The Response of Paraburkholderia terrae Strains to Two Soil Fungi and the Potential Role of Oxalate

Abstract

Fungal-associated Paraburkholderia terrae strains in soil have been extensively studied, but their sensing strategies to locate fungi in soil have remained largely elusive. In this study, we investigated the behavior of five mycosphere-isolated P. terrae strains [including the type-3 secretion system negative mutant BS001-ΔsctD and the type strain DSM 17804T] with respect to their fungal-sensing strategies. The putative role of oxalic acid as a signaling molecule in the chemotaxis toward soil fungi, as well as a potential carbon source, was assessed. First, all P. terrae strains, including the type strain, were found to sense, and show a chemotactic response toward, the different levels of oxalic acid (0.1, 0.5, and 0.8%) applied at a distance. The chemotactic responses were faster and stronger at lower concentrations (0.1%) than at higher ones. We then tested the chemotactic responses of all strains toward exudates of the soil fungi Lyophyllum sp. strain Karsten and Trichoderma asperellum 302 used in different dilutions (undiluted, 1:10, 1:100 diluted) versus the control. All P. terrae strains showed significant directed chemotactic behavior toward the exudate source, with full-strength exudates inciting the strongest responses. In a separate experiment, strain BS001 was shown to be able to grow on oxalate-amended (0.1 and 0.5%) mineral medium M9. Chemical analyses of the fungal secretomes using proton nuclear magnetic resonance (1H NMR), next to high-performance liquid chromatography (HPLC), indeed revealed the presence of oxalic acid (next to glycerol, acetic acid, formic acid, and fumaric acid) in the supernatants of both fungi. In addition, citric acid was found in the Lyophyllum sp. strain Karsten exudates. Given the fact that, next to oxalic acid, the other compounds can also serve as C and energy sources for P. terrae, the two fungi clearly offer ecological benefits to this bacterium. The oxalic acid released by the two fungi may have primarily acted as a signaling molecule, and, as a “second option,” a carbon source for P. terrae strains like BS001.

A Taxon-Wise Insight Into Rock Weathering and Nitrogen Fixation Functional Profiles of Proglacial Systems

“…Mesorhizobium and Paraburkholderia are also common diazotrophic components of the rhizosphere but have been detected as free-living organisms ( Ahmad et al, 2008 ), and they showed high presence of both these genes. Paraburkholderia was found to have chemotactic sensitivity for oxalate even if it was not directly shown that it can produce it ( Haq et al, 2018 ). Micromonospora also had high oxalate-related gene abundance especially in the first stages of the SW dataset.…”

It Takes Two to Tango: A Bacterial Biofilm Provides Protection against a Fungus-Feeding Bacterial Predator

“…led to a significant increase in the population of indigenous collimonads, however no reduction in the fungal biomass was reported. In addition to this, in the same experiment, no increase in the population of common fungal hyphae-associated bacteria such as Pseudomonas and Burkholderia, which are known to feed on fungal metabolites, was detected [ 38 , 53 , 99 , 100 ]. This observation further supports the “hyphal feeding” strategy of collimonads.…”

Gene mobility in microbiomes of the mycosphere and mycorrhizosphere –role of plasmids and bacteriophages

“…First, the active hyphae of fungi in soil often supply (release) small carbonaceous compounds that support the growth of associated bacteria. Thus, compounds such as: maltose, trehalose, L-rhamnose, D-sorbitol, D-glucuronic acid, p-hydroxy-phenylacetic acid, succinamic acid, glucuronamide, L-alanin amine, L-ornithine, glycerol, mannitol, oxalic acid, acetic acid, formic acid, citric acid, fumaric acid and CO 2 have all been shown to be released at fungal surfaces (Frey-Klett et al 2011;Churchland and Grayston 2014;Haq et al 2018). Moreover, hyphae of particular fungi are known to produce inhibitory (i.e.…”

“…Their network structures enable them to move around substances (e.g. bound carbon) and so carbon sources that are required for growth can be furnished to local bacteria (Haq et al 2018). Moreover, the hyphal networks can also translocate bacterial cells through soil Berthold et al 2016).…”