Abstract
BackgroundDickeya dadantii and Pectobacterium atrosepticum are phytopathogenic enterobacteria capable of facultative anaerobic growth in a wide range of O2 concentrations found in plant and natural environments. The transcriptional response to O2 remains under-explored for these and other phytopathogenic enterobacteria although it has been well characterized for animal-associated genera including Escherichia coli and Salmonella enterica. Knowledge of the extent of conservation of the transcriptional response across orthologous genes in more distantly related species is useful to identify rates and patterns of regulon evolution. Evolutionary events such as loss and acquisition of genes by lateral transfer events along each evolutionary branch results in lineage-specific genes, some of which may have been subsequently incorporated into the O2-responsive stimulon. Here we present a comparison of transcriptional profiles measured using densely tiled oligonucleotide arrays for two phytopathogens, Dickeya dadantii 3937 and Pectobacterium atrosepticum SCRI1043, grown to mid-log phase in MOPS minimal medium (0.1% glucose) with and without O2.ResultsMore than 7% of the genes of each phytopathogen are differentially expressed with greater than 3-fold changes under anaerobic conditions. In addition to anaerobic metabolism genes, the O2 responsive stimulon includes a variety of virulence and pathogenicity-genes. Few of these genes overlap with orthologous genes in the anaerobic stimulon of E. coli. We define these as the conserved core, in which the transcriptional pattern as well as genetic architecture are well preserved. This conserved core includes previously described anaerobic metabolic pathways such as fermentation. Other components of the anaerobic stimulon show variation in genetic content, genome architecture and regulation. Notably formate metabolism, nitrate/nitrite metabolism, and fermentative butanediol production, differ between E. coli and the phytopathogens. Surprisingly, the overlap of the anaerobic stimulon between the phytopathogens is also relatively small considering that they are closely related, occupy similar niches and employ similar strategies to cause disease. There are cases of interesting divergences in the pattern of transcription of genes between Dickeya and Pectobacterium for virulence-associated subsystems including the type VI secretion system (T6SS), suggesting that fine-tuning of the stimulon impacts interaction with plants or competing microbes.ConclusionsThe small number of genes (an even smaller number if we consider operons) comprising the conserved core transcriptional response to O2 limitation demonstrates the extent of regulatory divergence prevalent in the Enterobacteriaceae. Our orthology-driven comparative transcriptomics approach indicates that the adaptive response in the eneterobacteria is a result of interaction of core (regulators) and lineage-specific (structural and regulatory) genes. Our subsystems based approach reveals that similar phenotypic outcomes are sometimes achieved by each organism using different genes and regulatory strategies.
Highlights
Dickeya dadantii and Pectobacterium atrosepticum are phytopathogenic enterobacteria capable of facultative anaerobic growth in a wide range of O2 concentrations found in plant and natural environments
A large number of genes are in the O2-response stimulon Using a conditional false-discovery rate of 0.01, EBarrays [18] detects over 2204 differentially expressed genes in D. dadantii (48.5%), and 599 in P. atrosepticum (13.4%)
A substantial fraction of each genome is involved in the anaerobic stimulon even using our stringent criteria, consistent with published reports for E. coli K-12 [12] despite differences in array platforms and analysis methods
Summary
Dickeya dadantii and Pectobacterium atrosepticum are phytopathogenic enterobacteria capable of facultative anaerobic growth in a wide range of O2 concentrations found in plant and natural environments. D. dadantii strain 3937 (D. dadantii) was originally isolated from African violet and is better known by its former name Erwinia chrysanthemi 3937, and P. atrosepticum strain SCRI1043 was isolated from potato [2,3], but individual strains and these genera as a whole have broad host range, affecting over 50% of angiosperm plant orders [4] They are a world-wide problem for economically important crops and ornamental plants [5]. Dickeya and Pectobacterium are facultative anaerobes that are able to grow with or without O2 by shifting metabolic strategies from aerobic respiration to anaerobic respiration or fermentation [8] They experience a wide range of O2 concentrations in different plant tissues and natural reservoirs like soil and water [9]. Lack of O2 is thought to be one of the factors that can trigger rapid expansion of latent infections leading to devastating post-harvest destruction of entire crops in storage [5]
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