The Influence of Symbiosis on the Proteome of the <i>Exaiptasia</i> Endosymbiont <i>Breviolum minutum</i>
The cellular mechanisms responsible for the regulation of nutrient exchange, immune response, and symbiont population growth in the cnidarian–dinoflagellate symbiosis are poorly resolved. Here, we employed liquid chromatography–mass spectrometry to elucidate proteomic changes associated with symbios...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-01-01
|
| Series: | Microorganisms |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2076-2607/11/2/292 |
| _version_ | 1797619143977992192 |
|---|---|
| author | Amirhossein Gheitanchi Mashini Clinton A. Oakley Sandeep S. Beepat Lifeng Peng Arthur R. Grossman Virginia M. Weis Simon K. Davy |
| author_facet | Amirhossein Gheitanchi Mashini Clinton A. Oakley Sandeep S. Beepat Lifeng Peng Arthur R. Grossman Virginia M. Weis Simon K. Davy |
| author_sort | Amirhossein Gheitanchi Mashini |
| collection | DOAJ |
| description | The cellular mechanisms responsible for the regulation of nutrient exchange, immune response, and symbiont population growth in the cnidarian–dinoflagellate symbiosis are poorly resolved. Here, we employed liquid chromatography–mass spectrometry to elucidate proteomic changes associated with symbiosis in <i>Breviolum minutum</i>, a native symbiont of the sea anemone <i>Exaiptasia diaphana</i> (‘Aiptasia’). We manipulated nutrients available to the algae in culture and to the holobiont <i>in hospite</i> (i.e., in symbiosis) and then monitored the impacts of our treatments on host–endosymbiont interactions. Both the symbiotic and nutritional states had significant impacts on the <i>B. minutum</i> proteome. <i>B. minutum in hospite</i> showed an increased abundance of proteins involved in phosphoinositol metabolism (e.g., glycerophosphoinositol permease 1 and phosphatidylinositol phosphatase) relative to the free-living alga, potentially reflecting inter-partner signalling that promotes the stability of the symbiosis. Proteins potentially involved in concentrating and fixing inorganic carbon (e.g., carbonic anhydrase, V-type ATPase) and in the assimilation of nitrogen (e.g., glutamine synthase) were more abundant in free-living <i>B. minutum</i> than <i>in hospite</i>, possibly due to host-facilitated access to inorganic carbon and nitrogen limitation by the host when <i>in hospite</i>. Photosystem proteins increased in abundance at high nutrient levels irrespective of the symbiotic state, as did proteins involved in antioxidant defences (e.g., superoxide dismutase, glutathione s-transferase). Proteins involved in iron metabolism were also affected by the nutritional state, with an increased iron demand and uptake under low nutrient treatments. These results detail the changes in symbiont physiology in response to the host microenvironment and nutrient availability and indicate potential symbiont-driven mechanisms that regulate the cnidarian–dinoflagellate symbiosis. |
| first_indexed | 2024-03-11T08:23:56Z |
| format | Article |
| id | doaj.art-36c0b4878f1448a1a3189f7dc56695e3 |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-11T08:23:56Z |
| publishDate | 2023-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-36c0b4878f1448a1a3189f7dc56695e32023-11-16T22:13:53ZengMDPI AGMicroorganisms2076-26072023-01-0111229210.3390/microorganisms11020292The Influence of Symbiosis on the Proteome of the <i>Exaiptasia</i> Endosymbiont <i>Breviolum minutum</i>Amirhossein Gheitanchi Mashini0Clinton A. Oakley1Sandeep S. Beepat2Lifeng Peng3Arthur R. Grossman4Virginia M. Weis5Simon K. Davy6School of Biological Sciences, Victoria University of Wellington, Wellington 6140, New ZealandSchool of Biological Sciences, Victoria University of Wellington, Wellington 6140, New ZealandSchool of Biological Sciences, Victoria University of Wellington, Wellington 6140, New ZealandSchool of Biological Sciences, Victoria University of Wellington, Wellington 6140, New ZealandDepartment of Plant Biology, The Carnegie Institution for Science, Stanford, CA 94305, USADepartment of Integrative Biology, Oregon State University, Corvallis, OR 97331, USASchool of Biological Sciences, Victoria University of Wellington, Wellington 6140, New ZealandThe cellular mechanisms responsible for the regulation of nutrient exchange, immune response, and symbiont population growth in the cnidarian–dinoflagellate symbiosis are poorly resolved. Here, we employed liquid chromatography–mass spectrometry to elucidate proteomic changes associated with symbiosis in <i>Breviolum minutum</i>, a native symbiont of the sea anemone <i>Exaiptasia diaphana</i> (‘Aiptasia’). We manipulated nutrients available to the algae in culture and to the holobiont <i>in hospite</i> (i.e., in symbiosis) and then monitored the impacts of our treatments on host–endosymbiont interactions. Both the symbiotic and nutritional states had significant impacts on the <i>B. minutum</i> proteome. <i>B. minutum in hospite</i> showed an increased abundance of proteins involved in phosphoinositol metabolism (e.g., glycerophosphoinositol permease 1 and phosphatidylinositol phosphatase) relative to the free-living alga, potentially reflecting inter-partner signalling that promotes the stability of the symbiosis. Proteins potentially involved in concentrating and fixing inorganic carbon (e.g., carbonic anhydrase, V-type ATPase) and in the assimilation of nitrogen (e.g., glutamine synthase) were more abundant in free-living <i>B. minutum</i> than <i>in hospite</i>, possibly due to host-facilitated access to inorganic carbon and nitrogen limitation by the host when <i>in hospite</i>. Photosystem proteins increased in abundance at high nutrient levels irrespective of the symbiotic state, as did proteins involved in antioxidant defences (e.g., superoxide dismutase, glutathione s-transferase). Proteins involved in iron metabolism were also affected by the nutritional state, with an increased iron demand and uptake under low nutrient treatments. These results detail the changes in symbiont physiology in response to the host microenvironment and nutrient availability and indicate potential symbiont-driven mechanisms that regulate the cnidarian–dinoflagellate symbiosis.https://www.mdpi.com/2076-2607/11/2/292<i>Breviolum minutum</i>proteomicssymbiosisfree-livingAiptasia |
| spellingShingle | Amirhossein Gheitanchi Mashini Clinton A. Oakley Sandeep S. Beepat Lifeng Peng Arthur R. Grossman Virginia M. Weis Simon K. Davy The Influence of Symbiosis on the Proteome of the <i>Exaiptasia</i> Endosymbiont <i>Breviolum minutum</i> Microorganisms <i>Breviolum minutum</i> proteomics symbiosis free-living Aiptasia |
| title | The Influence of Symbiosis on the Proteome of the <i>Exaiptasia</i> Endosymbiont <i>Breviolum minutum</i> |
| title_full | The Influence of Symbiosis on the Proteome of the <i>Exaiptasia</i> Endosymbiont <i>Breviolum minutum</i> |
| title_fullStr | The Influence of Symbiosis on the Proteome of the <i>Exaiptasia</i> Endosymbiont <i>Breviolum minutum</i> |
| title_full_unstemmed | The Influence of Symbiosis on the Proteome of the <i>Exaiptasia</i> Endosymbiont <i>Breviolum minutum</i> |
| title_short | The Influence of Symbiosis on the Proteome of the <i>Exaiptasia</i> Endosymbiont <i>Breviolum minutum</i> |
| title_sort | influence of symbiosis on the proteome of the i exaiptasia i endosymbiont i breviolum minutum i |
| topic | <i>Breviolum minutum</i> proteomics symbiosis free-living Aiptasia |
| url | https://www.mdpi.com/2076-2607/11/2/292 |
| work_keys_str_mv | AT amirhosseingheitanchimashini theinfluenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT clintonaoakley theinfluenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT sandeepsbeepat theinfluenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT lifengpeng theinfluenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT arthurrgrossman theinfluenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT virginiamweis theinfluenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT simonkdavy theinfluenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT amirhosseingheitanchimashini influenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT clintonaoakley influenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT sandeepsbeepat influenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT lifengpeng influenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT arthurrgrossman influenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT virginiamweis influenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi AT simonkdavy influenceofsymbiosisontheproteomeoftheiexaiptasiaiendosymbiontibreviolumminutumi |