Abstract
Arabinose is a major plant aldopentose in the form of arabinans complexed in cell wall polysaccharides or glycoproteins (AGP), but comparatively rare as a monosaccharide. l-arabinose is an important bacterial metabolite, accessed by pectolytic micro-organisms such as Pectobacterium atrosepticum via pectin and hemicellulose degrading enzymes. However, not all plant-associated microbes encode cell-wall-degrading enzymes, yet can metabolize l-arabinose, raising questions about their use of and access to the glycan in plants. Therefore, we examined l-arabinose metabolism in the food-borne pathogen Escherichia coli O157:H7 (isolate Sakai) during its colonization of plants. l-arabinose metabolism (araBA) and transport (araF) genes were activated at 18 °C in vitro by l-arabinose and expressed over prolonged periods in planta. Although deletion of araBAD did not impact the colonization ability of E. coli O157:H7 (Sakai) on spinach and lettuce plants (both associated with STEC outbreaks), araA was induced on exposure to spinach cell-wall polysaccharides. Furthermore, debranched and arabinan oligosaccharides induced ara metabolism gene expression in vitro, and stimulated modest proliferation, while immobilized pectin did not. Thus, E. coli O157:H7 (Sakai) can utilize pectin/AGP-derived l-arabinose as a metabolite. Furthermore, it differs fundamentally in ara gene organization, transport and regulation from the related pectinolytic species P. atrosepticum, reflective of distinct plant-associated lifestyles.
Highlights
Arabinose is an abundant aldopentose in plant material that is not found in animals
To determine any essentiality of arabinose metabolism in planta, a knock-o ut mutant of the araBAD operon was made in STEC (Sakai) and tested in plant colonization ability primarily on spinach leaves and confirmed on the original plant models, spinach roots, lettuce roots and leaves
In STEC (Sakai), l-arabinose metabolism is active in plants but non-essential for its colonization: ara genes were responsive in vitro to leaf extracts and in planta during colonization for a range of plant models, but the gene cluster knock-o ut was not affected in spinach or lettuce colonization over a 10 day period
Summary
Arabinose is an abundant aldopentose in plant material that is not found in animals. It is present almost entirely as polysaccharides (arabinans) and glycoproteins, as l-arabinofuranose (l-Araf) complexed in the RG1 and RG2 pectin components of plant cell walls [1], as side chains in hemicellulose [2] or in arabinogalactan-proteins, AGP [3]. Free monomeric l-arabinopyranose (l-Arap) is present in intracellular and apoplastic compartments but is rare in comparison to fructose and sucrose [4]. L-arabinose metabolism is widespread in microbes, reflective of a beneficial function for accessing the carbohydrate directly from plants or as a dietary fibre in animal guts. L-arabinose metabolic systems comprise transport and metabolism genes and a master regulator. Intracellular l-arabinose enters the pentose phosphate pathway in a three-step degradation pathway via AraA, an isomerase that converts it to l-ribulose; AraB, a ribulokinase that catalyses l-ribulose phosphorylation to l-ribulose-5-phosphate; and AraD, an epimerase that
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