimek, Karel
Ghai, Rohit
author_sort Kavagutti, Vinicius S.
collection PubMed
description BACKGROUND: The phytoplankton spring bloom in freshwater habitats is a complex, recurring, and dynamic ecological spectacle that unfolds at multiple biological scales. Although enormous taxonomic shifts in microbial assemblages during and after the bloom have been reported, genomic information on the microbial community of the spring bloom remains scarce. RESULTS: We performed a high-resolution spatio-temporal sampling of the spring bloom in a freshwater reservoir and describe a multitude of previously unknown taxa using metagenome-assembled genomes of eukaryotes, prokaryotes, and viruses in combination with a broad array of methodologies. The recovered genomes reveal multiple distributional dynamics for several bacterial groups with progressively increasing stratification. Analyses of abundances of metagenome-assembled genomes in concert with CARD-FISH revealed remarkably similar in situ doubling time estimates for dominant genome-streamlined microbial lineages. Discordance between quantitations of cryptophytes arising from sequence data and microscopic identification suggested the presence of hidden, yet extremely abundant aplastidic cryptophytes that were confirmed by CARD-FISH analyses. Aplastidic cryptophytes are prevalent throughout the water column but have never been considered in prior models of plankton dynamics. We also recovered the first metagenomic-assembled genomes of freshwater protists (a diatom and a haptophyte) along with thousands of giant viral genomic contigs, some of which appeared similar to viruses infecting haptophytes but owing to lack of known representatives, most remained without any indication of their hosts. The contrasting distribution of giant viruses that are present in the entire water column to that of parasitic perkinsids residing largely in deeper waters allows us to propose giant viruses as the biological agents of top-down control and bloom collapse, likely in combination with bottom-up factors like a nutrient limitation. CONCLUSION: We reconstructed thousands of genomes of microbes and viruses from a freshwater spring bloom and show that such large-scale genome recovery allows tracking of planktonic succession in great detail. However, integration of metagenomic information with other methodologies (e.g., microscopy, CARD-FISH) remains critical to reveal diverse phenomena (e.g., distributional patterns, in situ doubling times) and novel participants (e.g., aplastidic cryptophytes) and to further refine existing ecological models (e.g., factors affecting bloom collapse). This work provides a genomic foundation for future approaches towards a fine-scale characterization of the organisms in relation to the rapidly changing environment during the course of the freshwater spring bloom. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01451-4.
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spelling pubmed-98789332023-01-27 High-resolution metagenomic reconstruction of the freshwater spring bloom Kavagutti, Vinicius S. Bulzu, Paul-Adrian Chiriac, Cecilia M. Salcher, Michaela M. Mukherjee, Indranil Shabarova, Tanja Grujčić, Vesna Mehrshad, Maliheh Kasalický, Vojtěch Andrei, Adrian-Stefan Jezberová, Jitka Seďa, Jaromir Rychtecký, Pavel Znachor, Petr Šimek, Karel Ghai, Rohit Microbiome Research BACKGROUND: The phytoplankton spring bloom in freshwater habitats is a complex, recurring, and dynamic ecological spectacle that unfolds at multiple biological scales. Although enormous taxonomic shifts in microbial assemblages during and after the bloom have been reported, genomic information on the microbial community of the spring bloom remains scarce. RESULTS: We performed a high-resolution spatio-temporal sampling of the spring bloom in a freshwater reservoir and describe a multitude of previously unknown taxa using metagenome-assembled genomes of eukaryotes, prokaryotes, and viruses in combination with a broad array of methodologies. The recovered genomes reveal multiple distributional dynamics for several bacterial groups with progressively increasing stratification. Analyses of abundances of metagenome-assembled genomes in concert with CARD-FISH revealed remarkably similar in situ doubling time estimates for dominant genome-streamlined microbial lineages. Discordance between quantitations of cryptophytes arising from sequence data and microscopic identification suggested the presence of hidden, yet extremely abundant aplastidic cryptophytes that were confirmed by CARD-FISH analyses. Aplastidic cryptophytes are prevalent throughout the water column but have never been considered in prior models of plankton dynamics. We also recovered the first metagenomic-assembled genomes of freshwater protists (a diatom and a haptophyte) along with thousands of giant viral genomic contigs, some of which appeared similar to viruses infecting haptophytes but owing to lack of known representatives, most remained without any indication of their hosts. The contrasting distribution of giant viruses that are present in the entire water column to that of parasitic perkinsids residing largely in deeper waters allows us to propose giant viruses as the biological agents of top-down control and bloom collapse, likely in combination with bottom-up factors like a nutrient limitation. CONCLUSION: We reconstructed thousands of genomes of microbes and viruses from a freshwater spring bloom and show that such large-scale genome recovery allows tracking of planktonic succession in great detail. However, integration of metagenomic information with other methodologies (e.g., microscopy, CARD-FISH) remains critical to reveal diverse phenomena (e.g., distributional patterns, in situ doubling times) and novel participants (e.g., aplastidic cryptophytes) and to further refine existing ecological models (e.g., factors affecting bloom collapse). This work provides a genomic foundation for future approaches towards a fine-scale characterization of the organisms in relation to the rapidly changing environment during the course of the freshwater spring bloom. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01451-4. BioMed Central 2023-01-26 /pmc/articles/PMC9878933/ /pubmed/36698172 http://dx.doi.org/10.1186/s40168-022-01451-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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
Kavagutti, Vinicius S.
Bulzu, Paul-Adrian
Chiriac, Cecilia M.
Salcher, Michaela M.
Mukherjee, Indranil
Shabarova, Tanja
Grujčić, Vesna
Mehrshad, Maliheh
Kasalický, Vojtěch
Andrei, Adrian-Stefan
Jezberová, Jitka
Seďa, Jaromir
Rychtecký, Pavel
Znachor, Petr
Šimek, Karel
Ghai, Rohit
High-resolution metagenomic reconstruction of the freshwater spring bloom
title High-resolution metagenomic reconstruction of the freshwater spring bloom
title_full High-resolution metagenomic reconstruction of the freshwater spring bloom
title_fullStr High-resolution metagenomic reconstruction of the freshwater spring bloom
title_full_unstemmed High-resolution metagenomic reconstruction of the freshwater spring bloom
title_short High-resolution metagenomic reconstruction of the freshwater spring bloom
title_sort high-resolution metagenomic reconstruction of the freshwater spring bloom
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9878933/
https://www.ncbi.nlm.nih.gov/pubmed/36698172
http://dx.doi.org/10.1186/s40168-022-01451-4
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