Unraveling Hypoxia Tolerance: Transcriptomic and Metabolic Insights from Lucinoma capensis in an Oxygen Minimum Zone

Abstract

The lucinid clam Lucinoma capensis thrives at the oxygen minimum zone margins in the Benguela Upwelling System, where oxygen levels fluctuate dramatically. Understanding its adaptation to such extreme conditions provides key insights into survival strategies under fluctuating oxygen availability. We investigated the transcriptomic and metabolomic responses of L. capensis under normoxia, hypoxia, and recovery, focusing on the gills and digestive gland. Our findings highlight distinct organ-specific responses, with the gills showing strong transcriptional changes to oxygen fluctuations, in contrast to the more stable profile observed in the digestive gland. Under hypoxic conditions, the gills exhibited coordinated downregulation of critical metabolic processes, including protein synthesis, transposable element activity, and immune function, suggesting a tightly regulated energy conservation strategy and mechanisms to preserve symbiont stability and genomic integrity. Activation of prokaryotic metabolism in the gills supports the symbionts role in host energy acquisition and sulfide detoxification during hypoxia. In contrast, the digestive gland showed minimal transcriptional shifts during anoxia, with upregulation of pathways supporting structural maintenance. Upon reoxygenation, the gills displayed an active and asymmetric recovery, characterized by rapid restoration of protein synthesis and gradual normalization of protein degradation and immune functions. Despite significant transcriptomic changes, the metabolome remained largely stable, reflecting L. capensiss resilience to oxygen fluctuations. However, an overshoot in TCA cycle intermediates and derepression of previously downregulated pathways indicate that reoxygenation involves active metabolic reprogramming, not merely a return to baseline. This study highlights the specialized tissue responses and symbiotic contributions that enable L. capensis to thrive in one of the oceans most challenging environments.