Modelling sponge-symbiont metabolism

Abstract

Marine sponges are increasingly being recognised for their nutrient cycling ecosystem services, linking pelagic nutrients with the benthic ecosystem. Furthermore, sponges are the most prolific producers of bioactive secondary metabolites in the marine environment. Despite their ecological and commercial value, little is know about the metabolic processes that are responsible. The inability to produce sufficient sponge biomass, and thus specific bioactive compounds, has been repeatedly identified as a major bottleneck towards commercialising sponge holobiont derived drugs. Likewise, nutrient cycling by sponges has been a relatively recent advancement in marine ecology and the scale of this process is unknown. This thesis takes a systems approach to understanding sponge-symbiont metabolic processes by utilising the genomic resources available for the demosponge Amphimedon queenslandica and its bacterial symbiont AqS1. Specifically, I undertake genome-scale modelling and metabolic flux analyses to investigate the metabolic networks present in this sponge as well as its associated vertically-transmitted microbial symbiont. The goal of this thesis is to generate the data required for, and subsequently develop, a dual-species genome-scale metabolic model for A. queenslandica and AqS1. This will provide a framework to further our understanding of how sponges produce their biomass while living in an oligotrophic, tropical reef environment.To develop a genome-scale metabolic model, the biochemical composition of the organism must first be determined. Knowledge of the relative quantities of macromolecules and their respective building blocks (e.g. protein and amino acids) is vital, as each requires different substrates, enzymes and cofactors for their synthesis. I adapted and developed methods to characterise the composition and abundance of DNA, RNA, protein, lipids and carbohydrates in a marine sponge. These methods are described in detail that allows them to be easily transferred to other, non-model, large marine organisms. This is followed by a detailed analysis of A. queenslandica's macromolecular, amino acid, fatty acid and sterol composition. The biochemical data from this chapter was used to generate a biomass equation that represent the average composition of adult A. queenslandica in the metabolic model. 3To understand how the metabolic network may work towards producing more biomass, it must be considered in the context of the environmental conditions that naturally constrain growth. The dominant environmental constraint on growth on an oligotrophic reef system is nutrient availability.The abundance of key elements, such as carbon and nitrogen, were quantified throughout the course of a year. To investigate effects on the sponge of any changes in nutrient availability, I concurrently sampled sponges and analysed their biochemical composition to the macromolecular level. Chapter 4 presents these data and discusses a number of trends and correlations in the biochemical composition of the sponges with chan...

An Integrative Model of Carbon and Nitrogen Metabolism in a Common Deep-Sea Sponge (Geodia barretti)

“…Such models are underexplored to quantify sponge-symbiont metabolism, despite their potential to elucidate the intricacies of the sponge physiology and their ecological significance. To date, only one study that employs a genomescale metabolic network model to reconstruct biochemical conversions in the sponge-symbiont system of the tropical sponge Amphimedon queenslandica exists (Watson, 2017). In our study, we applied the metabolic network model to quantify internal and unconstrained C, N, and O 2 fluxes of the common and abundant deep-sea G. barretti holobiont.…”