Abstract
Tagatose is a rare sugar with no negative impacts on human health and selective inhibitory effects on plant-associated microorganisms. Tagatose inhibited mycelial growth and negatively affected mitochondrial processes in Phytophthora infestans, but not in Phytophthora cinnamomi. The aim of this study was to elucidate metabolic changes and transcriptional reprogramming activated by P. infestans and P. cinnamomi in response to tagatose, in order to clarify the differential inhibitory mechanisms of tagatose and the species-specific reactions to this rare sugar. Phytophthora infestans and P. cinnamomi activated distinct metabolic and transcriptional changes in response to the rare sugar. Tagatose negatively affected mycelial growth, sugar content and amino acid content in P. infestans with a severe transcriptional reprogramming that included the downregulation of genes involved in transport, sugar metabolism, signal transduction, and growth-related process. Conversely, tagatose incubation upregulated genes related to transport, energy metabolism, sugar metabolism and oxidative stress in P. cinnamomi with no negative effects on mycelial growth, sugar content and amino acid content. Differential inhibitory effects of tagatose on Phytophthora spp. were associated with an attempted reaction of P. infestans, which was not sufficient to attenuate the negative impacts of the rare sugar and with an efficient response of P. cinnamomi with the reprogramming of multiple metabolic processes, such as genes related to glucose transport, pentose metabolism, tricarboxylic acid cycle, reactive oxygen species detoxification, mitochondrial and alternative respiration processes. Knowledge on the differential response of Phytophthora spp. to tagatose represent a step forward in the understanding functional roles of rare sugars.
Highlights
Rare sugars have been defined as monosaccharides and their derivatives that rarely exist in nature, such as tagatose, allose, sorbose, xylulose, and xylitol (Granström et al, 2004)
The differential inhibitory effect of tagatose on P. infestans and P. cinnamomi was associated with species-specific metabolic and transcriptional changes
An attempted response was upregulated by P. infestans, but it was not sufficient to contrast the negative effects of tagatose incubation on mycelial growth, sugar content and amino acid content
Summary
Rare sugars have been defined as monosaccharides and their derivatives that rarely exist in nature, such as tagatose, allose, sorbose, xylulose, and xylitol (Granström et al, 2004). Since tagatose does not have negative impacts on human health, it was ‘generally recognized as safe’ by the Food and Drug Administration and it is used as low-calorie sweetener in several countries (Levin, 2002; Vastenavond et al, 2011). Tagatose is not catabolised by some human-associated microorganisms, such as Bacillus cereus, Escherichia coli, Listeria monocytogenes, Staphylococcus aureus, and Yersinia enterocolitica (Bautista et al, 2000), indicating selective nutritional or anti-nutritional properties for specific microbial taxa. Tagatose enhanced the growth of Lactobacillus rhamnosus and upregulated genes associated with sugar metabolism (e.g., phosphotransferase encoding genes, phosphofructokinase and tagatose-6-phosphate kinase) (Koh et al, 2013), suggesting specific impacts of rare sugars on the microbial metabolism
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