Energy metabolism and regeneration are impaired by seawater acidification in the infaunal brittlestar Amphiura filiformis

Seawater acidification due to anthropogenic release of CO2 as well as the potential leakage of pure CO2 from sub-seabed carbon capture storage (CCS) sites may impose a serious threat to marine organisms. Although infaunal organisms can be expected to be particularly impacted by decreases in seawater pH, as a result of naturally acidified conditions in benthic habitats, information regarding physiological and behavioral responses is still scarce. Determination of P-O2 and P-CO2 gradients within burrows of the brittlestar Amphiura filiformis during environmental hypercapnia demonstrated that besides hypoxic conditions, increases of environmental P-CO2 are additive to the already high P-CO2 (up to 0.08 kPa) within the burrows. In response to up to 4 weeks exposure to pH 7.3 (0.3 kPa P-CO2) and pH 7.0 (0.6 kPa P-CO2), metabolic rates of A. filiformis were significantly reduced in pH 7.0 treatments, accompanied by increased ammonium excretion rates. Gene expression analyses demonstrated significant reductions of acid-base (NBCe and AQP9) and metabolic (G6PDH, LDH) genes. Determination of extracellular acid-base status indicated an uncompensated acidosis in CO2-treated animals, which could explain the depressed metabolic rates. Metabolic depression is associated with a retraction of filter feeding arms into sediment burrows. Regeneration of lost arm tissues following traumatic amputation is associated with significant increases in metabolic rate, and hypercapnic conditions (pH 7.0, 0.6 kPa) dramatically reduce the metabolic scope for regeneration, reflected in an 80% reduction in regeneration rate. Thus, the present work demonstrates that elevated seawater P-CO2 significantly affects the environment and the physiology of infaunal organisms like A. filiformis.