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Bacterial response to spatial gradients of algal-derived nutrients in a porous microplate

Photosynthetic microalgae are responsible for 50% of the global atmospheric CO(2) fixation into organic matter and hold potential as a renewable bioenergy source. Their metabolic interactions with the surrounding microbial community (the algal microbiome) play critical roles in carbon cycling, but d...

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Autores principales: Kim, Hyungseok, Kimbrel, Jeffrey A., Vaiana, Christopher A., Wollard, Jessica R., Mayali, Xavier, Buie, Cullen R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8940921/
https://www.ncbi.nlm.nih.gov/pubmed/34789844
http://dx.doi.org/10.1038/s41396-021-01147-x
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author Kim, Hyungseok
Kimbrel, Jeffrey A.
Vaiana, Christopher A.
Wollard, Jessica R.
Mayali, Xavier
Buie, Cullen R.
author_facet Kim, Hyungseok
Kimbrel, Jeffrey A.
Vaiana, Christopher A.
Wollard, Jessica R.
Mayali, Xavier
Buie, Cullen R.
author_sort Kim, Hyungseok
collection PubMed
description Photosynthetic microalgae are responsible for 50% of the global atmospheric CO(2) fixation into organic matter and hold potential as a renewable bioenergy source. Their metabolic interactions with the surrounding microbial community (the algal microbiome) play critical roles in carbon cycling, but due to methodological limitations, it has been challenging to examine how community development is influenced by spatial proximity to their algal host. Here we introduce a copolymer-based porous microplate to co-culture algae and bacteria, where metabolites are constantly exchanged between the microorganisms while maintaining physical separation. In the microplate, we found that the diatom Phaeodactylum tricornutum accumulated to cell abundances ~20 fold higher than under normal batch conditions due to constant replenishment of nutrients through the porous structure. We also demonstrate that algal-associated bacteria, both single isolates and complex communities, responded to inorganic nutrients away from their host as well as organic nutrients originating from the algae in a spatially predictable manner. These experimental findings coupled with a mathematical model suggest that host proximity and algal culture growth phase impact bacterial community development in a taxon-specific manner through organic and inorganic nutrient availability. Our novel system presents a useful tool to investigate universal metabolic interactions between microbes in aquatic ecosystems.
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spelling pubmed-89409212022-04-08 Bacterial response to spatial gradients of algal-derived nutrients in a porous microplate Kim, Hyungseok Kimbrel, Jeffrey A. Vaiana, Christopher A. Wollard, Jessica R. Mayali, Xavier Buie, Cullen R. ISME J Article Photosynthetic microalgae are responsible for 50% of the global atmospheric CO(2) fixation into organic matter and hold potential as a renewable bioenergy source. Their metabolic interactions with the surrounding microbial community (the algal microbiome) play critical roles in carbon cycling, but due to methodological limitations, it has been challenging to examine how community development is influenced by spatial proximity to their algal host. Here we introduce a copolymer-based porous microplate to co-culture algae and bacteria, where metabolites are constantly exchanged between the microorganisms while maintaining physical separation. In the microplate, we found that the diatom Phaeodactylum tricornutum accumulated to cell abundances ~20 fold higher than under normal batch conditions due to constant replenishment of nutrients through the porous structure. We also demonstrate that algal-associated bacteria, both single isolates and complex communities, responded to inorganic nutrients away from their host as well as organic nutrients originating from the algae in a spatially predictable manner. These experimental findings coupled with a mathematical model suggest that host proximity and algal culture growth phase impact bacterial community development in a taxon-specific manner through organic and inorganic nutrient availability. Our novel system presents a useful tool to investigate universal metabolic interactions between microbes in aquatic ecosystems. Nature Publishing Group UK 2021-11-17 2022-04 /pmc/articles/PMC8940921/ /pubmed/34789844 http://dx.doi.org/10.1038/s41396-021-01147-x Text en © The Author(s) 2021 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Kim, Hyungseok
Kimbrel, Jeffrey A.
Vaiana, Christopher A.
Wollard, Jessica R.
Mayali, Xavier
Buie, Cullen R.
Bacterial response to spatial gradients of algal-derived nutrients in a porous microplate
title Bacterial response to spatial gradients of algal-derived nutrients in a porous microplate
title_full Bacterial response to spatial gradients of algal-derived nutrients in a porous microplate
title_fullStr Bacterial response to spatial gradients of algal-derived nutrients in a porous microplate
title_full_unstemmed Bacterial response to spatial gradients of algal-derived nutrients in a porous microplate
title_short Bacterial response to spatial gradients of algal-derived nutrients in a porous microplate
title_sort bacterial response to spatial gradients of algal-derived nutrients in a porous microplate
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8940921/
https://www.ncbi.nlm.nih.gov/pubmed/34789844
http://dx.doi.org/10.1038/s41396-021-01147-x
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