The link between Fungal nutrition and Fungal Phenotype

Abstract

Carbon and nitrogen are key macro-nutrients affecting growth and fitness particularly in heterotrophic organisms. A considerable body of evidence suggests that many organisms including mammals, insects and slime moulds have a target intake that is optimal in the sense of maximising growth or ecological fitness. In nutritionally heterogeneous environments, these organisms show an ability to regulate the intake of carbon (C) and nitrogen (N) compounds by selecting different food types to reach the target ratio. This is now a major focus of research in diet-related chronic disease in humans including obesity. Fungi are one of the most important components of the terrestrial ecosystem, and play a key role in nutrient cycling, structural genesis, water infiltration and carbon storage in soil. The manner in which the fungal phenotype emerges in response to the complex nutritional environment of soil is fundamental to the persistence of these functions across space and time. We explore the extent to which the fungal phenotype can be understood in terms of a target ratio of C: N. We used the fungus Mucor mucedo as the model species, and studies its growth in different nutrient regimes by varying the C: N ratio, and including both organic and inorganic sources of nitrogen. There is evidence for a target C: N ratio in a homogeneous environment, although growth rate remains high over a relatively broad range in the ratio by comparison with other organisms. We attribute this to the capacity of fungi to recycle and translocate internal sources of nutrients to regions of high demand. In a heterogeneous environment, we provide evidence that this is the case, although nitrogen is more readily translocated than carbon in this species. In this study, a comparison of growth rate for different C: N ratios and nutrient concentrations indicates efficiency, the amplitude of the oscillations is a measure of stability. This provides an important constraint for our understanding of underlying regulatory pathways linking C and N to growth. A hyphal-level II model for fungal growth is developed to study the consequences of our findings for the emergence of the fungal phenotype, and is used to generate new hypotheses for future testing. Finally, a metabolic model is constructed that synthesises existing knowledge of carbon and nitrogen pathways in cells. We built two versions of this network model corresponding to the case of organic and inorganic sources of nitrogen respectively. Both models reproduced oscillatory growth observed in the laboratory experiments and, consistent with observation, the amplitude of the oscillations is positively correlated with the C: N ratio only for the inorganic N version of the model. A peak C: N ratio for fungal growth is also only predicted for inorganic sources of N, as we saw in the observed behaviour. The networks we built for this project may be highly conserved across the kingdom of life, therefore the models may be broadly applicable with certain modifications.