Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease

Abstract

Sea star wasting (SSW) disease describes a condition affecting asteroids that resulted in significant Northeastern Pacific population decline following a mass mortality event in 2013. The etiology of SSW is unresolved. We hypothesized that SSW is a sequela of microbial organic matter remineralization near respiratory surfaces, one consequence of which may be limited O2 availability at the animal-water interface. Microbial assemblages inhabiting tissues and at the asteroid-water interface bore signatures of copiotroph proliferation before SSW onset, followed by the appearance of putatively facultative and strictly anaerobic taxa at the time of lesion genesis and as animals died. SSW lesions were induced in Pisaster ochraceus by enrichment with a variety of organic matter (OM) sources. These results together illustrate that depleted O2 conditions at the animal-water interface may be established by heterotrophic microbial activity in response to organic matter loading. SSW was also induced by modestly (∼39%) depleted O2 conditions in aquaria, suggesting that small perturbations in dissolved O2 may exacerbate the condition. SSW susceptibility between species was significantly and positively correlated with surface rugosity, a key determinant of diffusive boundary layer thickness. Tissues of SSW-affected individuals collected in 2013–2014 bore δ15N signatures reflecting anaerobic processes, which suggests that this phenomenon may have affected asteroids during mass mortality at the time. The impacts of enhanced microbial activity and subsequent O2 diffusion limitation 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.

Sea star wasting disease pathology in Pisaster ochraceus shows a basal-to-surface process affecting color phenotypes differently

“…Samples for this study were collected during a concurrent study on the impacts of organic matter enrichment on asteroid wasting (Aquino et al 2021) performed at Bodega Bay, California, USA, in July− August 2019. Pisaster ochraceus (n = 20; mean ± SE mass 303 ± 26 g) were haphazardly collected from the field (Bodega Jetty; 38.3332°N, 123.0481°W) and housed collectively in large (ca.…”

“…10 5 cells of the cultured microalga Dunaliella tertiolecta, and particulate organic matter (POM; > 0.2 μm filtrate) from 120 ml of seawater collected at Bodega Bay; 5 control sea stars received no treatment. These treatments were chosen because it was hypothesized that organic matter (OM), especially that originating from primary production, could result in SSWD signs by producing suboxic microzones through heterotrophic respiration near asteroid surfaces (Aquino et al 2021). Peptone is a common component of marine bacterial culture media and selects for copiotrophic marine taxa (Moebus 1980).…”

“…Inability to replicate disease using heat-treated filterable extracts from SSWD-affected sea stars (Hewson et al 2018) could be explained by heat denaturing and inactivation of sea star proteins that mediate stiffness of MCT. So while SSWD is widely assumed to be infectious (Aalto et al 2020), a non-infectious cause is equally plausible (Aquino et al 2021). Temperature anomalies (Eisenlord et al 2016, Kohl et al 2016, Menge et al 2016, Aalto et al 2020, meteorological conditions (Hewson et al 2018), and seawater pCO 2 concentration (Menge et al 2016) are hypothesized environmental drivers of SSWD disease outbreaks.…”

“…Here, we took advantage of an experiment investigating the impacts of organic matter enrichment on genesis of SSWD in Pisaster ochraceus (Aquino et al 2021), a species affected by SSWD throughout the Pacific coast of North America, to examine the tissue and hematological changes associated with disease. Specifically, the hypothesis of the experiment was that SSWD lesions could be reproduced by amending surfaces of sea stars with organic matter that would result in proliferation of microorganisms leading to subsequent anoxia near animal surfaces and generation of gross lesions of SSWD.…”

“…Specifically, the hypothesis of the experiment was that SSWD lesions could be reproduced by amending surfaces of sea stars with organic matter that would result in proliferation of microorganisms leading to subsequent anoxia near animal surfaces and generation of gross lesions of SSWD. The details of the experiment and microbial and metabolic results are presented elsewhere (Aquino et al 2021). Our objective here was to document the pathology of experimentally reproduced SSWD lesions, including in specimens that formed lesions in the absence of external stimuli.…”