Micronutrient content drives elementome variability amongst the Symbiodiniaceae
Abstract 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...
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| Format: | Article |
| Language: | English |
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BMC
2022-04-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-022-03512-0 |
| _version_ | 1819061480973139968 |
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| author | Emma F. Camp Matthew R. Nitschke David Clases Raquel Gonzalez de Vega Hannah G. Reich Samantha Goyen David J. Suggett |
| author_facet | Emma F. Camp Matthew R. Nitschke David Clases Raquel Gonzalez de Vega Hannah G. Reich Samantha Goyen David J. Suggett |
| author_sort | Emma F. Camp |
| collection | DOAJ |
| description | Abstract 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 (C19.8N2.6 P1.0S18.8K0.7Ca0.1) · 1000 (Fe55.7Mn5.6Sr2.3Zn0.8Ni0.5Se0.3Cu0.2Mo0.1V0.04) mmol Phosphorous-1 versus (C25.4N3.1P1.0S23.1K0.9Ca0.4) · 1000 (Fe66.7Mn6.3Sr7.2Zn0.8Ni0.4Se0.2Cu0.2Mo0.2V0.05) 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. |
| first_indexed | 2024-12-21T14:43:34Z |
| format | Article |
| id | doaj.art-a9f493cfc982487ab76324927f8f885e |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-12-21T14:43:34Z |
| publishDate | 2022-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-a9f493cfc982487ab76324927f8f885e2022-12-21T19:00:07ZengBMCBMC Plant Biology1471-22292022-04-0122111410.1186/s12870-022-03512-0Micronutrient content drives elementome variability amongst the SymbiodiniaceaeEmma F. Camp0Matthew R. Nitschke1David Clases2Raquel Gonzalez de Vega3Hannah G. Reich4Samantha Goyen5David J. Suggett6Climate Change Cluster (C3), University of Technology SydneyClimate Change Cluster (C3), University of Technology SydneyThe Atomic Medicine Initiative, University of Technology SydneyThe Atomic Medicine Initiative, University of Technology SydneyDepartment of Biological Sciences, University of Rhode IslandClimate Change Cluster (C3), University of Technology SydneyClimate Change Cluster (C3), University of Technology SydneyAbstract 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 (C19.8N2.6 P1.0S18.8K0.7Ca0.1) · 1000 (Fe55.7Mn5.6Sr2.3Zn0.8Ni0.5Se0.3Cu0.2Mo0.1V0.04) mmol Phosphorous-1 versus (C25.4N3.1P1.0S23.1K0.9Ca0.4) · 1000 (Fe66.7Mn6.3Sr7.2Zn0.8Ni0.4Se0.2Cu0.2Mo0.2V0.05) 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.https://doi.org/10.1186/s12870-022-03512-0DinoflagellatesElemental phenotypingElementomeMacronutrients; Micronutrients; Redfield ratioSymbiodiniaceae |
| spellingShingle | Emma F. Camp Matthew R. Nitschke David Clases Raquel Gonzalez de Vega Hannah G. Reich Samantha Goyen David J. Suggett Micronutrient content drives elementome variability amongst the Symbiodiniaceae BMC Plant Biology Dinoflagellates Elemental phenotyping Elementome Macronutrients; Micronutrients; Redfield ratio 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 | Dinoflagellates Elemental phenotyping Elementome Macronutrients; Micronutrients; Redfield ratio Symbiodiniaceae |
| url | https://doi.org/10.1186/s12870-022-03512-0 |
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