Evidence that non-pathogenic microorganisms drive sea star wasting disease through boundary layer oxygen diffusion limitation

Sea star wasting disease describes a condition affecting asteroids that resulted in significant Northeastern Pacific population decline following a mass mortality event in 2013. The etiology of sea star wasting is unresolved. We hypothesized that asteroid wasting is a sequela of microbial organic matter remineralization near respiratory surfaces which leads to boundary layer oxygen diffusion limitation (BLODL). Wasting lesions were induced in Pisaster ochraceus by enrichment with a variety of organic matter (OM) sources and by experimentally reduced oxygen conditions. Microbial assemblages inhabiting tissues and at the asteroid-water interface bore signatures of copiotroph proliferation before wasting onset, followed by the proliferation of putatively facultative and strictly anaerobic taxa. These results together illustrate that suboxic conditions at the animal-water interface may be established by heterotrophic bacterial activity in response to organic matter loading. Wasting susceptibility was significantly and positively correlated with rugosity, a key determinant of boundary layer thickness. At a semi-continuously monitored field site (Langley Harbor), wasting predictably occurred at annual peak or decline in phytoplankton biomass over 5 years, suggesting that primary production-derived OM may contribute to BLODL. Finally, wasting individuals from 2013 - 2014 bore stable isotopic signatures reflecting anaerobic processes which suggests that this phenomenon may have affected asteroids during mass mortality. The impacts of BLODL may be more pronounced under higher temperatures due to lower O2 solubility, in more rugose asteroid species due to restricted hydrodynamic flow, and in larger specimens due to their lower surface area to volume ratios which affects diffusive respiratory potential. Moreover, our results demonstrate that marine invertebrate disease may result from heterotrophic microbial activity that occurs adjacent to respiratory tissues, which raises important questions about the etiology of marine diseases in other benthic taxa.