The red seaweed Asparagopsis taxiformis genome and integrative -omics analysis

Abstract

Abstract Seaweeds (marine macroalgae) are crucial to the functioning of healthy coastal ecosystems and global biogeochemical cycles, and sometimes provide novel solutions to help mitigate climate change. The red seaweed Asparagopsis taxiformis (Bonnemaisoniaceae, Rhodophyta) produces bioactive natural products that, when fed to cattle and sheep, can eradicate methane emissions from these livestock. However, in order to cultivate enough A. taxiformis to have a meaningful impact on global greenhouse gas emissions, we need to improve our understanding of the biology of this new crop. In this study, we used a domesticated diploid sporophyte (> 1.5 years in culture, with relatively low microbial diversity) to establish a high-quality draft nuclear genome for A. taxiformis from Queensland, Australia. The A. taxiformis lineage was confirmed as Lineage 6 (L6) based upon phylogenetic analysis (Cox2-3 spacer). The genome of A. taxiformis (L6) was 142 Mb in size with approximately 11,000 protein-coding genes, including those associated with secondary metabolism, photosynthesis and defence, and the assembly contained 70.67% repeat regions. Based on protein domain analysis, the most prominent lineage-specific duplications belonged to those containing WD repeat proteins, as well as bestrophin and N6_N4_Mtase domain proteins. Cultured (domesticated) A. taxiformis (L6) sporophytes contained 4-times more bromoform (the key anti-methanogenic natural product) compared to wild sporophytes. To obtain information regarding associated molecular differences, the genome was used as a reference to explore differential gene expression related to environment. Cultured sporophytes demonstrated an enrichment of regulatory factors (kinases, transcription factors), whereas wild sporophytes were enriched with defence and stress-related genes, including those involved in protein folding (heat shock proteins) and halogenated metabolite production. Wild sporophytes also expressed a relatively high level of novel secreted proteins, with similarity to collagen-alpha proteins (termed rhodophyte collagen-alpha-like proteins, RCAPs). Proteomic investigation of the genome of cultured sporophytes, resulting in the identification of over 400 proteins, including RCAPs, as well as numerous enzymes and phycobiliproteins, which will facilitate future functional characterisation. In summary, as the most comprehensive genomic resource for any Asparagopsis species, this resource provides a gateway for seaweed researchers to fast-track the development and production of Asparagopsis to meet demand by agriculture and do so with economic and environmental agility.