Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm

ABSTRACT Increasing anthropogenic inputs of fixed nitrogen are leading to greater eutrophication of aquatic environments, but it is unclear how this impacts the flux and fate of carbon in lacustrine and riverine systems. Here, we present evidence that the form of nitrogen governs the partitioning of...

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Autores principales:	Christopher R. Anderton, Jennifer M. Mobberley, Jessica K. Cole, Jamie R. Nunez, Robert Starke, Amy A. Boaro, Yasemin Yesiltepe, Beau R. Morton, Alexandra B. Cory, Hayley C. Cardamone, Kirsten S. Hofmockel, Mary S. Lipton, James J. Moran, Ryan S. Renslow, James K. Fredrickson, Stephen R. Lindemann
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	carbon cycling cyanobacteria mass spectrometry nitrogen cycling stable isotopes Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/63459e7e7f9f423ebb8dc4e93035cc20
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spelling	oai:doaj.org-article:63459e7e7f9f423ebb8dc4e93035cc202021-12-02T18:44:35ZNitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm10.1128/mSystems.00260-202379-5077https://doaj.org/article/63459e7e7f9f423ebb8dc4e93035cc202020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00260-20https://doaj.org/toc/2379-5077ABSTRACT Increasing anthropogenic inputs of fixed nitrogen are leading to greater eutrophication of aquatic environments, but it is unclear how this impacts the flux and fate of carbon in lacustrine and riverine systems. Here, we present evidence that the form of nitrogen governs the partitioning of carbon among members in a genome-sequenced, model phototrophic biofilm of 20 members. Consumption of NO3− as the sole nitrogen source unexpectedly resulted in more rapid transfer of carbon to heterotrophs than when NH4+ was also provided, suggesting alterations in the form of carbon exchanged. The form of nitrogen dramatically impacted net community nitrogen, but not carbon, uptake rates. Furthermore, this alteration in nitrogen form caused very large but focused alterations to community structure, strongly impacting the abundance of only two species within the biofilm and modestly impacting a third member species. Our data suggest that nitrogen metabolism may coordinate coupled carbon-nitrogen biogeochemical cycling in benthic biofilms and, potentially, in phototroph-heterotroph consortia more broadly. It further indicates that the form of nitrogen inputs may significantly impact the contribution of these communities to carbon partitioning across the terrestrial-aquatic interface. IMPORTANCE Anthropogenic inputs of nitrogen into aquatic ecosystems, and especially those of agricultural origin, involve a mix of chemical species. Although it is well-known in general that nitrogen eutrophication markedly influences the metabolism of aquatic phototrophic communities, relatively little is known regarding whether the specific chemical form of nitrogen inputs matter. Our data suggest that the nitrogen form alters the rate of nitrogen uptake significantly, whereas corresponding alterations in carbon uptake were minor. However, differences imposed by uptake of divergent nitrogen forms may result in alterations among phototroph-heterotroph interactions that rewire community metabolism. Furthermore, our data hint that availability of other nutrients (i.e., iron) might mediate the linkage between carbon and nitrogen cycling in these communities. Taken together, our data suggest that different nitrogen forms should be examined for divergent impacts on phototrophic communities in fluvial systems and that these anthropogenic nitrogen inputs may significantly differ in their ultimate biogeochemical impacts.Christopher R. AndertonJennifer M. MobberleyJessica K. ColeJamie R. NunezRobert StarkeAmy A. BoaroYasemin YesiltepeBeau R. MortonAlexandra B. CoryHayley C. CardamoneKirsten S. HofmockelMary S. LiptonJames J. MoranRyan S. RenslowJames K. FredricksonStephen R. LindemannAmerican Society for Microbiologyarticlecarbon cyclingcyanobacteriamass spectrometrynitrogen cyclingstable isotopesMicrobiologyQR1-502ENmSystems, Vol 5, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	carbon cycling cyanobacteria mass spectrometry nitrogen cycling stable isotopes Microbiology QR1-502
spellingShingle	carbon cycling cyanobacteria mass spectrometry nitrogen cycling stable isotopes Microbiology QR1-502 Christopher R. Anderton Jennifer M. Mobberley Jessica K. Cole Jamie R. Nunez Robert Starke Amy A. Boaro Yasemin Yesiltepe Beau R. Morton Alexandra B. Cory Hayley C. Cardamone Kirsten S. Hofmockel Mary S. Lipton James J. Moran Ryan S. Renslow James K. Fredrickson Stephen R. Lindemann Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm
description	ABSTRACT Increasing anthropogenic inputs of fixed nitrogen are leading to greater eutrophication of aquatic environments, but it is unclear how this impacts the flux and fate of carbon in lacustrine and riverine systems. Here, we present evidence that the form of nitrogen governs the partitioning of carbon among members in a genome-sequenced, model phototrophic biofilm of 20 members. Consumption of NO3− as the sole nitrogen source unexpectedly resulted in more rapid transfer of carbon to heterotrophs than when NH4+ was also provided, suggesting alterations in the form of carbon exchanged. The form of nitrogen dramatically impacted net community nitrogen, but not carbon, uptake rates. Furthermore, this alteration in nitrogen form caused very large but focused alterations to community structure, strongly impacting the abundance of only two species within the biofilm and modestly impacting a third member species. Our data suggest that nitrogen metabolism may coordinate coupled carbon-nitrogen biogeochemical cycling in benthic biofilms and, potentially, in phototroph-heterotroph consortia more broadly. It further indicates that the form of nitrogen inputs may significantly impact the contribution of these communities to carbon partitioning across the terrestrial-aquatic interface. IMPORTANCE Anthropogenic inputs of nitrogen into aquatic ecosystems, and especially those of agricultural origin, involve a mix of chemical species. Although it is well-known in general that nitrogen eutrophication markedly influences the metabolism of aquatic phototrophic communities, relatively little is known regarding whether the specific chemical form of nitrogen inputs matter. Our data suggest that the nitrogen form alters the rate of nitrogen uptake significantly, whereas corresponding alterations in carbon uptake were minor. However, differences imposed by uptake of divergent nitrogen forms may result in alterations among phototroph-heterotroph interactions that rewire community metabolism. Furthermore, our data hint that availability of other nutrients (i.e., iron) might mediate the linkage between carbon and nitrogen cycling in these communities. Taken together, our data suggest that different nitrogen forms should be examined for divergent impacts on phototrophic communities in fluvial systems and that these anthropogenic nitrogen inputs may significantly differ in their ultimate biogeochemical impacts.
format	article
author	Christopher R. Anderton Jennifer M. Mobberley Jessica K. Cole Jamie R. Nunez Robert Starke Amy A. Boaro Yasemin Yesiltepe Beau R. Morton Alexandra B. Cory Hayley C. Cardamone Kirsten S. Hofmockel Mary S. Lipton James J. Moran Ryan S. Renslow James K. Fredrickson Stephen R. Lindemann
author_facet	Christopher R. Anderton Jennifer M. Mobberley Jessica K. Cole Jamie R. Nunez Robert Starke Amy A. Boaro Yasemin Yesiltepe Beau R. Morton Alexandra B. Cory Hayley C. Cardamone Kirsten S. Hofmockel Mary S. Lipton James J. Moran Ryan S. Renslow James K. Fredrickson Stephen R. Lindemann
author_sort	Christopher R. Anderton
title	Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm
title_short	Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm
title_full	Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm
title_fullStr	Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm
title_full_unstemmed	Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm
title_sort	nitrogen source governs community carbon metabolism in a model hypersaline benthic phototrophic biofilm
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/63459e7e7f9f423ebb8dc4e93035cc20
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Nitrogen Source Governs Community Carbon Metabolism in a Model Hypersaline Benthic Phototrophic Biofilm

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