Quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles

<jats:title>Abstract</jats:title><jats:p>Nitrogen (<jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub>...

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Main Authors:	Chakraborty, Subhendu, Andersen, Ken H, Visser, André W, Inomura, Keisuke, Follows, Michael J, Riemann, Lasse
Format:	Article
Language:	English
Published:	Springer Science and Business Media LLC 2021
Online Access:	https://hdl.handle.net/1721.1/135568

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author	Chakraborty, Subhendu Andersen, Ken H Visser, André W Inomura, Keisuke Follows, Michael J Riemann, Lasse
author_facet	Chakraborty, Subhendu Andersen, Ken H Visser, André W Inomura, Keisuke Follows, Michael J Riemann, Lasse
author_sort	Chakraborty, Subhendu
collection	MIT
description	<jats:title>Abstract</jats:title><jats:p>Nitrogen (<jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula>) fixation by heterotrophic bacteria associated with sinking particles contributes to marine N cycling, but a mechanistic understanding of its regulation and significance are not available. Here we develop a mathematical model for unicellular heterotrophic bacteria growing on sinking marine particles. These bacteria can fix <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> under suitable environmental conditions. We find that the interactive effects of polysaccharide and polypeptide concentrations, sinking speed of particles, and surrounding <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{O}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>O</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> and <jats:inline-formula><jats:alternatives><jats:tex-math>$${{{\rm{NO}}}_{3}}^{-}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msup> <mml:mrow> <mml:msub> <mml:mrow> <mml:mi>NO</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>3</mml:mn> </mml:mrow> </mml:msub> </mml:mrow> <mml:mrow> <mml:mo>−</mml:mo> </mml:mrow> </mml:msup> </mml:math></jats:alternatives></jats:inline-formula> concentrations determine the <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation rate inside particles. <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation inside sinking particles is mainly fueled by <jats:inline-formula><jats:alternatives><jats:tex-math>$${{{\rm{SO}}}_{4}}^{2-}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msup> <mml:mrow> <mml:msub> <mml:mrow> <mml:mi>SO</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>4</mml:mn> </mml:mrow> </mml:msub> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> <mml:mo>−</mml:mo> </mml:mrow> </mml:msup> </mml:math></jats:alternatives></jats:inline-formula> respiration rather than <jats:inline-formula><jats:alternatives><jats:tex-math>$${{{\rm{NO}}}_{3}}^{-}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msup> <mml:mrow> <mml:msub> <mml:mrow> <mml:mi>NO</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>3</mml:mn> </mml:mrow> </mml:msub> </mml:mrow> <mml:mrow> <mml:mo>−</mml:mo> </mml:mrow> </mml:msup> </mml:math></jats:alternatives></jats:inline-formula> respiration. Our model suggests that anaerobic processes, including heterotrophic <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation, can take place in anoxic microenvironments inside sinking particles even in fully oxygenated marine waters. The modelled <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation rates are similar to bulk rates measured in the aphotic ocean, and our study consequently suggests that particle-associated heterotrophic <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation contributes significantly to oceanic <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation.</jats:p>
first_indexed	2024-09-23T08:26:07Z
format	Article
id	mit-1721.1/135568
institution	Massachusetts Institute of Technology
language	English
last_indexed	2024-09-23T08:26:07Z
publishDate	2021
publisher	Springer Science and Business Media LLC
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spelling	mit-1721.1/1355682021-10-28T04:58:14Z Quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles Chakraborty, Subhendu Andersen, Ken H Visser, André W Inomura, Keisuke Follows, Michael J Riemann, Lasse <jats:title>Abstract</jats:title><jats:p>Nitrogen (<jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula>) fixation by heterotrophic bacteria associated with sinking particles contributes to marine N cycling, but a mechanistic understanding of its regulation and significance are not available. Here we develop a mathematical model for unicellular heterotrophic bacteria growing on sinking marine particles. These bacteria can fix <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> under suitable environmental conditions. We find that the interactive effects of polysaccharide and polypeptide concentrations, sinking speed of particles, and surrounding <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{O}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>O</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> and <jats:inline-formula><jats:alternatives><jats:tex-math>$${{{\rm{NO}}}_{3}}^{-}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msup> <mml:mrow> <mml:msub> <mml:mrow> <mml:mi>NO</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>3</mml:mn> </mml:mrow> </mml:msub> </mml:mrow> <mml:mrow> <mml:mo>−</mml:mo> </mml:mrow> </mml:msup> </mml:math></jats:alternatives></jats:inline-formula> concentrations determine the <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation rate inside particles. <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation inside sinking particles is mainly fueled by <jats:inline-formula><jats:alternatives><jats:tex-math>$${{{\rm{SO}}}_{4}}^{2-}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msup> <mml:mrow> <mml:msub> <mml:mrow> <mml:mi>SO</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>4</mml:mn> </mml:mrow> </mml:msub> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> <mml:mo>−</mml:mo> </mml:mrow> </mml:msup> </mml:math></jats:alternatives></jats:inline-formula> respiration rather than <jats:inline-formula><jats:alternatives><jats:tex-math>$${{{\rm{NO}}}_{3}}^{-}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msup> <mml:mrow> <mml:msub> <mml:mrow> <mml:mi>NO</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>3</mml:mn> </mml:mrow> </mml:msub> </mml:mrow> <mml:mrow> <mml:mo>−</mml:mo> </mml:mrow> </mml:msup> </mml:math></jats:alternatives></jats:inline-formula> respiration. Our model suggests that anaerobic processes, including heterotrophic <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation, can take place in anoxic microenvironments inside sinking particles even in fully oxygenated marine waters. The modelled <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation rates are similar to bulk rates measured in the aphotic ocean, and our study consequently suggests that particle-associated heterotrophic <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation contributes significantly to oceanic <jats:inline-formula><jats:alternatives><jats:tex-math>$${{\rm{N}}}_{2}$$</jats:tex-math><mml:math xmlns:mml="http://www.w3.org/1998/Math/MathML"> <mml:msub> <mml:mrow> <mml:mi>N</mml:mi> </mml:mrow> <mml:mrow> <mml:mn>2</mml:mn> </mml:mrow> </mml:msub> </mml:math></jats:alternatives></jats:inline-formula> fixation.</jats:p> 2021-10-27T20:24:04Z 2021-10-27T20:24:04Z 2021-12 2021-09-16T16:15:55Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/135568 en 10.1038/s41467-021-23875-6 Nature Communications Creative Commons Attribution 4.0 International license https://creativecommons.org/licenses/by/4.0/ application/pdf Springer Science and Business Media LLC Nature
spellingShingle	Chakraborty, Subhendu Andersen, Ken H Visser, André W Inomura, Keisuke Follows, Michael J Riemann, Lasse Quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles
title	Quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles
title_full	Quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles
title_fullStr	Quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles
title_full_unstemmed	Quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles
title_short	Quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles
title_sort	quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles
url	https://hdl.handle.net/1721.1/135568
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Quantifying nitrogen fixation by heterotrophic bacteria in sinking marine particles

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