Metabolic Adaptations of Benthic Forams: Foraminiferal Species Adaptations to Intertidal Mudflat Assessed by a Metabolic Approach

Abstract

Benthic foraminifera are characterized by their rapid response and high resistance to variable and extreme conditions such as those typically found in intertidal environments. However, knowledge of cellular and metabolic adaptations by foraminifera remains incomplete. Here we explore the metabolic profile of three species from an intertidal mudflat: Haynesina germanica (kleptoplast, mixotrophic), Elphidium oceanense, and Ammonia confertitesta (heterotrophic). Given the challenges associated with culturing foraminifera, specimens were collected directly from the field. To analyze their metabolic profiles, a non-targeted gas chromatography–mass spectrometry methodology was optimized with the aim of reducing sample size. We constructed a foraminifera-specific library containing 382 features. Within the 30 metabolites identified, those present in all three species include osmolytes, oxidant- and thermo-protective molecules, which are consistent with their high tolerance to variations in environmental conditions. Species-specific features were also observed. A. confertitesta accumulates myoinositol, aspartate, and asparagine. H. germanica accumulated malate, glycerate, and glycolate/glyoxylate, indicating concurrent activity of a C4-like carbon concentrating mechanism and photorespiratory metabolism. Our approach enabled us to discriminate between the species based on their metabolites and highlights two probable metabolic pathways not previously described in kleptoplast foraminifera. These metabolic adaptations likely contribute to the ecological success of intertidal foraminiferal species.