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

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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.

OriginalsprogEngelsk
TidsskriftISME Journal
Vol/bind16
Udgave nummer3
Sider (fra-til)822-832
Antal sider11
ISSN1751-7362
DOI
StatusUdgivet - 2022

Bibliografisk note

Funding Information:
The authors thank Romain Mallet for his help at the Imaging core facility (SCIAM) of the University of Angers (MEB images) and Sofie Jakobsen for her technical assistance during work in Denmark. TJ was funded by the “FRESCO” project, a project supported by the Region Pays de Loire and the University of Angers. CL was funded by the Swiss National Science Foundation (grant no. 200021_149333). The work was further supported by the French national programme CNRS EC2CO-LEFE project “ForChlo”, a French-Danish research collaboration grant of the Institut Français du Danemark (BJ, MK), a grant from the Independent Research Fund Denmark ǀ Technical and Production Sciences (MK; DFF-8022-00301B), an infrastructure grant from the Carlsberg Foundation (MK) and the BIO-Tide project, funded through the 2015–2016 BiodivERsA COFUND call for research proposals, with the national funders BelSPO, FWO, ANR and SNSF. The electron microscopy platform of the University of Lausanne is thanked for access to the equipment and technical assistance.

Publisher Copyright:
© 2021, The Author(s).

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