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Methane-Derived Carbon as a Driver for Cyanobacterial Growth

Methane, a potent greenhouse gas produced in freshwater ecosystems, can be used by methane-oxidizing bacteria (MOB) and can therefore subsidize the pelagic food web with energy and carbon. Consortia of MOB and photoautotrophs have been described in aquatic ecosystems and MOB can benefit from photoau...

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Autores principales: Cerbin, Slawek, Pérez, Germán, Rybak, Michał, Wejnerowski, Łukasz, Konowalczyk, Adam, Helmsing, Nico, Naus-Wiezer, Suzanne, Meima-Franke, Marion, Pytlak, Łukasz, Raaijmakers, Ciska, Nowak, Witold, Bodelier, Paul L. E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9010870/
https://www.ncbi.nlm.nih.gov/pubmed/35432228
http://dx.doi.org/10.3389/fmicb.2022.837198
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author Cerbin, Slawek
Pérez, Germán
Rybak, Michał
Wejnerowski, Łukasz
Konowalczyk, Adam
Helmsing, Nico
Naus-Wiezer, Suzanne
Meima-Franke, Marion
Pytlak, Łukasz
Raaijmakers, Ciska
Nowak, Witold
Bodelier, Paul L. E.
author_facet Cerbin, Slawek
Pérez, Germán
Rybak, Michał
Wejnerowski, Łukasz
Konowalczyk, Adam
Helmsing, Nico
Naus-Wiezer, Suzanne
Meima-Franke, Marion
Pytlak, Łukasz
Raaijmakers, Ciska
Nowak, Witold
Bodelier, Paul L. E.
author_sort Cerbin, Slawek
collection PubMed
description Methane, a potent greenhouse gas produced in freshwater ecosystems, can be used by methane-oxidizing bacteria (MOB) and can therefore subsidize the pelagic food web with energy and carbon. Consortia of MOB and photoautotrophs have been described in aquatic ecosystems and MOB can benefit from photoautotrophs which produce oxygen, thereby enhancing CH(4) oxidation. Methane oxidation can account for accumulation of inorganic carbon (i.e., CO(2)) and the release of exometabolites that may both be important factors influencing the structure of phytoplankton communities. The consortium of MOB and phototroph has been mainly studied for methane-removing biotechnologies, but there is still little information on the role of these interactions in freshwater ecosystems especially in the context of cyanobacterial growth and bloom development. We hypothesized that MOB could be an alternative C source to support cyanobacterial growth in freshwater systems. We detected low δ(13)C values in cyanobacterial blooms (the lowest detected value −59.97‰ for Planktothrix rubescens) what could be the result of the use of methane-derived carbon by cyanobacteria and/or MOB attached to their cells. We further proved the presence of metabolically active MOB on cyanobacterial filaments using the fluorescein isothiocyanate (FITC) based activity assay. The PCR results also proved the presence of the pmoA gene in several non-axenic cultures of cyanobacteria. Finally, experiments comprising the co-culture of the cyanobacterium Aphanizomenon gracile with the methanotroph Methylosinus sporium proved that cyanobacterial growth was significantly improved in the presence of MOB, presumably through utilizing CO(2) released by MOB. On the other hand, (13)C-CH(4) labeled incubations showed the uptake and assimilation of MOB-derived metabolites by the cyanobacterium. We also observed a higher growth of MOB in the presence of cyanobacteria under a higher irradiance regime, then when grown alone, underpinning the bidirectional influence with as of yet unknown environmental consequences.
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spelling pubmed-90108702022-04-16 Methane-Derived Carbon as a Driver for Cyanobacterial Growth Cerbin, Slawek Pérez, Germán Rybak, Michał Wejnerowski, Łukasz Konowalczyk, Adam Helmsing, Nico Naus-Wiezer, Suzanne Meima-Franke, Marion Pytlak, Łukasz Raaijmakers, Ciska Nowak, Witold Bodelier, Paul L. E. Front Microbiol Microbiology Methane, a potent greenhouse gas produced in freshwater ecosystems, can be used by methane-oxidizing bacteria (MOB) and can therefore subsidize the pelagic food web with energy and carbon. Consortia of MOB and photoautotrophs have been described in aquatic ecosystems and MOB can benefit from photoautotrophs which produce oxygen, thereby enhancing CH(4) oxidation. Methane oxidation can account for accumulation of inorganic carbon (i.e., CO(2)) and the release of exometabolites that may both be important factors influencing the structure of phytoplankton communities. The consortium of MOB and phototroph has been mainly studied for methane-removing biotechnologies, but there is still little information on the role of these interactions in freshwater ecosystems especially in the context of cyanobacterial growth and bloom development. We hypothesized that MOB could be an alternative C source to support cyanobacterial growth in freshwater systems. We detected low δ(13)C values in cyanobacterial blooms (the lowest detected value −59.97‰ for Planktothrix rubescens) what could be the result of the use of methane-derived carbon by cyanobacteria and/or MOB attached to their cells. We further proved the presence of metabolically active MOB on cyanobacterial filaments using the fluorescein isothiocyanate (FITC) based activity assay. The PCR results also proved the presence of the pmoA gene in several non-axenic cultures of cyanobacteria. Finally, experiments comprising the co-culture of the cyanobacterium Aphanizomenon gracile with the methanotroph Methylosinus sporium proved that cyanobacterial growth was significantly improved in the presence of MOB, presumably through utilizing CO(2) released by MOB. On the other hand, (13)C-CH(4) labeled incubations showed the uptake and assimilation of MOB-derived metabolites by the cyanobacterium. We also observed a higher growth of MOB in the presence of cyanobacteria under a higher irradiance regime, then when grown alone, underpinning the bidirectional influence with as of yet unknown environmental consequences. Frontiers Media S.A. 2022-04-01 /pmc/articles/PMC9010870/ /pubmed/35432228 http://dx.doi.org/10.3389/fmicb.2022.837198 Text en Copyright © 2022 Cerbin, Pérez, Rybak, Wejnerowski, Konowalczyk, Helmsing, Naus-Wiezer, Meima-Franke, Pytlak, Raaijmakers, Nowak and Bodelier. https://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
Cerbin, Slawek
Pérez, Germán
Rybak, Michał
Wejnerowski, Łukasz
Konowalczyk, Adam
Helmsing, Nico
Naus-Wiezer, Suzanne
Meima-Franke, Marion
Pytlak, Łukasz
Raaijmakers, Ciska
Nowak, Witold
Bodelier, Paul L. E.
Methane-Derived Carbon as a Driver for Cyanobacterial Growth
title Methane-Derived Carbon as a Driver for Cyanobacterial Growth
title_full Methane-Derived Carbon as a Driver for Cyanobacterial Growth
title_fullStr Methane-Derived Carbon as a Driver for Cyanobacterial Growth
title_full_unstemmed Methane-Derived Carbon as a Driver for Cyanobacterial Growth
title_short Methane-Derived Carbon as a Driver for Cyanobacterial Growth
title_sort methane-derived carbon as a driver for cyanobacterial growth
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9010870/
https://www.ncbi.nlm.nih.gov/pubmed/35432228
http://dx.doi.org/10.3389/fmicb.2022.837198
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