Dark Diazotrophy during the Late Summer in Surface Waters of Chile Bay, West Antarctic Peninsula

Although crucial for the addition of new nitrogen in marine ecosystems, dinitrogen (N<sub>2</sub>) fixation remains an understudied process, especially under dark conditions and in polar coastal areas, such as the West Antarctic Peninsula (WAP). New measurements of light and dark N<su...

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Main Authors: María E. Alcamán-Arias, Jerónimo Cifuentes-Anticevic, Wilson Castillo-Inaipil, Laura Farías, Cynthia Sanhueza, Beatriz Fernández-Gómez, Josefa Verdugo, Leslie Abarzua, Christina Ridley, Javier Tamayo-Leiva, Beatriz Díez
Format: Article
Language:English
Published: MDPI AG 2022-05-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/10/6/1140
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author María E. Alcamán-Arias
Jerónimo Cifuentes-Anticevic
Wilson Castillo-Inaipil
Laura Farías
Cynthia Sanhueza
Beatriz Fernández-Gómez
Josefa Verdugo
Leslie Abarzua
Christina Ridley
Javier Tamayo-Leiva
Beatriz Díez
author_facet María E. Alcamán-Arias
Jerónimo Cifuentes-Anticevic
Wilson Castillo-Inaipil
Laura Farías
Cynthia Sanhueza
Beatriz Fernández-Gómez
Josefa Verdugo
Leslie Abarzua
Christina Ridley
Javier Tamayo-Leiva
Beatriz Díez
author_sort María E. Alcamán-Arias
collection DOAJ
description Although crucial for the addition of new nitrogen in marine ecosystems, dinitrogen (N<sub>2</sub>) fixation remains an understudied process, especially under dark conditions and in polar coastal areas, such as the West Antarctic Peninsula (WAP). New measurements of light and dark N<sub>2</sub> fixation rates in parallel with carbon (C) fixation rates, as well as analysis of the genetic marker <i>nif</i>H for diazotrophic organisms, were conducted during the late summer in the coastal waters of Chile Bay, South Shetland Islands, WAP. During six late summers (February 2013 to 2019), Chile Bay was characterized by high NO<sub>3</sub><sup>−</sup> concentrations (~20 µM) and an NH<sub>4</sub><sup>+</sup> content that remained stable near 0.5 µM. The N:P ratio was approximately 14.1, thus close to that of the Redfield ratio (16:1). The presence of Cluster I and Cluster III <i>nif</i>H gene sequences closely related to Alpha-, Delta- and, to a lesser extent, Gammaproteobacteria, suggests that chemosynthetic and heterotrophic bacteria are primarily responsible for N<sub>2</sub> fixation in the bay. Photosynthetic carbon assimilation ranged from 51.18 to 1471 nmol C L<sup>−1</sup> d<sup>−1</sup>, while dark chemosynthesis ranged from 9.24 to 805 nmol C L<sup>−1</sup> d<sup>−1</sup>. N<sub>2</sub> fixation rates were higher under dark conditions (up to 45.40 nmol N L<sup>−1</sup> d<sup>−1</sup>) than under light conditions (up to 7.70 nmol N L<sup>−1</sup> d<sup>−1</sup>), possibly contributing more than 37% to new nitrogen-based production (≥2.5 g N m<sup>−2</sup> y<sup>−1</sup>). Of all the environmental factors measured, only PO<sub>4</sub><sup>3-</sup> exhibited a significant correlation with C and N<sub>2</sub> rates, being negatively correlated (<i>p</i> < 0.05) with dark chemosynthesis and N<sub>2</sub> fixation under the light condition, revealing the importance of the N:P ratio for these processes in Chile Bay. This significant contribution of N<sub>2</sub> fixation expands the ubiquity and biological potential of these marine chemosynthetic diazotrophs. As such, this process should be considered along with the entire N cycle when further reviewing highly productive Antarctic coastal waters and the diazotrophic potential of the global marine ecosystem.
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spelling doaj.art-c21bca205fd14a858dbbf671535232d12023-11-23T18:03:39ZengMDPI AGMicroorganisms2076-26072022-05-01106114010.3390/microorganisms10061140Dark Diazotrophy during the Late Summer in Surface Waters of Chile Bay, West Antarctic PeninsulaMaría E. Alcamán-Arias0Jerónimo Cifuentes-Anticevic1Wilson Castillo-Inaipil2Laura Farías3Cynthia Sanhueza4Beatriz Fernández-Gómez5Josefa Verdugo6Leslie Abarzua7Christina Ridley8Javier Tamayo-Leiva9Beatriz Díez10Departamento de Oceanografía, Universidad de Concepción, Concepción 4030000, ChileDepartamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Santiago 8331150, ChileDepartamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Santiago 8331150, ChileDepartamento de Oceanografía, Universidad de Concepción, Concepción 4030000, ChileDepartamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Santiago 8331150, ChileDepartamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Santiago 8331150, ChileAlfred-Wegener-Institute, Helmholtz Centre for Polar and Marine Research, 27570 Bremerhaven, GermanyDepartamento de Oceanografía, Universidad de Concepción, Concepción 4030000, ChileCenter for Climate and Resilience Research (CR)2, Universidad de Chile, Blanco Encalada 2002, Santiago 8320000, ChileCenter for Climate and Resilience Research (CR)2, Universidad de Chile, Blanco Encalada 2002, Santiago 8320000, ChileCenter for Climate and Resilience Research (CR)2, Universidad de Chile, Blanco Encalada 2002, Santiago 8320000, ChileAlthough crucial for the addition of new nitrogen in marine ecosystems, dinitrogen (N<sub>2</sub>) fixation remains an understudied process, especially under dark conditions and in polar coastal areas, such as the West Antarctic Peninsula (WAP). New measurements of light and dark N<sub>2</sub> fixation rates in parallel with carbon (C) fixation rates, as well as analysis of the genetic marker <i>nif</i>H for diazotrophic organisms, were conducted during the late summer in the coastal waters of Chile Bay, South Shetland Islands, WAP. During six late summers (February 2013 to 2019), Chile Bay was characterized by high NO<sub>3</sub><sup>−</sup> concentrations (~20 µM) and an NH<sub>4</sub><sup>+</sup> content that remained stable near 0.5 µM. The N:P ratio was approximately 14.1, thus close to that of the Redfield ratio (16:1). The presence of Cluster I and Cluster III <i>nif</i>H gene sequences closely related to Alpha-, Delta- and, to a lesser extent, Gammaproteobacteria, suggests that chemosynthetic and heterotrophic bacteria are primarily responsible for N<sub>2</sub> fixation in the bay. Photosynthetic carbon assimilation ranged from 51.18 to 1471 nmol C L<sup>−1</sup> d<sup>−1</sup>, while dark chemosynthesis ranged from 9.24 to 805 nmol C L<sup>−1</sup> d<sup>−1</sup>. N<sub>2</sub> fixation rates were higher under dark conditions (up to 45.40 nmol N L<sup>−1</sup> d<sup>−1</sup>) than under light conditions (up to 7.70 nmol N L<sup>−1</sup> d<sup>−1</sup>), possibly contributing more than 37% to new nitrogen-based production (≥2.5 g N m<sup>−2</sup> y<sup>−1</sup>). Of all the environmental factors measured, only PO<sub>4</sub><sup>3-</sup> exhibited a significant correlation with C and N<sub>2</sub> rates, being negatively correlated (<i>p</i> < 0.05) with dark chemosynthesis and N<sub>2</sub> fixation under the light condition, revealing the importance of the N:P ratio for these processes in Chile Bay. This significant contribution of N<sub>2</sub> fixation expands the ubiquity and biological potential of these marine chemosynthetic diazotrophs. As such, this process should be considered along with the entire N cycle when further reviewing highly productive Antarctic coastal waters and the diazotrophic potential of the global marine ecosystem.https://www.mdpi.com/2076-2607/10/6/1140nitrogen fixationheterotrophic diazotrophyWAP/new productiondiazotrophy
spellingShingle María E. Alcamán-Arias
Jerónimo Cifuentes-Anticevic
Wilson Castillo-Inaipil
Laura Farías
Cynthia Sanhueza
Beatriz Fernández-Gómez
Josefa Verdugo
Leslie Abarzua
Christina Ridley
Javier Tamayo-Leiva
Beatriz Díez
Dark Diazotrophy during the Late Summer in Surface Waters of Chile Bay, West Antarctic Peninsula
Microorganisms
nitrogen fixation
heterotrophic diazotrophy
WAP/new production
diazotrophy
title Dark Diazotrophy during the Late Summer in Surface Waters of Chile Bay, West Antarctic Peninsula
title_full Dark Diazotrophy during the Late Summer in Surface Waters of Chile Bay, West Antarctic Peninsula
title_fullStr Dark Diazotrophy during the Late Summer in Surface Waters of Chile Bay, West Antarctic Peninsula
title_full_unstemmed Dark Diazotrophy during the Late Summer in Surface Waters of Chile Bay, West Antarctic Peninsula
title_short Dark Diazotrophy during the Late Summer in Surface Waters of Chile Bay, West Antarctic Peninsula
title_sort dark diazotrophy during the late summer in surface waters of chile bay west antarctic peninsula
topic nitrogen fixation
heterotrophic diazotrophy
WAP/new production
diazotrophy
url https://www.mdpi.com/2076-2607/10/6/1140
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