Symbiodinium-Induced Formation of Microbialites: Mechanistic Insights From in Vitro Experiments and the Prospect of Its Occurrence in Nature
Dinoflagellates in the genus Symbiodinium exhibit a variety of life styles, ranging from mutualistic endosymbioses with animal and protist hosts to free-living life styles. In culture, Symbiodinium spp. and naturally associated bacteria are known to form calcifying biofilms that produce so-called sy...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-05-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2018.00998/full |
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| author | Jörg C. Frommlet Daniel Wangpraseurt Daniel Wangpraseurt Maria L. Sousa Bárbara Guimarães Mariana Medeiros da Silva Michael Kühl Michael Kühl João Serôdio |
| author_facet | Jörg C. Frommlet Daniel Wangpraseurt Daniel Wangpraseurt Maria L. Sousa Bárbara Guimarães Mariana Medeiros da Silva Michael Kühl Michael Kühl João Serôdio |
| author_sort | Jörg C. Frommlet |
| collection | DOAJ |
| description | Dinoflagellates in the genus Symbiodinium exhibit a variety of life styles, ranging from mutualistic endosymbioses with animal and protist hosts to free-living life styles. In culture, Symbiodinium spp. and naturally associated bacteria are known to form calcifying biofilms that produce so-called symbiolites, i.e., aragonitic microbialites that incorporate Symbiodinium as endolithic cells. In this study, we investigated (i) how algal growth and the combined physiological activity of these bacterial-algal associations affect the physicochemical macroenvironment in culture and the microenvironment within bacterial-algal biofilms, and (ii) how these interactions induce the formation of symbiolites. In batch culture, calcification typically commenced when Symbiodinium spp. growth approached stationary phase and when photosynthetic activity and its influence on pH and the carbonate system of the culture medium had already subsided, indicating that symbiolite formation is not simply a function of photosynthetic activity in the bulk medium. Physical disturbance of bacteria-algal biofilms, via repeated detaching and dispersing of the developing biofilm, generally impeded symbiolite formation, suggesting that the structural integrity of biofilms plays an important role in generating conditions conducive to calcification. Microsensor measurements of pH and O2 revealed a biofilm microenvironment characterized by high photosynthetic rates and by dynamic changes in photosynthesis and respiration with light intensity and culture age. Ca2+ microsensor measurements confirmed the significance of the biofilm microenvironment in inducing calcification, as photosynthesis within the biofilm induced calcification without the influence of batch culture medium and under environmentally relevant flow conditions. Furthermore, first quantitative data on calcification from 26 calcifying cultures enabled a first broad comparison of Symbiodinium-induced bacterial-algal calcification with other calcification processes. Our findings support the idea that symbiolite formation is a typical, photosynthesis-induced, bacterial-algal calcification process that is likely to occur under natural conditions. |
| first_indexed | 2024-12-12T16:35:59Z |
| format | Article |
| id | doaj.art-3c26f753736b418b852420cda78eb452 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-12T16:35:59Z |
| publishDate | 2018-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-3c26f753736b418b852420cda78eb4522022-12-22T00:18:39ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-05-01910.3389/fmicb.2018.00998335836Symbiodinium-Induced Formation of Microbialites: Mechanistic Insights From in Vitro Experiments and the Prospect of Its Occurrence in NatureJörg C. Frommlet0Daniel Wangpraseurt1Daniel Wangpraseurt2Maria L. Sousa3Bárbara Guimarães4Mariana Medeiros da Silva5Michael Kühl6Michael Kühl7João Serôdio8Department of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Aveiro, PortugalMarine Biological Section, Department of Biology, University of Copenhagen, Helsingør, DenmarkDepartment of Chemistry, University of Cambridge, Cambridge, United KingdomDepartment of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Aveiro, PortugalDepartment of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Aveiro, PortugalCoral Reef and Global Changes Research Group (RECOR), Department of Oceanography, Institute of Geosciences, Federal University of Bahia (UFBA), Salvador, BrazilMarine Biological Section, Department of Biology, University of Copenhagen, Helsingør, DenmarkClimate Change Cluster, University of Technology Sydney, Sydney, NSW, AustraliaDepartment of Biology and Centre for Environmental and Marine Studies (CESAM), University of Aveiro, Aveiro, PortugalDinoflagellates in the genus Symbiodinium exhibit a variety of life styles, ranging from mutualistic endosymbioses with animal and protist hosts to free-living life styles. In culture, Symbiodinium spp. and naturally associated bacteria are known to form calcifying biofilms that produce so-called symbiolites, i.e., aragonitic microbialites that incorporate Symbiodinium as endolithic cells. In this study, we investigated (i) how algal growth and the combined physiological activity of these bacterial-algal associations affect the physicochemical macroenvironment in culture and the microenvironment within bacterial-algal biofilms, and (ii) how these interactions induce the formation of symbiolites. In batch culture, calcification typically commenced when Symbiodinium spp. growth approached stationary phase and when photosynthetic activity and its influence on pH and the carbonate system of the culture medium had already subsided, indicating that symbiolite formation is not simply a function of photosynthetic activity in the bulk medium. Physical disturbance of bacteria-algal biofilms, via repeated detaching and dispersing of the developing biofilm, generally impeded symbiolite formation, suggesting that the structural integrity of biofilms plays an important role in generating conditions conducive to calcification. Microsensor measurements of pH and O2 revealed a biofilm microenvironment characterized by high photosynthetic rates and by dynamic changes in photosynthesis and respiration with light intensity and culture age. Ca2+ microsensor measurements confirmed the significance of the biofilm microenvironment in inducing calcification, as photosynthesis within the biofilm induced calcification without the influence of batch culture medium and under environmentally relevant flow conditions. Furthermore, first quantitative data on calcification from 26 calcifying cultures enabled a first broad comparison of Symbiodinium-induced bacterial-algal calcification with other calcification processes. Our findings support the idea that symbiolite formation is a typical, photosynthesis-induced, bacterial-algal calcification process that is likely to occur under natural conditions.https://www.frontiersin.org/article/10.3389/fmicb.2018.00998/fullSymbiodiniumcoral endosymbiontfree-living life stylebacterial-algal calcificationphotosynthesis-induced calcificationmicrobialite |
| spellingShingle | Jörg C. Frommlet Daniel Wangpraseurt Daniel Wangpraseurt Maria L. Sousa Bárbara Guimarães Mariana Medeiros da Silva Michael Kühl Michael Kühl João Serôdio Symbiodinium-Induced Formation of Microbialites: Mechanistic Insights From in Vitro Experiments and the Prospect of Its Occurrence in Nature Frontiers in Microbiology Symbiodinium coral endosymbiont free-living life style bacterial-algal calcification photosynthesis-induced calcification microbialite |
| title | Symbiodinium-Induced Formation of Microbialites: Mechanistic Insights From in Vitro Experiments and the Prospect of Its Occurrence in Nature |
| title_full | Symbiodinium-Induced Formation of Microbialites: Mechanistic Insights From in Vitro Experiments and the Prospect of Its Occurrence in Nature |
| title_fullStr | Symbiodinium-Induced Formation of Microbialites: Mechanistic Insights From in Vitro Experiments and the Prospect of Its Occurrence in Nature |
| title_full_unstemmed | Symbiodinium-Induced Formation of Microbialites: Mechanistic Insights From in Vitro Experiments and the Prospect of Its Occurrence in Nature |
| title_short | Symbiodinium-Induced Formation of Microbialites: Mechanistic Insights From in Vitro Experiments and the Prospect of Its Occurrence in Nature |
| title_sort | symbiodinium induced formation of microbialites mechanistic insights from in vitro experiments and the prospect of its occurrence in nature |
| topic | Symbiodinium coral endosymbiont free-living life style bacterial-algal calcification photosynthesis-induced calcification microbialite |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2018.00998/full |
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