Journal cover Journal topic
Biogeosciences An interactive open-access journal of the European Geosciences Union
Biogeosciences, 14, 901-920, 2017
© Author(s) 2017. This work is distributed
under the Creative Commons Attribution 3.0 License.
Research article
28 Feb 2017
Cyanobacterial endobionts within a major marine planktonic calcifier (Globigerina bulloides, Foraminifera) revealed by 16S rRNA metabarcoding
Clare Bird1, Kate F. Darling1,2, Ann D. Russell3, Catherine V. Davis3, Jennifer Fehrenbacher3,4, Andrew Free5, Michael Wyman6, and Bryne T. Ngwenya1 1School of Geosciences, University of Edinburgh, Grant Institute, The King's Buildings, James Hutton Road, Edinburgh, EH9 3FE, UK
2School of Geography and Geosciences, University of St Andrews, North Street, St Andrews, KY16 9AL, UK
3Earth and Planetary Sciences, University of California Davis, 2119 Earth and Physical Sciences, One Shields Avenue, Davis, CA 95616, USA
4College of Earth, Ocean, and Atmospheric Sciences, Oregon State University, Corvallis, OR 97331, USA
5School of Biological Sciences, University of Edinburgh, Roger Land Building, The King's Buildings, Alexander Crum Brown Road, Edinburgh, EH9 3FF, UK
6Biological and Environmental Sciences, Faculty of Natural Sciences, Cottrell Building, University of Stirling, Stirling, FK9 4LA, UK
Abstract. We investigated the possibility of bacterial symbiosis in Globigerina bulloides, a palaeoceanographically important, planktonic foraminifer. This marine protist is commonly used in micropalaeontological investigations of climatically sensitive subpolar and temperate water masses as well as wind-driven upwelling regions of the world's oceans. G. bulloides is unusual because it lacks the protist algal symbionts that are often found in other spinose species. In addition, it has a large offset in its stable carbon and oxygen isotopic compositions compared to other planktonic foraminifer species, and also that predicted from seawater equilibrium. This is suggestive of novel differences in ecology and life history of G. bulloides, making it a good candidate for investigating the potential for bacterial symbiosis as a contributory factor influencing shell calcification. Such information is essential to evaluate fully the potential response of G. bulloides to ocean acidification and climate change. To investigate possible ecological interactions between G. bulloides and marine bacteria, 18S rRNA gene sequencing, fluorescence microscopy, 16S rRNA gene metabarcoding and transmission electron microscopy (TEM) were performed on individual specimens of G. bulloides (type IId) collected from two locations in the California Current. Intracellular DNA extracted from five G. bulloides specimens was subjected to 16S rRNA gene metabarcoding and, remarkably, 37–87 % of all 16S rRNA gene sequences recovered were assigned to operational taxonomic units (OTUs) from the picocyanobacterium Synechococcus. This finding was supported by TEM observations of intact Synechococcus cells in both the cytoplasm and vacuoles of G. bulloides. Their concentrations were up to 4 orders of magnitude greater inside the foraminifera than those reported for the California Current water column and approximately 5 % of the intracellular Synechococcus cells observed were undergoing cell division. This suggests that Synechococcus is an endobiont of G. bulloides type IId, which is the first report of a bacterial endobiont in the planktonic foraminifera. We consider the potential roles of Synechococcus and G. bulloides within the relationship and the need to determine how widespread the association is within the widely distributed G. bulloides morphospecies. The possible influence of Synechococcus respiration on G. bulloides shell geochemistry is also explored.

Citation: Bird, C., Darling, K. F., Russell, A. D., Davis, C. V., Fehrenbacher, J., Free, A., Wyman, M., and Ngwenya, B. T.: Cyanobacterial endobionts within a major marine planktonic calcifier (Globigerina bulloides, Foraminifera) revealed by 16S rRNA metabarcoding, Biogeosciences, 14, 901-920, doi:10.5194/bg-14-901-2017, 2017.
Publications Copernicus
Short summary
Accurate ecological data on planktic foraminifera (calcifying microbes that play an important role in the carbon cycle) are important for modelling their response to climate change. We studied the species G. bulloides. A lack of algal symbionts and unusual shell chemistry suggest a different life history compared to other spinose species. We demonstrate that G. bulloides hosts cyanobacterial endobionts. This has implications for modelling this species and for understanding its shell chemistry.
Accurate ecological data on planktic foraminifera (calcifying microbes that play an important...