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Micronutrient content drives elementome variability amongst the Symbiodiniaceae

BACKGROUND: Elements are the basis of life on Earth, whereby organisms are essentially evolved chemical substances that dynamically interact with each other and their environment. Determining species elemental quotas (their elementome) is a key indicator for their success across environments with di...

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Autores principales: Camp, Emma F., Nitschke, Matthew R., Clases, David, Gonzalez de Vega, Raquel, Reich, Hannah G., Goyen, Samantha, Suggett, David J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8994382/
https://www.ncbi.nlm.nih.gov/pubmed/35395710
http://dx.doi.org/10.1186/s12870-022-03512-0
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author Camp, Emma F.
Nitschke, Matthew R.
Clases, David
Gonzalez de Vega, Raquel
Reich, Hannah G.
Goyen, Samantha
Suggett, David J.
author_facet Camp, Emma F.
Nitschke, Matthew R.
Clases, David
Gonzalez de Vega, Raquel
Reich, Hannah G.
Goyen, Samantha
Suggett, David J.
author_sort Camp, Emma F.
collection PubMed
description BACKGROUND: Elements are the basis of life on Earth, whereby organisms are essentially evolved chemical substances that dynamically interact with each other and their environment. Determining species elemental quotas (their elementome) is a key indicator for their success across environments with different resource availabilities. Elementomes remain undescribed for functionally diverse dinoflagellates within the family Symbiodiniaceae that includes coral endosymbionts. We used dry combustion and ICP-MS to assess whether Symbiodiniaceae (ten isolates spanning five genera Breviolum, Cladocopium, Durusdinium, Effrenium, Symbiodinium) maintained under long-term nutrient replete conditions have unique elementomes (six key macronutrients and nine micronutrients) that would reflect evolutionarily conserved preferential elemental acquisition. For three isolates we assessed how elevated temperature impacted their elementomes. Further, we tested whether Symbiodiniaceae conform to common stoichiometric hypotheses (e.g., the growth rate hypothesis) documented in other marine algae. This study considers whether Symbiodiniaceae isolates possess unique elementomes reflective of their natural ecologies, evolutionary histories, and resistance to environmental change. RESULTS: Symbiodiniaceae isolates maintained under long-term luxury uptake conditions, all exhibited highly divergent elementomes from one another, driven primarily by differential content of micronutrients. All N:P and C:P ratios were below the Redfield ratio values, whereas C:N was close to the Redfield value. Elevated temperature resulted in a more homogenised elementome across isolates. The Family-level elementome was (C(19.8)N(2.6) P(1.0)S(18.8)K(0.7)Ca(0.1)) · 1000 (Fe(55.7)Mn(5.6)Sr(2.3)Zn(0.8)Ni(0.5)Se(0.3)Cu(0.2)Mo(0.1)V(0.04)) mmol Phosphorous(-1) versus (C(25.4)N(3.1)P(1.0)S(23.1)K(0.9)Ca(0.4)) · 1000 (Fe(66.7)Mn(6.3)Sr(7.2)Zn(0.8)Ni(0.4)Se(0.2)Cu(0.2)Mo(0.2)V(0.05)) mmol Phosphorous (-1) at 27.4 ± 0.4 °C and 30.7 ± 0.01 °C, respectively. Symbiodiniaceae isolates tested here conformed to some, but not all, stoichiometric principles. CONCLUSIONS: Elementomes for Symbiodiniaceae diverge from those reported for other marine algae, primarily via lower C:N:P and different micronutrient expressions. Long-term maintenance of Symbiodiniaceae isolates in culture under common nutrient replete conditions suggests isolates have evolutionary conserved preferential uptake for certain elements that allows these unique elementomes to be identified. Micronutrient content (normalised to phosphorous) commonly increased in the Symbiodiniaceae isolates in response to elevated temperature, potentially indicating a common elemental signature to warming. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03512-0.
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spelling pubmed-89943822022-04-10 Micronutrient content drives elementome variability amongst the Symbiodiniaceae Camp, Emma F. Nitschke, Matthew R. Clases, David Gonzalez de Vega, Raquel Reich, Hannah G. Goyen, Samantha Suggett, David J. BMC Plant Biol Research Article BACKGROUND: Elements are the basis of life on Earth, whereby organisms are essentially evolved chemical substances that dynamically interact with each other and their environment. Determining species elemental quotas (their elementome) is a key indicator for their success across environments with different resource availabilities. Elementomes remain undescribed for functionally diverse dinoflagellates within the family Symbiodiniaceae that includes coral endosymbionts. We used dry combustion and ICP-MS to assess whether Symbiodiniaceae (ten isolates spanning five genera Breviolum, Cladocopium, Durusdinium, Effrenium, Symbiodinium) maintained under long-term nutrient replete conditions have unique elementomes (six key macronutrients and nine micronutrients) that would reflect evolutionarily conserved preferential elemental acquisition. For three isolates we assessed how elevated temperature impacted their elementomes. Further, we tested whether Symbiodiniaceae conform to common stoichiometric hypotheses (e.g., the growth rate hypothesis) documented in other marine algae. This study considers whether Symbiodiniaceae isolates possess unique elementomes reflective of their natural ecologies, evolutionary histories, and resistance to environmental change. RESULTS: Symbiodiniaceae isolates maintained under long-term luxury uptake conditions, all exhibited highly divergent elementomes from one another, driven primarily by differential content of micronutrients. All N:P and C:P ratios were below the Redfield ratio values, whereas C:N was close to the Redfield value. Elevated temperature resulted in a more homogenised elementome across isolates. The Family-level elementome was (C(19.8)N(2.6) P(1.0)S(18.8)K(0.7)Ca(0.1)) · 1000 (Fe(55.7)Mn(5.6)Sr(2.3)Zn(0.8)Ni(0.5)Se(0.3)Cu(0.2)Mo(0.1)V(0.04)) mmol Phosphorous(-1) versus (C(25.4)N(3.1)P(1.0)S(23.1)K(0.9)Ca(0.4)) · 1000 (Fe(66.7)Mn(6.3)Sr(7.2)Zn(0.8)Ni(0.4)Se(0.2)Cu(0.2)Mo(0.2)V(0.05)) mmol Phosphorous (-1) at 27.4 ± 0.4 °C and 30.7 ± 0.01 °C, respectively. Symbiodiniaceae isolates tested here conformed to some, but not all, stoichiometric principles. CONCLUSIONS: Elementomes for Symbiodiniaceae diverge from those reported for other marine algae, primarily via lower C:N:P and different micronutrient expressions. Long-term maintenance of Symbiodiniaceae isolates in culture under common nutrient replete conditions suggests isolates have evolutionary conserved preferential uptake for certain elements that allows these unique elementomes to be identified. Micronutrient content (normalised to phosphorous) commonly increased in the Symbiodiniaceae isolates in response to elevated temperature, potentially indicating a common elemental signature to warming. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03512-0. BioMed Central 2022-04-09 /pmc/articles/PMC8994382/ /pubmed/35395710 http://dx.doi.org/10.1186/s12870-022-03512-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Camp, Emma F.
Nitschke, Matthew R.
Clases, David
Gonzalez de Vega, Raquel
Reich, Hannah G.
Goyen, Samantha
Suggett, David J.
Micronutrient content drives elementome variability amongst the Symbiodiniaceae
title Micronutrient content drives elementome variability amongst the Symbiodiniaceae
title_full Micronutrient content drives elementome variability amongst the Symbiodiniaceae
title_fullStr Micronutrient content drives elementome variability amongst the Symbiodiniaceae
title_full_unstemmed Micronutrient content drives elementome variability amongst the Symbiodiniaceae
title_short Micronutrient content drives elementome variability amongst the Symbiodiniaceae
title_sort micronutrient content drives elementome variability amongst the symbiodiniaceae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8994382/
https://www.ncbi.nlm.nih.gov/pubmed/35395710
http://dx.doi.org/10.1186/s12870-022-03512-0
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