The meta-transcriptome of a seaweed holobiont in culture: Linking gene expression with growth and senescence

Abstract

Aquaculture of the red seaweed genus Asparagopsis is rapidly expanding due to its potential to mitigate enteric methane emissions from cattle rumen. These developments include sea-based culture of gametophytes and land-based culture of tetrasporophytes. Successful establishment of land-based aquaculture relies on providing species-specific optimal conditions, including stocking density of the culture. However, an understanding of the gene expression across the Asparagopsis holobiont at different stocking densities is lacking. Here, we applied a meta-transcriptomic approach to investigate the gene expression of Asparagopsis taxiformis tetrasporophytes and their associated microbiome at different stocking densities ranging from 0.18 g FW L−1 to 5 g FW L−1. Overall, the specific growth rate of A. taxiformis decreased as stocking density increased (from 10.7 % day−1 to −0.2 % day−1). The highest density was characterised by downregulation of photosynthesis-related genes and upregulation of some putative defense-related genes in the seaweed. The microbial transcript abundance was positively correlated to stocking density, with prominent activity of Actinomycetes as seaweed growth rate slowed. Additionally, several microbial virulence factors such as OmpA were upregulated in the highest seaweed density. Altogether, our transcriptomic data suggested the onset of senescence in A. taxiformis cultured at the highest stocking density, although the appearance of the filaments was visibly unaffected. This “hidden” senescence was accompanied by a shift to virulence in the associated microbiome. The meta-transcriptome could therefore be used as a tool to monitor system health for commercial Asparagopsis farms. This work also demonstrates the potential of employing omics to assess optimal culture conditions of any seaweed species.