Siderophore-Mediated Iron Acquisition Influences Motility and Is Required for Full Virulence of the Xylem-Dwelling Bacterial Phytopathogen Pantoea stewartii subsp. stewartii

Abstract

Iron is a key micronutrient for microbial growth but is often present in low concentrations or in biologically unavailable forms. Many microorganisms overcome this challenge by producing siderophores, which are ferric-iron chelating compounds that enable the solubilization and acquisition of iron in a bioactive form. Pantoea stewartii subsp. stewartii, the causal agent of Stewart's wilt of sweet corn, produces a siderophore under iron-limiting conditions. The proteins involved in the biosynthesis and export of this siderophore are encoded by the iucABCD-iutA operon, which is homologous to the aerobactin biosynthetic gene cluster found in a number of enteric pathogens. Mutations in iucA and iutA resulted in a decrease in surfacebased motility that P. stewartii utilizes during the early stages of biofilm formation, indicating that active iron acquisition impacts surface motility for P. stewartii. Furthermore, bacterial movement in planta is also dependent on a functional siderophore biosynthesis and uptake pathway. Most notably, siderophore-mediated iron acquisition is required for full virulence in the sweet corn host, indicating that active iron acquisition is essential for pathogenic fitness for this important xylem-dwelling bacterial pathogen. P antoea stewartii subsp. stewartii, a Gram-negative bacterial phytopathogen, is the causal agent of a severe seedling wilt in susceptible corn cultivars called Stewart's wilt (1-3). The bacterium is transmitted by an insect vector, the corn flea beetle (Chaetocnema pulicaria), that introduces the pathogen into the plant tissue when it creates scratching wounds on the leaf surface during feeding. There are two phases of Stewart's wilt, a leaf blight and a wilting phase. During the initial infection phase, leaf blight occurs when the bacteria colonize the apoplastic space and cause characteristic water-soaked lesions. As infection progresses, the bacteria preferentially colonize the xylem, where they move systemically through the plant and block water flow, thereby causing the wilting observed in susceptible young seedlings. P. stewartii forms biofilms in the xylem, a process which is regulated in a cell density-dependent manner and requires flagellar-based surface motility and production of an exopolysaccharide (EPS) matrix (4-6). It is these biofilms and the associated EPS that presumably lead to xylem vessel blockage (5, 7). P. stewartii is able to reach very high cell densities and spread quickly within the xylem, in part due to flagellar motility and secretion of a plant cell wall-degrading enzyme (4, 8). However, it is not fully known how the bacterium obtains the suite of required nutrients for rapid growth within the plant or what environmental factors influence the transition from the planktonic to the biofilm state, which is necessary for systemic colonization of the xylem. Iron is commonly a limiting nutrient for microbial growth because it is often insoluble at biological pH within tissues and thus unavailable for utilization. Specifically, in plant tissues th...

Streptomycesvolatile compounds influence exploration and microbial community dynamics by altering iron availability

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Promising bacterial genera for agricultural practices: An insight on plant growth-promoting properties and microbial safety aspects

“…Usually, hydroxamates are more commonly found in neutral to acid environments while catecholates are more commonly found in neutral to alkaline environments (Saha et al, 2013). Several bacterial genera were described to produce siderophores, such as Azotobacter (Baars et al, 2016;McRose et al, 2017;Romero-Perdomo et al, 2017), Azospirillum (Banik et al, 2016), Bacillus (Kesaulya et al, 2018;Pourbabaee et al, 2018), Dickeya (Sandy and Butler, 2011), Klebsiella (Bailey et al, 2018;Zhang et al, 2017), Nocardia (Hoshino et al, 2011), Pantoea (Burbank et al, 2015;Soutar and Stavrinides, 2018), Paenibacillus (Liu et al, 2017), Pseudomonas (Baune et al, 2017;Deori et al, 2018;Pourbabaee et al, 2018), Serratia (Coulthurst, 2014) and Streptomyces (Gáll et al, 2016;Goudjal et al, 2016;Schütze et al, 2014).…”

“…Pantoea stewartii subsp. stewartii produces a siderophore under iron-limiting conditions, which biosynthesis and export of proteins are encoded by the iucABCD-iutA operon; this operon is homologous to the aerobactin biosynthetic gene cluster found in a number of enteric pathogens (Burbank et al, 2015). It was also described that the strain Pantoea eucalypti M91 is capable of producing pyoverdine-like and pyochelin-like siderophores under alkaline growth conditions (Campestre et al, 2016).…”

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