The physiological cost of diazotrophy for Trichodesmium erythraeum IMS101
Trichodesmium plays a significant role in the oligotrophic oceans, fixing nitrogen in an area corresponding to half of the Earth's surface, representing up to 50% of new production in some oligotrophic tropical and subtropical oceans. Whilst Trichodesmium blooms at the surface exhibit a strong...
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| description | Trichodesmium plays a significant role in the oligotrophic oceans, fixing nitrogen in an area corresponding to half of the Earth's surface, representing up to 50% of new production in some oligotrophic tropical and subtropical oceans. Whilst Trichodesmium blooms at the surface exhibit a strong dependence on diazotrophy, colonies at depth or at the surface after a mixing event could be utilising additional N-sources. We conducted experiments to establish how acclimation to varying N-sources affects the growth, elemental composition, light absorption coefficient, N2 fixation, PSII electron transport rate and the relationship between net and gross photosynthetic O2 exchange in T. erythraeum IMS101. To do this, cultures were acclimated to growth medium containing NH4+ and NO3- (replete concentrations) or N2 only (diazotrophic control). The light dependencies of O2 evolution and O2 uptake were measured using membrane inlet mass spectrometry (MIMS), while PSII electron transport rates were measured from fluorescence light curves (FLCs). We found that at a saturating light intensity, Trichodesmium growth was ~ 10% and 13% lower when grown on N2 than with NH4+ and NO3-, respectively. Oxygen uptake increased linearly with net photosynthesis across all light intensities ranging from darkness to 1100 μmol photons m-2 s-1. The maximum rates and initial slopes of light response curves for C-specific gross and net photosynthesis and the slope of the relationship between gross and net photosynthesis increased significantly under non-diazotrophic conditions. We attribute these observations to a reduced expenditure of reductant and ATP for nitrogenase activity under non-diazotrophic conditions which allows NADPH and ATP to be re-directed to CO2 fixation and/or biosynthesis. The energy and reductant conserved through utilising additional N-sources could enhance Trichodesmium's productivity and growth and have major implications for its role in ocean C and N cycles. |
| doi_str_mv | 10.1371/journal.pone.0195638 |
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Whilst Trichodesmium blooms at the surface exhibit a strong dependence on diazotrophy, colonies at depth or at the surface after a mixing event could be utilising additional N-sources. We conducted experiments to establish how acclimation to varying N-sources affects the growth, elemental composition, light absorption coefficient, N2 fixation, PSII electron transport rate and the relationship between net and gross photosynthetic O2 exchange in T. erythraeum IMS101. To do this, cultures were acclimated to growth medium containing NH4+ and NO3- (replete concentrations) or N2 only (diazotrophic control). The light dependencies of O2 evolution and O2 uptake were measured using membrane inlet mass spectrometry (MIMS), while PSII electron transport rates were measured from fluorescence light curves (FLCs). We found that at a saturating light intensity, Trichodesmium growth was ~ 10% and 13% lower when grown on N2 than with NH4+ and NO3-, respectively. Oxygen uptake increased linearly with net photosynthesis across all light intensities ranging from darkness to 1100 μmol photons m-2 s-1. The maximum rates and initial slopes of light response curves for C-specific gross and net photosynthesis and the slope of the relationship between gross and net photosynthesis increased significantly under non-diazotrophic conditions. We attribute these observations to a reduced expenditure of reductant and ATP for nitrogenase activity under non-diazotrophic conditions which allows NADPH and ATP to be re-directed to CO2 fixation and/or biosynthesis. The energy and reductant conserved through utilising additional N-sources could enhance Trichodesmium's productivity and growth and have major implications for its role in ocean C and N cycles.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0195638</identifier><identifier>PMID: 29641568</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Absorption coefficient ; Absorption, Physicochemical ; Absorptivity ; Acclimation ; Acclimatization ; Amino acids ; ATP ; Biology and Life Sciences ; Biosynthesis ; Carbon ; Carbon dioxide ; Carbon dioxide fixation ; Carbon sequestration ; Chemical composition ; Cyanobacteria ; Darkness ; Earth Sciences ; Earth surface ; Ecology and Environmental Sciences ; Electromagnetic absorption ; Electron Transport ; Energy conservation ; Evolution ; Filamentous bacteria ; Fluorescence ; Light ; Light absorption ; Light intensity ; Limnology ; Luminous intensity ; Marine ecology ; Mass spectrometry ; Mass spectroscopy ; Methods ; NADP ; Nitrates ; Nitrogen ; Nitrogen Fixation ; Nitrogen-fixing microorganisms ; Nitrogenase ; Nitrogenation ; Oceanography ; Oceans ; Oxygen ; Oxygen - metabolism ; Oxygen uptake ; Photons ; Photosynthesis ; Photosystem II ; Photosystem II Protein Complex - metabolism ; Physical Sciences ; Physiological aspects ; Physiology ; Plankton ; Slopes ; Trichodesmium - cytology ; Trichodesmium - metabolism ; Trichodesmium - physiology ; Trichodesmium - radiation effects</subject><ispartof>PloS one, 2018-04, Vol.13 (4), p.e0195638-e0195638</ispartof><rights>COPYRIGHT 2018 Public Library of Science</rights><rights>2018 Boatman et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Whilst Trichodesmium blooms at the surface exhibit a strong dependence on diazotrophy, colonies at depth or at the surface after a mixing event could be utilising additional N-sources. We conducted experiments to establish how acclimation to varying N-sources affects the growth, elemental composition, light absorption coefficient, N2 fixation, PSII electron transport rate and the relationship between net and gross photosynthetic O2 exchange in T. erythraeum IMS101. To do this, cultures were acclimated to growth medium containing NH4+ and NO3- (replete concentrations) or N2 only (diazotrophic control). The light dependencies of O2 evolution and O2 uptake were measured using membrane inlet mass spectrometry (MIMS), while PSII electron transport rates were measured from fluorescence light curves (FLCs). We found that at a saturating light intensity, Trichodesmium growth was ~ 10% and 13% lower when grown on N2 than with NH4+ and NO3-, respectively. Oxygen uptake increased linearly with net photosynthesis across all light intensities ranging from darkness to 1100 μmol photons m-2 s-1. The maximum rates and initial slopes of light response curves for C-specific gross and net photosynthesis and the slope of the relationship between gross and net photosynthesis increased significantly under non-diazotrophic conditions. We attribute these observations to a reduced expenditure of reductant and ATP for nitrogenase activity under non-diazotrophic conditions which allows NADPH and ATP to be re-directed to CO2 fixation and/or biosynthesis. The energy and reductant conserved through utilising additional N-sources could enhance Trichodesmium's productivity and growth and have major implications for its role in ocean C and N cycles.</description><subject>Absorption coefficient</subject><subject>Absorption, Physicochemical</subject><subject>Absorptivity</subject><subject>Acclimation</subject><subject>Acclimatization</subject><subject>Amino acids</subject><subject>ATP</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Carbon</subject><subject>Carbon dioxide</subject><subject>Carbon dioxide fixation</subject><subject>Carbon sequestration</subject><subject>Chemical composition</subject><subject>Cyanobacteria</subject><subject>Darkness</subject><subject>Earth Sciences</subject><subject>Earth surface</subject><subject>Ecology and Environmental Sciences</subject><subject>Electromagnetic absorption</subject><subject>Electron Transport</subject><subject>Energy conservation</subject><subject>Evolution</subject><subject>Filamentous bacteria</subject><subject>Fluorescence</subject><subject>Light</subject><subject>Light absorption</subject><subject>Light intensity</subject><subject>Limnology</subject><subject>Luminous intensity</subject><subject>Marine ecology</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Methods</subject><subject>NADP</subject><subject>Nitrates</subject><subject>Nitrogen</subject><subject>Nitrogen Fixation</subject><subject>Nitrogen-fixing microorganisms</subject><subject>Nitrogenase</subject><subject>Nitrogenation</subject><subject>Oceanography</subject><subject>Oceans</subject><subject>Oxygen</subject><subject>Oxygen - metabolism</subject><subject>Oxygen uptake</subject><subject>Photons</subject><subject>Photosynthesis</subject><subject>Photosystem II</subject><subject>Photosystem II Protein Complex - metabolism</subject><subject>Physical Sciences</subject><subject>Physiological 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Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Boatman, Tobias G</au><au>Davey, Phillip A</au><au>Lawson, Tracy</au><au>Geider, Richard J</au><au>Campbell, Douglas A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The physiological cost of diazotrophy for Trichodesmium erythraeum IMS101</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2018-04-11</date><risdate>2018</risdate><volume>13</volume><issue>4</issue><spage>e0195638</spage><epage>e0195638</epage><pages>e0195638-e0195638</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Trichodesmium plays a significant role in the oligotrophic oceans, fixing nitrogen in an area corresponding to half of the Earth's surface, representing up to 50% of new production in some oligotrophic tropical and subtropical oceans. Whilst Trichodesmium blooms at the surface exhibit a strong dependence on diazotrophy, colonies at depth or at the surface after a mixing event could be utilising additional N-sources. We conducted experiments to establish how acclimation to varying N-sources affects the growth, elemental composition, light absorption coefficient, N2 fixation, PSII electron transport rate and the relationship between net and gross photosynthetic O2 exchange in T. erythraeum IMS101. To do this, cultures were acclimated to growth medium containing NH4+ and NO3- (replete concentrations) or N2 only (diazotrophic control). The light dependencies of O2 evolution and O2 uptake were measured using membrane inlet mass spectrometry (MIMS), while PSII electron transport rates were measured from fluorescence light curves (FLCs). We found that at a saturating light intensity, Trichodesmium growth was ~ 10% and 13% lower when grown on N2 than with NH4+ and NO3-, respectively. Oxygen uptake increased linearly with net photosynthesis across all light intensities ranging from darkness to 1100 μmol photons m-2 s-1. The maximum rates and initial slopes of light response curves for C-specific gross and net photosynthesis and the slope of the relationship between gross and net photosynthesis increased significantly under non-diazotrophic conditions. We attribute these observations to a reduced expenditure of reductant and ATP for nitrogenase activity under non-diazotrophic conditions which allows NADPH and ATP to be re-directed to CO2 fixation and/or biosynthesis. The energy and reductant conserved through utilising additional N-sources could enhance Trichodesmium's productivity and growth and have major implications for its role in ocean C and N cycles.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>29641568</pmid><doi>10.1371/journal.pone.0195638</doi><tpages>e0195638</tpages><orcidid>https://orcid.org/0000-0001-7541-3844</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2018-04, Vol.13 (4), p.e0195638-e0195638 |
| issn | 1932-6203 1932-6203 |
| language | eng |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Absorption coefficient Absorption, Physicochemical Absorptivity Acclimation Acclimatization Amino acids ATP Biology and Life Sciences Biosynthesis Carbon Carbon dioxide Carbon dioxide fixation Carbon sequestration Chemical composition Cyanobacteria Darkness Earth Sciences Earth surface Ecology and Environmental Sciences Electromagnetic absorption Electron Transport Energy conservation Evolution Filamentous bacteria Fluorescence Light Light absorption Light intensity Limnology Luminous intensity Marine ecology Mass spectrometry Mass spectroscopy Methods NADP Nitrates Nitrogen Nitrogen Fixation Nitrogen-fixing microorganisms Nitrogenase Nitrogenation Oceanography Oceans Oxygen Oxygen - metabolism Oxygen uptake Photons Photosynthesis Photosystem II Photosystem II Protein Complex - metabolism Physical Sciences Physiological aspects Physiology Plankton Slopes Trichodesmium - cytology Trichodesmium - metabolism Trichodesmium - physiology Trichodesmium - radiation effects |
| title | The physiological cost of diazotrophy for Trichodesmium erythraeum IMS101 |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T19%3A15%3A18IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20physiological%20cost%20of%20diazotrophy%20for%20Trichodesmium%20erythraeum%20IMS101&rft.jtitle=PloS%20one&rft.au=Boatman,%20Tobias%20G&rft.date=2018-04-11&rft.volume=13&rft.issue=4&rft.spage=e0195638&rft.epage=e0195638&rft.pages=e0195638-e0195638&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0195638&rft_dat=%3Cgale_plos_%3EA534255265%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2024149382&rft_id=info:pmid/29641568&rft_galeid=A534255265&rft_doaj_id=oai_doaj_org_article_340fffaaa0b349d58eeb730a049503e9&rfr_iscdi=true |