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Dynamics of a methanol-fed marine denitrifying biofilm: 2—impact of environmental changes on the microbial community

BACKGROUND: The biofilm of a methanol-fed, marine denitrification system is composed of a multi-species microbial community, among which Hyphomicrobium nitrativorans and Methylophaga nitratireducenticrescens are the principal bacteria involved in the denitrifying activities. To assess its resilience...

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Autores principales: Villemur, Richard, Payette, Geneviève, Geoffroy, Valérie, Mauffrey, Florian, Martineau, Christine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697039/
https://www.ncbi.nlm.nih.gov/pubmed/31423359
http://dx.doi.org/10.7717/peerj.7467
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author Villemur, Richard
Payette, Geneviève
Geoffroy, Valérie
Mauffrey, Florian
Martineau, Christine
author_facet Villemur, Richard
Payette, Geneviève
Geoffroy, Valérie
Mauffrey, Florian
Martineau, Christine
author_sort Villemur, Richard
collection PubMed
description BACKGROUND: The biofilm of a methanol-fed, marine denitrification system is composed of a multi-species microbial community, among which Hyphomicrobium nitrativorans and Methylophaga nitratireducenticrescens are the principal bacteria involved in the denitrifying activities. To assess its resilience to environmental changes, the biofilm was cultivated in artificial seawater (ASW) under anoxic conditions and exposed to a range of specific environmental conditions. We previously reported the impact of these changes on the denitrifying activities and the co-occurrence of H. nitrativorans strain NL23 and M. nitratireducenticrescens in the biofilm cultures. Here, we report the impact of these changes on the dynamics of the overall microbial community of the denitrifying biofilm. METHODS: The original biofilm (OB) taken from the denitrification system was cultivated in ASW under anoxic conditions with a range of NaCl concentrations, and with four combinations of nitrate/methanol concentrations and temperatures. The OB was also cultivated in the commercial Instant Ocean seawater (IO). The bacterial diversity of the biofilm cultures and the OB was determined by 16S ribosomal RNA gene sequences. Culture approach was used to isolate other denitrifying bacteria from the biofilm cultures. The metatranscriptomes of selected biofilm cultures were derived, along with the transcriptomes of planktonic pure cultures of H. nitrativorans strain NL23 and M. nitratireducenticrescens strain GP59. RESULTS: High proportions of M. nitratireducenticrescens occurred in the biofilm cultures. H. nitrativorans strain NL23 was found in high proportion in the OB, but was absent in the biofilm cultures cultivated in the ASW medium at 2.75% NaCl. It was found however in low proportions in the biofilm cultures cultivated in the ASW medium at 0–1% NaCl and in the IO biofilm cultures. Denitrifying bacterial isolates affiliated to Marinobacter spp. and Paracoccus spp. were isolated. Up regulation of the denitrification genes of strains GP59 and NL23 occurred in the biofilm cultures compared to the planktonic pure cultures. Denitrifying bacteria affiliated to the Stappia spp. were metabolically active in the biofilm cultures. CONCLUSIONS: These results illustrate the dynamics of the microbial community in the denitrifying biofilm cultures in adapting to different environmental conditions. The NaCl concentration is an important factor affecting the microbial community in the biofilm cultures. Up regulation of the denitrification genes of M. nitratireducenticrescens strain GP59 and H. nitrativorans strain NL23 in the biofilm cultures suggests different mechanisms of regulation of the denitrification pathway in the biofilm. Other denitrifying heterotrophic bacteria are present in low proportions, suggesting that the biofilm has the potential to adapt to heterotrophic, non-methylotrophic environments.
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spelling pubmed-66970392019-08-16 Dynamics of a methanol-fed marine denitrifying biofilm: 2—impact of environmental changes on the microbial community Villemur, Richard Payette, Geneviève Geoffroy, Valérie Mauffrey, Florian Martineau, Christine PeerJ Biodiversity BACKGROUND: The biofilm of a methanol-fed, marine denitrification system is composed of a multi-species microbial community, among which Hyphomicrobium nitrativorans and Methylophaga nitratireducenticrescens are the principal bacteria involved in the denitrifying activities. To assess its resilience to environmental changes, the biofilm was cultivated in artificial seawater (ASW) under anoxic conditions and exposed to a range of specific environmental conditions. We previously reported the impact of these changes on the denitrifying activities and the co-occurrence of H. nitrativorans strain NL23 and M. nitratireducenticrescens in the biofilm cultures. Here, we report the impact of these changes on the dynamics of the overall microbial community of the denitrifying biofilm. METHODS: The original biofilm (OB) taken from the denitrification system was cultivated in ASW under anoxic conditions with a range of NaCl concentrations, and with four combinations of nitrate/methanol concentrations and temperatures. The OB was also cultivated in the commercial Instant Ocean seawater (IO). The bacterial diversity of the biofilm cultures and the OB was determined by 16S ribosomal RNA gene sequences. Culture approach was used to isolate other denitrifying bacteria from the biofilm cultures. The metatranscriptomes of selected biofilm cultures were derived, along with the transcriptomes of planktonic pure cultures of H. nitrativorans strain NL23 and M. nitratireducenticrescens strain GP59. RESULTS: High proportions of M. nitratireducenticrescens occurred in the biofilm cultures. H. nitrativorans strain NL23 was found in high proportion in the OB, but was absent in the biofilm cultures cultivated in the ASW medium at 2.75% NaCl. It was found however in low proportions in the biofilm cultures cultivated in the ASW medium at 0–1% NaCl and in the IO biofilm cultures. Denitrifying bacterial isolates affiliated to Marinobacter spp. and Paracoccus spp. were isolated. Up regulation of the denitrification genes of strains GP59 and NL23 occurred in the biofilm cultures compared to the planktonic pure cultures. Denitrifying bacteria affiliated to the Stappia spp. were metabolically active in the biofilm cultures. CONCLUSIONS: These results illustrate the dynamics of the microbial community in the denitrifying biofilm cultures in adapting to different environmental conditions. The NaCl concentration is an important factor affecting the microbial community in the biofilm cultures. Up regulation of the denitrification genes of M. nitratireducenticrescens strain GP59 and H. nitrativorans strain NL23 in the biofilm cultures suggests different mechanisms of regulation of the denitrification pathway in the biofilm. Other denitrifying heterotrophic bacteria are present in low proportions, suggesting that the biofilm has the potential to adapt to heterotrophic, non-methylotrophic environments. PeerJ Inc. 2019-08-13 /pmc/articles/PMC6697039/ /pubmed/31423359 http://dx.doi.org/10.7717/peerj.7467 Text en ©2019 Villemur et al. https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Biodiversity
Villemur, Richard
Payette, Geneviève
Geoffroy, Valérie
Mauffrey, Florian
Martineau, Christine
Dynamics of a methanol-fed marine denitrifying biofilm: 2—impact of environmental changes on the microbial community
title Dynamics of a methanol-fed marine denitrifying biofilm: 2—impact of environmental changes on the microbial community
title_full Dynamics of a methanol-fed marine denitrifying biofilm: 2—impact of environmental changes on the microbial community
title_fullStr Dynamics of a methanol-fed marine denitrifying biofilm: 2—impact of environmental changes on the microbial community
title_full_unstemmed Dynamics of a methanol-fed marine denitrifying biofilm: 2—impact of environmental changes on the microbial community
title_short Dynamics of a methanol-fed marine denitrifying biofilm: 2—impact of environmental changes on the microbial community
title_sort dynamics of a methanol-fed marine denitrifying biofilm: 2—impact of environmental changes on the microbial community
topic Biodiversity
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697039/
https://www.ncbi.nlm.nih.gov/pubmed/31423359
http://dx.doi.org/10.7717/peerj.7467
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