Pespeni MH and Lloyd MM (2023), Sea stars resist wasting through active immune ...

ECB-ART-51322

Proc Biol Sci 2023 Jul 12;2902002:20230347. doi: 10.1098/rspb.2023.0347.

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Sea stars resist wasting through active immune and collagen systems.

Pespeni MH , Lloyd MM .

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Epidemics are becoming more common and severe, however, pinpointing the causes can be challenging, particularly in marine environments. The cause of sea star wasting (SSW) disease, the ongoing, largest known panzootic of marine wildlife, is unresolved. Here, we measured gene expression longitudinally of 24 adult Pisaster ochraceus sea stars, collected from a recovered site, as they remained asymptomatic (8 individuals) or naturally progressed through SSW (16 individuals) in individual aquaria. Immune, tissue integrity and pro-collagen genes were more highly expressed in asymptomatic relative to wasting individuals, while hypoxia-inducible factor 1-α and RNA processing genes were more highly expressed in wasting relative to asymptomatic individuals. Integrating microbiome data from the same tissue samples, we identified genes and microbes whose abundance/growth was associated with disease status. Importantly, sea stars that remained visibly healthy showed that laboratory conditions had little effect on microbiome composition. Lastly, considering genotypes at 98 145 single-nucleotide polymorphism, we found no variants associated with final health status. These findings suggest that animals exposed to the cause(s) of SSW remain asymptomatic with an active immune response and sustained control of their collagen system while animals that succumb to wasting show evidence of responding to hypoxia and dysregulation of RNA processing systems.

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	Figure 1. . Differences in gene expression between asymptomatic and wasting sea stars in common garden conditions. Log-normalized expression of three immune-related genes upregulated in asymptomatic samples relative to wasting (a) and three transcription and translation-related genes upregulated in wasting samples relative to asymptomatic (b). GO categories enriched by genes upregulated (orange) or downregulated (purple) in asymptomatic individuals compared to wasting individuals, summarized by biological process (c). The fraction preceding the GO term indicates the number of genes annotated with the term that pass p-value threshold of 0.05. (d) Density plots of the Wald's test statistic of each gene in the differential expression analysis comparing wasting to asymptomatic animals. Transcripts with annotations related to collagen (orange) are separated from all other transcripts (grey). Negative test statistic values indicate lower gene expression in samples from wasting relative to asymptomatic individuals.
	Figure 2. . Differences in gene expression of (a) HIF-1-α (padj < 0.001) and (b) collagenase 3, matrix metalloproteinase-13 (padj < 0.0001) for asymptomatic and wasting sea stars. Each point represents expression from a biopsy.
	Figure 3. . Differences in gene expression between asymptomatic, early-stage and late-stage wasting individuals. (a) Principal component analysis plot of transcript expression in samples taken from asymptomatic individuals (orange), early-stage disease animals (teal) or late-stage disease animals (blue). Ellipses are drawn around each group's centroid (confidence interval, 0.95). (b) Biological process GO categories enriched by genes upregulated (orange) or downregulated (green) in asymptomatic versus early-stage wasting individuals. The size and boldness of the font indicates the significance of the term as indicated by the legend. The fraction preceding the GO term indicates the number of genes annotated with the term that pass an unadjusted p-value threshold of 0.05. (c) Biological process GO categories enriched by genes upregulated (orange) or downregulated (blue) in asymptomatic versus late-stage wasting individuals.
	Figure 4. . Growth/abundances of correlated transcripts and microbes. Heatmap of normalized expression/abundance of all transcripts and OTUs per sample in the black module identified by WGCNA. Rows are annotated pink for genes or green for OTUs. Columns are annotated yellow for asymptomatic, teal for early-stage wasting or blue for late-stage wasting individuals.
	Figure 5. . Resilience and stability of the microbiome of asymptomatic sea stars through time in laboratory conditions. (a) Time course of microbiome composition of the eight sea stars that remained visibly asymptomatic through the duration of the experiment; (b) minimal changes in community composition in pairwise comparisons across days (weighted Unifrac PERMANOVA pseudo-F = 0.938, p = 0.489).

References [+] :

Aalto, Models with environmental drivers offer a plausible mechanism for the rapid spread of infectious disease outbreaks in marine organisms. 2020, Pubmed, Echinobase