Microplastic-induced transcriptional stress in the filter-feeding ciliate Stentor coeruleus: A novel avenue for understanding unicellular responses

Polystyrene microplastics, as emerging environmental contaminants, have exerted widespread impacts on multicellular organisms in aquatic ecosystems. However, little is known about how they affect ecologically crucial unicellular eukaryotes, especially filter-feeding ciliates that connect the microbial and classical trophic networks in aquatic environments. Here, we investigated the filter-feeding ciliate Stentor coeruleus as a model organism, revealing that it exhibited strong survival capabilities under high-concentration microplastic stress, with phenotypic changes limited to altered pigment production and reduced predatory capacity. Notably, these phenotypes returned to normal within 24 h after microplastic removal, indicating a reversible adaptation mechanism. Our transcriptomic profiling revealed that microplastics activate redox stress responses in S. coeruleus, including the upregulation of key oxidoreductase genes (e.g., GST, GPx, SOD, and aldo-keto reductases), modulation of lipid metabolism, membrane protein modification, proteostasis maintenance (mediated by HSP70, DnaJ, and ubiquitin-related genes), and xenobiotic clearance through upregulation of the ABC transporter family. Furthermore, our feeding recovery experiments provide the first evidence that short-term exposure to high microplastic concentrations, despite not affecting survival rates, significantly disrupts energy transfer efficiency within microbial food webs. Overall, these results uncover the underlying molecular mechanisms and offer a novel ecological perspective on the threat posed by microplastics to microbial food webs.