Genome‐wide characterization of Phytophthora infestans metabolism: a systems biology approach

Abstract

SUMMARYGenome-scale metabolic models (GEMs) provide a functional view of the complex network of biochemical reactions in the living cell. Initially mainly applied to reconstruct the metabolism of model organisms, the availability of increasingly sophisticated reconstruction methods and more extensive biochemical databases now make it possible to reconstruct GEMs for less wellcharacterized organisms, and have the potential to unravel the metabolism in pathogen-host systems. Here, we present a GEM for the oomycete plant pathogen Phytophthora infestans as a first step towards an integrative model with its host. We predict the biochemical reactions in different cellular compartments and investigate the gene-protein-reaction associations in this model to obtain an impression of the biochemical capabilities of P. infestans. Furthermore, we generate life stage-specific models to place the transcriptomic changes of the genes encoding metabolic enzymes into a functional context. In sporangia and zoospores, there is an overall down-regulation, most strikingly reflected in the fatty acid biosynthesis pathway. To investigate the robustness of the GEM, we simulate gene deletions to predict which enzymes are essential for in vitro growth. This model is an essential first step towards an understanding of P. infestans and its interactions with plants as a system, which will help to formulate new hypotheses on infection mechanisms and disease prevention.

Exchanges at the Plant-Oomycete Interface That Influence Disease

“…Regardless of where nutrients are acquired, plants contain myriad compounds to support pathogen growth. Metabolic models based on genome data indicate that most oomycetes can utilize the major plant hexoses, disaccharides, organic acids, starch, and sugar alcohols, although pentose utilization is restricted by the absence of arabinose isomerase (Rodenburg et al, 2018). Most oomycetes also can use the major nitrogen sources found in planta, including amino acids, ammonium, and nitrate.…”

A Genome-Scale Metabolic Reconstruction of Phytophthora infestans With the Integration of Transcriptional Data Reveals the Key Metabolic Patterns Involved in the Interaction of Its Host

“…A comparison was made between the model of Rodenburg et al ( 2017 ) (iSR1301) and the one produced in the present study to determine the similarities and differences between them (Table 4 ). For the full model reconstructions before CSMs reconstructions, 778 reactions within the cell were shared.…”

“…For the full model reconstructions before CSMs reconstructions, 778 reactions within the cell were shared. Likewise, 794 unique reactions were identified for the model used in this study, and 708 for the model constructed by Rodenburg et al ( 2017 ). Also, the pathways, in which the reactions shared between the two reconstructions are involved, were identified (Figure S3 ).…”

“…In 2013, Seidl et al ( 2013 ) constructed a gene network of P. infestans and determined functional models related to its life stages using predictions of protein-protein interactions. Rodenburg et al ( 2017 ) then reconstructed the first genome-scale metabolic model for P. infestans , based on reactions found in the Kyoto Encyclopedia of Genes and Genomes (KEGG) (Rodenburg et al, 2017 ). They also used RNA sequencing data to quantify gene expression in four in vitro life stages of P. infestans , i.e., mycelium, sporangia, zoospores, and germinating cysts (Rodenburg et al, 2017 ).…”

“…The transcriptomic data of the strain 1,306 were selected for the present study because it is the most comprehensive study of the metabolic changes of the pathogen during its development (Ah-Fong et al, 2017 ). For the initial genome-scale metabolic network, we used our own reconstruction, different from the one proposed by Rodenburg et al ( 2017 ) because when they published their reconstruction, ours was in an advanced stage and we decided to continue using it. A thorough comparison of both reconstructions is made available in this study to the scientific community.…”