Kleptoplast distribution, photosynthetic efficiency and sequestration mechanisms in intertidal benthic foraminifera

Type Article
Date 2022-03
Language English
Author(s) Jesus BrunoORCID1, 2, Jauffrais ThierryORCID3, 4, Trampe Erik C. L.ORCID5, Goessling Johannes W.5, Lekieffre Charlotte6, Meibom AndersORCID7, 8, Kühl MichaelORCID5, Geslin Emmanuelle4
Affiliation(s) 1 : EA2160, Laboratoire Mer Molécules Santé, Université de Nantes, Nantes, France
2 : BioISI—Biosystems & Integrative Sciences Institute, Campo Grande University of Lisboa, Faculty of Sciences, Lisboa, Portugal
3 : Ifremer, IRD, Univ Nouvelle-Calédonie, Univ La Réunion, CNRS, UMR 9220 ENTROPIE, 101 Promenade Roger Laroque, 98897, Noumea, New Caledonia
4 : LPG UMR 6112, Univ Angers, Université de Nantes, CNRS, F-49000, Angers, France
5 : Marine Biological Section, Department of Biology, University of Copenhagen, Strandpromenaden 5, 3000, Helsingør, DK, Denmark
6 : Cell and Plant Physiology Laboratory, University of Grenoble Alpes, CNRS, CEA, INRAE, Grenoble, France
7 : Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering (ENAC), Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015, Lausanne, Switzerland
8 : Center for Advanced Surface Analysis, Institute of Earth Sciences, University of Lausanne, Lausanne, Switzerland
Source Isme Journal (1751-7362) (Springer Science and Business Media LLC), 2022-03 , Vol. 16 , N. 3 , P. 822-832
DOI 10.1038/s41396-021-01128-0
WOS© Times Cited 2
Abstract

Foraminifera are ubiquitously distributed in marine habitats, playing a major role in marine sediment carbon sequestration and the nitrogen cycle. They exhibit a wide diversity of feeding and behavioural strategies (heterotrophy, autotrophy and mixotrophy), including species with the ability of sequestering intact functional chloroplasts from their microalgal food source (kleptoplastidy), resulting in a mixotrophic lifestyle. The mechanisms by which kleptoplasts are integrated and kept functional inside foraminiferal cytosol are poorly known. In our study, we investigated relationships between feeding strategies, kleptoplast spatial distribution and photosynthetic functionality in two shallow-water benthic foraminifera (Haynesina germanica and Elphidium williamsoni), both species feeding on benthic diatoms. We used a combination of observations of foraminiferal feeding behaviour, test morphology, cytological TEM-based observations and HPLC pigment analysis, with non-destructive, single-cell level imaging of kleptoplast spatial distribution and PSII quantum efficiency. The two species showed different feeding strategies, with H. germanica removing diatom content at the foraminifer’s apertural region and E. williamsoni on the dorsal site. All E. williamsoni parameters showed that this species has higher autotrophic capacity albeit both feeding on benthic diatoms. This might represent two different stages in the evolutionary process of establishing a permanent symbiotic relationship, or may reflect different trophic strategies.

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How to cite 

Jesus Bruno, Jauffrais Thierry, Trampe Erik C. L., Goessling Johannes W., Lekieffre Charlotte, Meibom Anders, Kühl Michael, Geslin Emmanuelle (2022). Kleptoplast distribution, photosynthetic efficiency and sequestration mechanisms in intertidal benthic foraminifera. Isme Journal, 16(3), 822-832. Publisher's official version : https://doi.org/10.1038/s41396-021-01128-0 , Open Access version : https://archimer.ifremer.fr/doc/00728/83992/