Niche-specific metabolic adaptation in biotrophic and necrotrophic oomycetes is manifested in differential use of nutrients, variation in gene content, and enzyme evolution

Abstract

The use of host nutrients to support pathogen growth is central to disease. We addressed the relationship between metabolism and trophic behavior by comparing metabolic gene expression during potato tuber colonization by two oomycetes, the hemibiotroph Phytophthora infestans and the necrotroph Pythium ultimum . Genes for several pathways including amino acid, nucleotide, and cofactor biosynthesis were expressed more by Ph . infestans during its biotrophic stage compared to Py . ultimum . In contrast, Py . ultimum had higher expression of genes for metabolizing compounds that are normally sequestered within plant cells but released to the pathogen upon plant cell lysis, such as starch and triacylglycerides. The transcription pattern of metabolic genes in Ph . infestans during late infection became more like that of Py . ultimum , consistent with the former's transition to necrotrophy. Interspecific variation in metabolic gene content was limited but included the presence of γ-amylase only in Py . ultimum . The pathogens were also found to employ strikingly distinct strategies for using nitrate. Measurements of mRNA, 15 N labeling studies, enzyme assays, and immunoblotting indicated that the assimilation pathway in Ph . infestans was nitrate-insensitive but induced during amino acid and ammonium starvation. In contrast, the pathway was nitrate-induced but not amino acid-repressed in Py . ultimum . The lack of amino acid repression in Py . ultimum appears due to the absence of a transcription factor common to fungi and Phytophthora that acts as a nitrogen metabolite repressor. Evidence for functional diversification in nitrate reductase protein was also observed. Its temperature optimum was adapted to each organism's growth range, and its K m was much lower in Py . ultimum . In summary, we observed divergence in patterns of gene expression, gene content, and enzyme function which contribute to the fitness of each species in its niche.

Carbon metabolism, transcriptome and RNA editome in developmental paths differentiation ofCoprinopsis cinerea

“…Vegetative mycelium grows in changeable environment and it is in charge of primary occupation of new habitat. The Agaricales-specific and species unique genes are very likely to benefit the fungus on niche segmentation and adapting to the complex and changing environment during vegetative growth (38, 67, 68). High expression on species-specific genes and relative lower selective pressure of purifying selection enable mycelium to minimize the interspecific competition and improve fitness (69).…”

Conserved Subgroups of the Plant-Specific RWP-RK Transcription Factor Family Are Present in Oomycete Pathogens

“…Plant-pathogenic oomycetes comprise approximately 200 formal and provisional species of the genus Phytophthora, which are arguably the most devastating pathogens of dicotyledonous plants, as well as downy mildew and Pythium species (Kamoun, 2003;Yang et al, 2017). Gene transcriptional regulation has been well characterized as an important biological process necessary for successful infection and normal sexual and asexual development in several oomycete plant pathogens (Wang et al, 2011;Ye et al, 2011;Ah-Fong et al, 2019). Genomic and functional analyses have identified several novel promoters (Mcleod et al, 2004;Xiang et al, 2009;Roy et al, 2013), TFs (Xiang and Judelson, 2010;Ye et al, 2013;Pham et al, 2018), and regulatory non-coding RNAs (Jia et al, 2017;Wang Y. et al, 2018), indicating that a number of transcriptional regulatory components and mechanisms are relatively specific to oomycetes in comparison to other eukaryotic organisms; however, detailed analyses are still largely lacking.…”

Uncovering oomycete metabolism using systems biology

“…This can be indicative for a nutrient transporter on the plasma membrane that is capable of transporting the respective metabolite. In addition, radioactively labelled metabolites can be added to the medium to test the assimilation of specific nutrients (Ah-Fong et al, 2019), such as carbohydrates and lipids. For metabolites for which changes in abundance are measured, uptake and demand (transport) reactions should be added to the model.…”

“…This suggests a similar magnitude of expansions/contractions of gene families encoding metabolic enzymes (metabolic gene families) for most species, resulting in similar-sized sets of metabolic enzymes in the proteomes. It should be noted, however, that these numbers do not provide insight into the metabolic capacity of each species, as the size of a metabolic gene family is just one of the many factors that determine the metabolic fluxes of an organism (Ah-Fong et al, 2019). Factors such as (post-)transcriptional/translational regulation, reaction stoichiometry, enzyme activity, pH, and temperature all contribute to the physiological state of an organism (Wegner et al, 2015).…”

“…Apparently, oomycetes rapidly evolved into highly divergent species that vary in growth substrates and lifestyle (Danies et al, 2013;Hodgson, 1958;Leesutthiphonchai et al, 2018) and they have the capacity to readily adapt to the environment, to overcome host resistance, or to develop fungicide resistance (Derevnina, Petre, et al, 2016;Matson et al, 2015). It is conceivable that many of these adaptations are driven by a pathogenic lifestyle (Ah-Fong et al, 2019). The genome dynamics also translate into fundamental differences in metabolism (Judelson, 2017).…”