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

Bruno Jesus,Erik C L Trampe,Anders Meibom,Emmanuelle Geslin,Johannes W Goessling,Michael Kühl,Thierry Jauffrais,Charlotte Lekieffre

doi:10.1038/s41396-021-01128-0

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.

Highlights

Foraminifera are unicellular eukaryotes that contribute significantly to the carbon and nitrogen biogeochemical cycles in marine habitats
Mixotrophic growth involving the acquisition and functionalization of prey chloroplasts in the host is a widespread trait among protists [24,25,26, 74], which can have a significant impact in the microbial food web [26]
The two foraminiferal species H. germanica and E. williamsoni showed differences in feeding mechanisms and in kleptoplast functionality suggesting that both species are capable of sustaining active chloroplasts but with different functionality levels

Summary

Introduction

Foraminifera are unicellular eukaryotes that contribute significantly to the carbon and nitrogen biogeochemical cycles in marine habitats. Foraminifera employ a diversity of feeding and behavioural strategies encompassing heterotrophic, autotrophic and mixotrophic life styles [6,7,8,9,10,11] This wide range of feeding strategies increases their capacity to occupy different ecological niches, allowing foraminifera to be found in most marine environments ranging from shallow-water to deep-sea basins and open oceans [12, 13]. Some benthic foraminifera are capable of sequestering chloroplasts from their microalgal food source, i.e. diatoms [5, 14,15,16] and retain them photosynthetically active in their cytosol [15, 17,18,19] This process of sequestering and exploiting foreign plastids is referred to as kleptoplastidy [20] and has been extensively studied in sacoglossan gastropods e.g. Foraminiferal kleptoplasts exhibit different functionality levels and different retention times in the host cell, ranging from a short lifetime (24–48 h)—with none or little photosynthetic functionality—to longer (>2 weeks to 3 months) associations with the foraminiferal host showing high kleptoplast activity [15, 18, 19, 33]

Methods

Results

Conclusion