Ketoglutarate Transport Protein KgtP Is Secreted through the Type III Secretion System and Contributes to Virulence in Xanthomonas oryzae pv. oryzae

Abstract

bThe phytopathogenic prokaryote Xanthomonas oryzae pv. oryzae is the causal agent of bacterial leaf blight (BB) of rice and utilizes a type III secretion system (T3SS) to deliver T3SS effectors into rice cells. In this report, we show that the ketoglutarate transport protein (KgtP) is secreted in an HpaB-independent manner through the T3SS of X. oryzae pv. oryzae PXO99A and localizes to the host cell membrane for ␣-ketoglutaric acid export. kgtP contained an imperfect PIP box (plant-inducible promoter) in the promoter region and was positively regulated by HrpX and HrpG. A kgtP deletion mutant was impaired in bacterial virulence and growth in planta; furthermore, the mutant showed reduced growth in minimal media containing ␣-ketoglutaric acid or sodium succinate as the sole carbon source. The reduced virulence and the deficiency in ␣-ketoglutaric acid utilization by the kgtP mutant were restored to wild-type levels by the presence of kgtP in trans. The expression of OsIDH, which is responsible for the synthesis of ␣-ketoglutaric acid in rice, was enhanced when KgtP was present in the pathogen. To our knowledge, this is the first report demonstrating that KgtP, which is regulated by HrpG and HrpX and secreted by the T3SS in Xanthomonas oryzae pv. oryzae, transports ␣-ketoglutaric acid when the pathogen infects rice.

The Emergence of 2-Oxoglutarate as a Master Regulator Metabolite

“…However, 2-OG seems to leak from E. coli cells under certain culture conditions (13). Interestingly, in Xanthomonas oryzae, the kgtP-encoded transporter plays an important role as a plant virulence effector, since it is secreted by the type III secretion system to the plant cell membrane, where it may be involved in 2-OG acquisition from host rice cells (32).…”

Glucose-6-phosphate dehydrogenase is required for extracellular polysaccharide production, cell motility and the full virulence of Xanthomonas oryzae pv. oryzicola

“…In the past, substantial progress has been made to elucidate molecular mechanisms of the Xoc-rice pathosystem [1e7]. One important aspect of the Xoc-rice pathosystem is the ability of bacterium to obtain nutrients from host rice to establish successful infection [6,7]. However, little is known about the links between bacterial nutrients acquisition and pathogenesis in this field.…”

“…[14,18]. Currently, several genes, like ppsA [20], aceA [20], mls [20], glk [16], gapA [14], kgtP [7], and fbaB [6], which involved in carbohydrate metabolism of Xanthomonas spp. have been investigated in some details.…”

Genetic Analysis of the Assimilation of C 5 -Dicarboxylic Acids in Pseudomonas aeruginosa PAO1

“…␣-KG-dependent hydroxylases are ubiquitous among bacteria and participate in various cellular functions (7), including the assimilation of key nutrients, e.g., sulfur and phosphate, and the biosynthesis of complex molecules such as antibiotics and lipid A. Interestingly, there have been a few recently published papers reporting that ␣-KG might be a preferred nutrient for some bacteria during the course of an infectious state (8)(9)(10). ␣-KG is a suitable growth substrate for most bacteria, but the genes involved in the transport and assimilation of ␣-KG have been investigated for only a small number of bacterial species, including Escherichia coli (10)(11)(12), Staphylococcus aureus (13), Bacillus licheniformis (14), Lactococcus lactis (15), Xanthomonas oryzae (9), and Rhizobium tropici (8). Missing from the literature are studies describing the genetic regulation of ␣-KG assimilation in Pseudomonas, which is surprising, because these bacteria are well known for their versatile metabolism, enabling them to consume a wide range of substrates.…”