Effects of heavy metal pollution (Fe, Mn, Ni) on the large benthic foraminifera Amphistegina lobifera: implications for metabolic function and coevolved host-endosymbiont interactions

Foraminifera are remarkably diverse unicellular eukaryotes that inhabit almost all marginal marine environments and perform crucial functions for a multitude of biotic and abiotic processes. Large benthic foraminifera (LBF) such as Amphistegina lobifera are essential contributors to marine carbon and nitrogen cycling, carbon sequestration, and overall biomass in their corresponding ecosystems. Furthermore, many LBF - including A. lobifera – have obligate photosymbiotic relationships with microalgae (predominantly diatoms of the family Fragilariaceae), which assist in the formation of the foraminifera’s calcareous shell.

Shallow marine habitats are often severely impacted by anthropogenic activities due to the introduction of multiple organic and inorganic pollutants by agricultural, domestic, and industrial sources. Among these pollutants, heavy metals are particularly problematic because of their toxicity and long-lasting impact on affected environments. We exposed 140 A. lobifera individuals to various concentrations of selected metals (Fe, Mn, Ni) to evaluate possible effects on their metabolism. During incubation, the cultures were provided with ¹³C- and ¹⁵N-labeled microalgae as a food source, which allows for the quantification of food uptake and metabolic activity via isotope-ratio mass spectrometry. For assessing the health of the photobionts, both the maximum quantum efficiency of photosystem II and photoactive area were measured via pulse-amplitude modulation fluorescence imaging. This novel combination of analytical methods allowed us to examine the complex host-endosymbiont reactions to heavy metal pollution in detail.

Within the first 10 days of contaminant exposure, almost all incubated individuals exhibited a reduction in C and N ingestion, as well as a decline in photosynthetic area and maximum quantum yield. Conversely, after 15 days of incubation an increase in food C and especially N uptake was noticeable in certain cultures, while the activity and health of the photobionts further declined. This metal-specific decoupling between host and photosymbiont implies differential stress tolerance of the partners towards environmental pollutants and exemplifies the necessity for further research in order to fully understand the implications of anthropogenic pollution in coastal marine areas for marine microbial communities.