Cadmium impairs gliding motility of a soil diatom through maladaptive feedback

Abstract

Diatom gliding motility is a key functional trait that enables soil diatoms to exploit heterogeneous microhabitats and contributes to essential ecosystem functions such as extracellular polymeric substance (EPS) secretion and soil aggregation. However, how heavy metal contamination affects this behavior remains poorly understood. Here, we investigated the responses of the soil diatom Mayamaea densestriata to environmentally relevant cadmium (Cd) concentrations by integrating physiological measurements, ultrastructural observations, transcriptomic analyses, and recovery experiments. Low Cd exposure (1.0 mg L −1 ) significantly reduced gliding motility while physiological performance remained largely unaffected, whereas higher Cd concentrations (2.5 mg L −1 ) impaired both motility and photosynthetic activity. Ultrastructural analyses revealed that Cd induced the formation of EPS–silica granules on the valve surface and within the raphe slit, physically obstructing cell movement. Transcriptomic analyses showed coordinated upregulation of cytoskeletal motor proteins and EPS biosynthesis genes despite continued motility decline, suggesting a maladaptive response in which transcriptional activation failed to restore motility and instead reinforced raphe obstruction. Recovery experiments further demonstrated that prolonged Cd exposure reduced growth resilience after contaminant removal, indicating persistent intracellular impairment beyond reversible surface blockage. Together, these findings reveal a previously unrecognized mechanism by which Cd disrupts the ecological functioning of soil diatoms through coupled physical and physiological constraints on motility. Our study provides new insight into how heavy metal contamination alters the behavior of soil microorganisms and highlights gliding motility as a sensitive functional trait linking contaminant exposure with soil ecosystem functioning.