Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece
Marine nitrogen-fixing cyanobacteria are largely confined to the tropical and subtropical ocean. It has been argued that their global biogeographical distribution reflects the physiologically feasible temperature range at which they can perform nitrogen fixation. In this study we refine this line of...
Published in: | The ISME Journal |
---|---|
Main Authors: | , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
2013
|
Subjects: | |
Online Access: | https://hdl.handle.net/11370/da3b9ab8-07ff-482e-b811-c335be7c311c https://research.rug.nl/en/publications/da3b9ab8-07ff-482e-b811-c335be7c311c https://doi.org/10.1038/ismej.2013.103 |
id |
ftunigroningenpu:oai:pure.rug.nl:publications/da3b9ab8-07ff-482e-b811-c335be7c311c |
---|---|
record_format |
openpolar |
spelling |
ftunigroningenpu:oai:pure.rug.nl:publications/da3b9ab8-07ff-482e-b811-c335be7c311c 2024-06-02T08:11:35+00:00 Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece Brauer, Verena S. Stomp, Maayke Rosso, Camillo van Beusekom, Sebastiaan A. M. Emmerich, Barbara Stal, Lucas J. Huisman, Jef 2013-11 https://hdl.handle.net/11370/da3b9ab8-07ff-482e-b811-c335be7c311c https://research.rug.nl/en/publications/da3b9ab8-07ff-482e-b811-c335be7c311c https://doi.org/10.1038/ismej.2013.103 eng eng https://research.rug.nl/en/publications/da3b9ab8-07ff-482e-b811-c335be7c311c info:eu-repo/semantics/closedAccess Brauer , V S , Stomp , M , Rosso , C , van Beusekom , S A M , Emmerich , B , Stal , L J & Huisman , J 2013 , ' Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece ' , ISME Journal , vol. 7 , no. 11 , pp. 2105-2115 . https://doi.org/10.1038/ismej.2013.103 climate change day-night cycle nitrogenase nitrogen fixation respiration unicellular cyanobacteria TROPICAL NORTH-ATLANTIC SP STRAIN ATCC-51142 DIAZOTROPHIC CYANOBACTERIUM FIXING CYANOBACTERIA PACIFIC-OCEAN N-2 FIXATION LIGHT-DARK ATCC 51142 TRANSCRIPTIONAL ANALYSIS CROCOSPHAERA-WATSONII article 2013 ftunigroningenpu https://doi.org/10.1038/ismej.2013.103 2024-05-07T19:05:36Z Marine nitrogen-fixing cyanobacteria are largely confined to the tropical and subtropical ocean. It has been argued that their global biogeographical distribution reflects the physiologically feasible temperature range at which they can perform nitrogen fixation. In this study we refine this line of argumentation for the globally important group of unicellular diazotrophic cyanobacteria, and pose the following two hypotheses: (i) nitrogen fixation is limited by nitrogenase activity at low temperature and by oxygen diffusion at high temperature, which is manifested by a shift from strong to weak temperature dependence of nitrogenase activity, and (ii) high respiration rates are required to maintain very low levels of oxygen for nitrogenase, which results in enhanced respiratory cost per molecule of fixed nitrogen at low temperature. We tested these hypotheses in laboratory experiments with the unicellular cyanobacterium Cyanothece sp. BG043511. In line with the first hypothesis, the specific growth rate increased strongly with temperature from 18 to 30 degrees C, but leveled off at higher temperature under nitrogen-fixing conditions. As predicted by the second hypothesis, the respiratory cost of nitrogen fixation and also the cellular C:N ratio rose sharply at temperatures below 21 degrees C. In addition, we found that low temperature caused a strong delay in the onset of the nocturnal nitrogenase activity, which shortened the remaining nighttime available for nitrogen fixation. Together, these results point at a lower temperature limit for unicellular nitrogen-fixing cyanobacteria, which offers an explanation for their (sub) tropical distribution and suggests expansion of their biogeographical range by global warming. Article in Journal/Newspaper North Atlantic University of Groningen research database Pacific The ISME Journal 7 11 2105 2115 |
institution |
Open Polar |
collection |
University of Groningen research database |
op_collection_id |
ftunigroningenpu |
language |
English |
topic |
climate change day-night cycle nitrogenase nitrogen fixation respiration unicellular cyanobacteria TROPICAL NORTH-ATLANTIC SP STRAIN ATCC-51142 DIAZOTROPHIC CYANOBACTERIUM FIXING CYANOBACTERIA PACIFIC-OCEAN N-2 FIXATION LIGHT-DARK ATCC 51142 TRANSCRIPTIONAL ANALYSIS CROCOSPHAERA-WATSONII |
spellingShingle |
climate change day-night cycle nitrogenase nitrogen fixation respiration unicellular cyanobacteria TROPICAL NORTH-ATLANTIC SP STRAIN ATCC-51142 DIAZOTROPHIC CYANOBACTERIUM FIXING CYANOBACTERIA PACIFIC-OCEAN N-2 FIXATION LIGHT-DARK ATCC 51142 TRANSCRIPTIONAL ANALYSIS CROCOSPHAERA-WATSONII Brauer, Verena S. Stomp, Maayke Rosso, Camillo van Beusekom, Sebastiaan A. M. Emmerich, Barbara Stal, Lucas J. Huisman, Jef Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece |
topic_facet |
climate change day-night cycle nitrogenase nitrogen fixation respiration unicellular cyanobacteria TROPICAL NORTH-ATLANTIC SP STRAIN ATCC-51142 DIAZOTROPHIC CYANOBACTERIUM FIXING CYANOBACTERIA PACIFIC-OCEAN N-2 FIXATION LIGHT-DARK ATCC 51142 TRANSCRIPTIONAL ANALYSIS CROCOSPHAERA-WATSONII |
description |
Marine nitrogen-fixing cyanobacteria are largely confined to the tropical and subtropical ocean. It has been argued that their global biogeographical distribution reflects the physiologically feasible temperature range at which they can perform nitrogen fixation. In this study we refine this line of argumentation for the globally important group of unicellular diazotrophic cyanobacteria, and pose the following two hypotheses: (i) nitrogen fixation is limited by nitrogenase activity at low temperature and by oxygen diffusion at high temperature, which is manifested by a shift from strong to weak temperature dependence of nitrogenase activity, and (ii) high respiration rates are required to maintain very low levels of oxygen for nitrogenase, which results in enhanced respiratory cost per molecule of fixed nitrogen at low temperature. We tested these hypotheses in laboratory experiments with the unicellular cyanobacterium Cyanothece sp. BG043511. In line with the first hypothesis, the specific growth rate increased strongly with temperature from 18 to 30 degrees C, but leveled off at higher temperature under nitrogen-fixing conditions. As predicted by the second hypothesis, the respiratory cost of nitrogen fixation and also the cellular C:N ratio rose sharply at temperatures below 21 degrees C. In addition, we found that low temperature caused a strong delay in the onset of the nocturnal nitrogenase activity, which shortened the remaining nighttime available for nitrogen fixation. Together, these results point at a lower temperature limit for unicellular nitrogen-fixing cyanobacteria, which offers an explanation for their (sub) tropical distribution and suggests expansion of their biogeographical range by global warming. |
format |
Article in Journal/Newspaper |
author |
Brauer, Verena S. Stomp, Maayke Rosso, Camillo van Beusekom, Sebastiaan A. M. Emmerich, Barbara Stal, Lucas J. Huisman, Jef |
author_facet |
Brauer, Verena S. Stomp, Maayke Rosso, Camillo van Beusekom, Sebastiaan A. M. Emmerich, Barbara Stal, Lucas J. Huisman, Jef |
author_sort |
Brauer, Verena S. |
title |
Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece |
title_short |
Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece |
title_full |
Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece |
title_fullStr |
Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece |
title_full_unstemmed |
Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece |
title_sort |
low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium cyanothece |
publishDate |
2013 |
url |
https://hdl.handle.net/11370/da3b9ab8-07ff-482e-b811-c335be7c311c https://research.rug.nl/en/publications/da3b9ab8-07ff-482e-b811-c335be7c311c https://doi.org/10.1038/ismej.2013.103 |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
North Atlantic |
genre_facet |
North Atlantic |
op_source |
Brauer , V S , Stomp , M , Rosso , C , van Beusekom , S A M , Emmerich , B , Stal , L J & Huisman , J 2013 , ' Low temperature delays timing and enhances the cost of nitrogen fixation in the unicellular cyanobacterium Cyanothece ' , ISME Journal , vol. 7 , no. 11 , pp. 2105-2115 . https://doi.org/10.1038/ismej.2013.103 |
op_relation |
https://research.rug.nl/en/publications/da3b9ab8-07ff-482e-b811-c335be7c311c |
op_rights |
info:eu-repo/semantics/closedAccess |
op_doi |
https://doi.org/10.1038/ismej.2013.103 |
container_title |
The ISME Journal |
container_volume |
7 |
container_issue |
11 |
container_start_page |
2105 |
op_container_end_page |
2115 |
_version_ |
1800757787036221440 |