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Bacterioplankton Communities in Dissolved Organic Carbon-Rich Amazonian Black Water

The Amazon River basin sustains dramatic hydrochemical gradients defined by three water types: white, clear, and black waters. In black water, important loads of allochthonous humic dissolved organic matter (DOM) result from the bacterioplankton degradation of plant lignin. However, the bacterial ta...

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Autores principales: Sylvain, François-Étienne, Bouslama, Sidki, Holland, Aleicia, Leroux, Nicolas, Mercier, Pierre-Luc, Val, Adalberto Luis, Derome, Nicolas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10269884/
https://www.ncbi.nlm.nih.gov/pubmed/37199657
http://dx.doi.org/10.1128/spectrum.04793-22
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author Sylvain, François-Étienne
Bouslama, Sidki
Holland, Aleicia
Leroux, Nicolas
Mercier, Pierre-Luc
Val, Adalberto Luis
Derome, Nicolas
author_facet Sylvain, François-Étienne
Bouslama, Sidki
Holland, Aleicia
Leroux, Nicolas
Mercier, Pierre-Luc
Val, Adalberto Luis
Derome, Nicolas
author_sort Sylvain, François-Étienne
collection PubMed
description The Amazon River basin sustains dramatic hydrochemical gradients defined by three water types: white, clear, and black waters. In black water, important loads of allochthonous humic dissolved organic matter (DOM) result from the bacterioplankton degradation of plant lignin. However, the bacterial taxa involved in this process remain unknown, since Amazonian bacterioplankton has been poorly studied. Its characterization could lead to a better understanding of the carbon cycle in one of the Earth’s most productive hydrological systems. Our study characterized the taxonomic structure and functions of Amazonian bacterioplankton to better understand the interplay between this community and humic DOM. We conducted a field sampling campaign comprising 15 sites distributed across the three main Amazonian water types (representing a gradient of humic DOM), and a 16S rRNA metabarcoding analysis based on bacterioplankton DNA and RNA extracts. Bacterioplankton functions were inferred using 16S rRNA data in combination with a tailored functional database from 90 Amazonian basin shotgun metagenomes from the literature. We discovered that the relative abundances of fluorescent DOM fractions (humic-, fulvic-, and protein-like) were major drivers of bacterioplankton structure. We identified 36 genera for which the relative abundance was significantly correlated with humic DOM. The strongest correlations were found in the Polynucleobacter, Methylobacterium, and Acinetobacter genera, three low abundant but omnipresent taxa that possessed several genes involved in the main steps of the β-aryl ether enzymatic degradation pathway of diaryl humic DOM residues. Overall, this study identified key taxa with DOM degradation genomic potential, the involvement of which in allochthonous Amazonian carbon transformation and sequestration merits further investigation. IMPORTANCE The Amazon basin discharge carries an important load of terrestrially derived dissolved organic matter (DOM) to the ocean. The bacterioplankton from this basin potentially plays important roles in transforming this allochthonous carbon, which has consequences on marine primary productivity and global carbon sequestration. However, the structure and function of Amazonian bacterioplanktonic communities remain poorly studied, and their interactions with DOM are unresolved. In this study, we (i) sampled bacterioplankton in all the main Amazon tributaries, (ii) combined information from the taxonomic structure and functional repertory of Amazonian bacterioplankton communities to understand their dynamics, (iii) identified the main physicochemical parameters shaping bacterioplanktonic communities among a set of >30 measured environmental parameters, and (iv) characterized how bacterioplankton structure varies according to the relative abundance of humic compounds, a by-product from the bacterial degradation process of allochthonous DOM.
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spelling pubmed-102698842023-06-16 Bacterioplankton Communities in Dissolved Organic Carbon-Rich Amazonian Black Water Sylvain, François-Étienne Bouslama, Sidki Holland, Aleicia Leroux, Nicolas Mercier, Pierre-Luc Val, Adalberto Luis Derome, Nicolas Microbiol Spectr Research Article The Amazon River basin sustains dramatic hydrochemical gradients defined by three water types: white, clear, and black waters. In black water, important loads of allochthonous humic dissolved organic matter (DOM) result from the bacterioplankton degradation of plant lignin. However, the bacterial taxa involved in this process remain unknown, since Amazonian bacterioplankton has been poorly studied. Its characterization could lead to a better understanding of the carbon cycle in one of the Earth’s most productive hydrological systems. Our study characterized the taxonomic structure and functions of Amazonian bacterioplankton to better understand the interplay between this community and humic DOM. We conducted a field sampling campaign comprising 15 sites distributed across the three main Amazonian water types (representing a gradient of humic DOM), and a 16S rRNA metabarcoding analysis based on bacterioplankton DNA and RNA extracts. Bacterioplankton functions were inferred using 16S rRNA data in combination with a tailored functional database from 90 Amazonian basin shotgun metagenomes from the literature. We discovered that the relative abundances of fluorescent DOM fractions (humic-, fulvic-, and protein-like) were major drivers of bacterioplankton structure. We identified 36 genera for which the relative abundance was significantly correlated with humic DOM. The strongest correlations were found in the Polynucleobacter, Methylobacterium, and Acinetobacter genera, three low abundant but omnipresent taxa that possessed several genes involved in the main steps of the β-aryl ether enzymatic degradation pathway of diaryl humic DOM residues. Overall, this study identified key taxa with DOM degradation genomic potential, the involvement of which in allochthonous Amazonian carbon transformation and sequestration merits further investigation. IMPORTANCE The Amazon basin discharge carries an important load of terrestrially derived dissolved organic matter (DOM) to the ocean. The bacterioplankton from this basin potentially plays important roles in transforming this allochthonous carbon, which has consequences on marine primary productivity and global carbon sequestration. However, the structure and function of Amazonian bacterioplanktonic communities remain poorly studied, and their interactions with DOM are unresolved. In this study, we (i) sampled bacterioplankton in all the main Amazon tributaries, (ii) combined information from the taxonomic structure and functional repertory of Amazonian bacterioplankton communities to understand their dynamics, (iii) identified the main physicochemical parameters shaping bacterioplanktonic communities among a set of >30 measured environmental parameters, and (iv) characterized how bacterioplankton structure varies according to the relative abundance of humic compounds, a by-product from the bacterial degradation process of allochthonous DOM. American Society for Microbiology 2023-05-18 /pmc/articles/PMC10269884/ /pubmed/37199657 http://dx.doi.org/10.1128/spectrum.04793-22 Text en Copyright © 2023 Sylvain et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Sylvain, François-Étienne
Bouslama, Sidki
Holland, Aleicia
Leroux, Nicolas
Mercier, Pierre-Luc
Val, Adalberto Luis
Derome, Nicolas
Bacterioplankton Communities in Dissolved Organic Carbon-Rich Amazonian Black Water
title Bacterioplankton Communities in Dissolved Organic Carbon-Rich Amazonian Black Water
title_full Bacterioplankton Communities in Dissolved Organic Carbon-Rich Amazonian Black Water
title_fullStr Bacterioplankton Communities in Dissolved Organic Carbon-Rich Amazonian Black Water
title_full_unstemmed Bacterioplankton Communities in Dissolved Organic Carbon-Rich Amazonian Black Water
title_short Bacterioplankton Communities in Dissolved Organic Carbon-Rich Amazonian Black Water
title_sort bacterioplankton communities in dissolved organic carbon-rich amazonian black water
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10269884/
https://www.ncbi.nlm.nih.gov/pubmed/37199657
http://dx.doi.org/10.1128/spectrum.04793-22
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