BENTHIC FORAMINIFERA WITH ANAEROBIC MICROBIAL-LIKE METABOLISMS PROVIDE HYPOTHETICAL INSIGHTS INTO EARLY MICROEUKARYOTE EVOLUTION

Abiotic factors play vital roles in shaping ecosystems, biodiversity and evolution. Ecological, cytological and biochemical studies demonstrate several benthic foraminiferal (foram) species are facultative anaerobes, and they and/or their symbionts are often able to perform complete denitrification. Such attributes raise many questions in micropaleontology and microbiology: If the foram proper performs nitrate respiration and anaerobic energy metabolism, did the group descend from early microeukaryotes that emerged before the Great Oxidation Event? Are forams able to denitrify or are microbial associates (symbionts) performing denitrification, a process classically considered to be exclusively bacterial? Are there additional oxygen-independent energy-producing metabolic pathways performed by forams? We will discuss our recent (meta)transcriptomic results for two abundant, but cytologically distinct, benthic forams from the severely hypoxic to anoxic Santa Barbara Basin (CA, USA). Bolivina argentea is highly abundant in sediments typically beneath low-oxygen (~10µM O₂) waters while Nonionella stella is highly abundant in severely depleted (0.1µM O₂) to anoxic sediments. Both taxa expressed genes for denitrification and anaerobic energy metabolism regardless of environmental conditions (variables: O₂, H₂S, nitrate, hydrogen peroxide). While we know a thriving N. stella population living far below the euphotic zone (>500m) sequesters diatom chloroplasts, ‘omics has only recently revealed that these chloroplasts are species specific and their genome is nearly completely expressed, raising questions about kleptoplast function and roles. Might the kleptoplasts provide essential services to the host beyond classic photosynthesis? Results suggest that early forams or their ancestors originated in an anoxic milieu. The ability of at least two benthic forams to perform multiple oxygen-independent energy metabolisms suggests these protists still depend on metabolisms similar to bacteria and archaea. The complexity of foram metabolic and cellular structure suggests that this deep eukaryotic lineage may have impacted Earth’s Neoproterozoic ecosystem. Funded by US NSF IOS 1557430 (WHOI, JB, CH, SW) & 1557566 (URI, YZ).