Cargando…

Utilization of low-molecular-weight organic compounds by the filterable fraction of a lotic microbiome

Filterable microorganisms participate in dissolved organic carbon (DOC) cycling in freshwater systems, however their exact functional role remains unknown. We determined the taxonomic identity and community dynamics of prokaryotic microbiomes in the 0.22 µm-filtered fraction and unfiltered freshwate...

Descripción completa

Detalles Bibliográficos
Autores principales: Ghuneim, Lydia-Ann J, Distaso, Marco A, Chernikova, Tatyana N, Bargiela, Rafael, Lunev, Evgenii A, Korzhenkov, Aleksei A, Toshchakov, Stepan V, Rojo, David, Barbas, Coral, Ferrer, Manuel, Golyshina, Olga V, Golyshin, Peter N, Jones, David L
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7864478/
https://www.ncbi.nlm.nih.gov/pubmed/33264383
http://dx.doi.org/10.1093/femsec/fiaa244
_version_ 1783647672332189696
author Ghuneim, Lydia-Ann J
Distaso, Marco A
Chernikova, Tatyana N
Bargiela, Rafael
Lunev, Evgenii A
Korzhenkov, Aleksei A
Toshchakov, Stepan V
Rojo, David
Barbas, Coral
Ferrer, Manuel
Golyshina, Olga V
Golyshin, Peter N
Jones, David L
author_facet Ghuneim, Lydia-Ann J
Distaso, Marco A
Chernikova, Tatyana N
Bargiela, Rafael
Lunev, Evgenii A
Korzhenkov, Aleksei A
Toshchakov, Stepan V
Rojo, David
Barbas, Coral
Ferrer, Manuel
Golyshina, Olga V
Golyshin, Peter N
Jones, David L
author_sort Ghuneim, Lydia-Ann J
collection PubMed
description Filterable microorganisms participate in dissolved organic carbon (DOC) cycling in freshwater systems, however their exact functional role remains unknown. We determined the taxonomic identity and community dynamics of prokaryotic microbiomes in the 0.22 µm-filtered fraction and unfiltered freshwater from the Conwy River (North Wales, UK) in microcosms and, using targeted metabolomics and (14)C-labelling, examined their role in the utilization of amino acids, organic acids and sugars spiked at environmentally-relevant (nanomolar) concentrations. To identify changes in community structure, we used 16S rRNA amplicon and shotgun sequencing. Unlike the unfiltered water samples where the consumption of DOC was rapid, the filtered fraction showed a 3-day lag phase before the consumption started. Analysis of functional categories of clusters of orthologous groups of proteins (COGs) showed that COGs associated with energy production increased in number in both fractions with substrate addition. The filtered fraction utilized low-molecular-weight (LMW) DOC at much slower rates than the whole community. Addition of nanomolar concentrations of LMW DOC did not measurably influence the composition of the microbial community nor the rate of consumption across all substrate types in either fraction. We conclude that due to their low activity, filterable microorganisms play a minor role in LMW DOC processing within a short residence time of lotic freshwater systems.
format Online
Article
Text
id pubmed-7864478
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-78644782021-02-10 Utilization of low-molecular-weight organic compounds by the filterable fraction of a lotic microbiome Ghuneim, Lydia-Ann J Distaso, Marco A Chernikova, Tatyana N Bargiela, Rafael Lunev, Evgenii A Korzhenkov, Aleksei A Toshchakov, Stepan V Rojo, David Barbas, Coral Ferrer, Manuel Golyshina, Olga V Golyshin, Peter N Jones, David L FEMS Microbiol Ecol Research Article Filterable microorganisms participate in dissolved organic carbon (DOC) cycling in freshwater systems, however their exact functional role remains unknown. We determined the taxonomic identity and community dynamics of prokaryotic microbiomes in the 0.22 µm-filtered fraction and unfiltered freshwater from the Conwy River (North Wales, UK) in microcosms and, using targeted metabolomics and (14)C-labelling, examined their role in the utilization of amino acids, organic acids and sugars spiked at environmentally-relevant (nanomolar) concentrations. To identify changes in community structure, we used 16S rRNA amplicon and shotgun sequencing. Unlike the unfiltered water samples where the consumption of DOC was rapid, the filtered fraction showed a 3-day lag phase before the consumption started. Analysis of functional categories of clusters of orthologous groups of proteins (COGs) showed that COGs associated with energy production increased in number in both fractions with substrate addition. The filtered fraction utilized low-molecular-weight (LMW) DOC at much slower rates than the whole community. Addition of nanomolar concentrations of LMW DOC did not measurably influence the composition of the microbial community nor the rate of consumption across all substrate types in either fraction. We conclude that due to their low activity, filterable microorganisms play a minor role in LMW DOC processing within a short residence time of lotic freshwater systems. Oxford University Press 2020-12-02 /pmc/articles/PMC7864478/ /pubmed/33264383 http://dx.doi.org/10.1093/femsec/fiaa244 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of FEMS. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Ghuneim, Lydia-Ann J
Distaso, Marco A
Chernikova, Tatyana N
Bargiela, Rafael
Lunev, Evgenii A
Korzhenkov, Aleksei A
Toshchakov, Stepan V
Rojo, David
Barbas, Coral
Ferrer, Manuel
Golyshina, Olga V
Golyshin, Peter N
Jones, David L
Utilization of low-molecular-weight organic compounds by the filterable fraction of a lotic microbiome
title Utilization of low-molecular-weight organic compounds by the filterable fraction of a lotic microbiome
title_full Utilization of low-molecular-weight organic compounds by the filterable fraction of a lotic microbiome
title_fullStr Utilization of low-molecular-weight organic compounds by the filterable fraction of a lotic microbiome
title_full_unstemmed Utilization of low-molecular-weight organic compounds by the filterable fraction of a lotic microbiome
title_short Utilization of low-molecular-weight organic compounds by the filterable fraction of a lotic microbiome
title_sort utilization of low-molecular-weight organic compounds by the filterable fraction of a lotic microbiome
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7864478/
https://www.ncbi.nlm.nih.gov/pubmed/33264383
http://dx.doi.org/10.1093/femsec/fiaa244
work_keys_str_mv AT ghuneimlydiaannj utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT distasomarcoa utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT chernikovatatyanan utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT bargielarafael utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT lunevevgeniia utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT korzhenkovalekseia utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT toshchakovstepanv utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT rojodavid utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT barbascoral utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT ferrermanuel utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT golyshinaolgav utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT golyshinpetern utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome
AT jonesdavidl utilizationoflowmolecularweightorganiccompoundsbythefilterablefractionofaloticmicrobiome