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Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability

Bacterioplankton consume about half of the dissolved organic matter (DOM) produced by phytoplankton. DOM released from phytoplankton consists of a myriad of compounds that span a range of biological reactivity from labile to recalcitrant. Linking specific bacterioplankton lineages to the incorporati...

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Autores principales: Liu, Shuting, Baetge, Nicholas, Comstock, Jacqueline, Opalk, Keri, Parsons, Rachel, Halewood, Elisa, English, Chance J., Giovannoni, Stephen, Bolaños, Luis M., Nelson, Craig E., Vergin, Kevin, Carlson, Craig A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7575717/
https://www.ncbi.nlm.nih.gov/pubmed/33117322
http://dx.doi.org/10.3389/fmicb.2020.580397
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author Liu, Shuting
Baetge, Nicholas
Comstock, Jacqueline
Opalk, Keri
Parsons, Rachel
Halewood, Elisa
English, Chance J.
Giovannoni, Stephen
Bolaños, Luis M.
Nelson, Craig E.
Vergin, Kevin
Carlson, Craig A.
author_facet Liu, Shuting
Baetge, Nicholas
Comstock, Jacqueline
Opalk, Keri
Parsons, Rachel
Halewood, Elisa
English, Chance J.
Giovannoni, Stephen
Bolaños, Luis M.
Nelson, Craig E.
Vergin, Kevin
Carlson, Craig A.
author_sort Liu, Shuting
collection PubMed
description Bacterioplankton consume about half of the dissolved organic matter (DOM) produced by phytoplankton. DOM released from phytoplankton consists of a myriad of compounds that span a range of biological reactivity from labile to recalcitrant. Linking specific bacterioplankton lineages to the incorporation of DOM compounds into biomass is important to understand microbial niche partitioning. We conducted a series of DNA-stable isotope probing (SIP) experiments using (13)C-labeled substrates of varying lability including amino acids, cyanobacteria lysate, and DOM from diatom and cyanobacteria isolates concentrated on solid phase extraction PPL columns (SPE-DOM). Amendments of substrates into Sargasso Sea bacterioplankton communities were conducted to explore microbial response and DNA-SIP was used to determine which lineages of Bacteria and Archaea were responsible for uptake and incorporation. Greater increases in bacterioplankton abundance and DOC removal were observed in incubations amended with cyanobacteria-derived lysate and amino acids compared to the SPE-DOM, suggesting that the latter retained proportionally more recalcitrant DOM compounds. DOM across a range of bioavailability was utilized by diverse prokaryotic taxa with copiotrophs becoming the most abundant (13)C-incorporating taxa in the amino acid treatment and oligotrophs becoming the most abundant (13)C-incorporating taxa in SPE-DOM treatments. The lineages that responded to SPE-DOM amendments were also prevalent in the mesopelagic of the Sargasso Sea, suggesting that PPL extraction of phytoplankton-derived DOM isolates compounds of ecological relevance to oligotrophic heterotrophic bacterioplankton. Our study indicates that DOM quality is an important factor controlling the diversity of the microbial community response, providing insights into the roles of different bacterioplankton in resource exploitation and efficiency of marine carbon cycling.
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spelling pubmed-75757172020-10-27 Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability Liu, Shuting Baetge, Nicholas Comstock, Jacqueline Opalk, Keri Parsons, Rachel Halewood, Elisa English, Chance J. Giovannoni, Stephen Bolaños, Luis M. Nelson, Craig E. Vergin, Kevin Carlson, Craig A. Front Microbiol Microbiology Bacterioplankton consume about half of the dissolved organic matter (DOM) produced by phytoplankton. DOM released from phytoplankton consists of a myriad of compounds that span a range of biological reactivity from labile to recalcitrant. Linking specific bacterioplankton lineages to the incorporation of DOM compounds into biomass is important to understand microbial niche partitioning. We conducted a series of DNA-stable isotope probing (SIP) experiments using (13)C-labeled substrates of varying lability including amino acids, cyanobacteria lysate, and DOM from diatom and cyanobacteria isolates concentrated on solid phase extraction PPL columns (SPE-DOM). Amendments of substrates into Sargasso Sea bacterioplankton communities were conducted to explore microbial response and DNA-SIP was used to determine which lineages of Bacteria and Archaea were responsible for uptake and incorporation. Greater increases in bacterioplankton abundance and DOC removal were observed in incubations amended with cyanobacteria-derived lysate and amino acids compared to the SPE-DOM, suggesting that the latter retained proportionally more recalcitrant DOM compounds. DOM across a range of bioavailability was utilized by diverse prokaryotic taxa with copiotrophs becoming the most abundant (13)C-incorporating taxa in the amino acid treatment and oligotrophs becoming the most abundant (13)C-incorporating taxa in SPE-DOM treatments. The lineages that responded to SPE-DOM amendments were also prevalent in the mesopelagic of the Sargasso Sea, suggesting that PPL extraction of phytoplankton-derived DOM isolates compounds of ecological relevance to oligotrophic heterotrophic bacterioplankton. Our study indicates that DOM quality is an important factor controlling the diversity of the microbial community response, providing insights into the roles of different bacterioplankton in resource exploitation and efficiency of marine carbon cycling. Frontiers Media S.A. 2020-10-07 /pmc/articles/PMC7575717/ /pubmed/33117322 http://dx.doi.org/10.3389/fmicb.2020.580397 Text en Copyright © 2020 Liu, Baetge, Comstock, Opalk, Parsons, Halewood, English, Giovannoni, Bolaños, Nelson, Vergin and Carlson. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Liu, Shuting
Baetge, Nicholas
Comstock, Jacqueline
Opalk, Keri
Parsons, Rachel
Halewood, Elisa
English, Chance J.
Giovannoni, Stephen
Bolaños, Luis M.
Nelson, Craig E.
Vergin, Kevin
Carlson, Craig A.
Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability
title Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability
title_full Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability
title_fullStr Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability
title_full_unstemmed Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability
title_short Stable Isotope Probing Identifies Bacterioplankton Lineages Capable of Utilizing Dissolved Organic Matter Across a Range of Bioavailability
title_sort stable isotope probing identifies bacterioplankton lineages capable of utilizing dissolved organic matter across a range of bioavailability
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7575717/
https://www.ncbi.nlm.nih.gov/pubmed/33117322
http://dx.doi.org/10.3389/fmicb.2020.580397
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