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, 15N 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 Km 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.
Highlights
The most fundamental characteristic of microbial pathogenesis is the use of host nutrients to support pathogen growth [1, 2]
Understanding how host nutrients are used by pathogens may lead to strategies for limiting disease, for example by developing inhibitors of metabolic pathways needed for pathogen growth
A comparison was made between the metabolism of Phytophthora infestans and Pythium ultimum during potato tuber colonization
Summary
The most fundamental characteristic of microbial pathogenesis is the use of host nutrients to support pathogen growth [1, 2]. Trophic lifestyles of plant pathogens have been categorized as biotrophic when the host stays alive during the nutrient exchange, or necrotrophic when the pathogen kills and feeds on the remains of plant cells [3]. Smaller changes include mutations that modify regulatory proteins, alter promoter activity, or change the substrate affinity, reaction kinetics, or allosteric regulation of an enzyme [8,9,10,11]. Such mutations occur spontaneously within pathogen populations and when selected may help tune metabolism to a lifestyle, environment, or new host
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