Transcriptional Responses of the Bacterium Burkholderia terrae BS001 to the Fungal Host Lyophyllum sp. Strain Karsten under Soil-Mimicking Conditions

Abstract

In this study, the mycosphere isolate Burkholderia terrae BS001 was confronted with the soil fungus Lyophyllum sp. strain Karsten on soil extract agar plates in order to examine its transcriptional responses over time. At the initial stages of the experiment (T1—day 3; T2—day 5), contact between both partner organisms was absent, whereas in the final stage (T3—day 8), the two populations made intimate physical contact. Overall, a strong modulation of the strain BS001 gene expression patterns was found. First, the stationary-phase sigma factor RpoS, and numerous genes under its control, were strongly expressed as a response to the soil extract agar, and this extended over the whole temporal regime. In the system, B. terrae BS001 apparently perceived the presence of the fungal hyphae already at the early experimental stages (T1, T2), by strongly upregulating a suite of chemotaxis and flagellar motility genes. With respect to specific metabolism and energy generation, a picture of differential involvement in different metabolic routes was obtained. Initial (T1, T2) up- or downregulation of ethanolamine and mandelate uptake and utilization pathways was substituted by a strong investment, in the presence of the fungus, in the expression of putative metabolic gene clusters (T3). Specifically at T3, five clustered genes that are potentially involved in energy generation coupled to an oxidative stress response, and two genes encoding short-chain dehydrogenases/oxidoreductases (SDR), were highly upregulated. In contrast, the dnaE2 gene (related to general stress response; encoding error-prone DNA polymerase) was transcriptionally downregulated at this stage. This study revealed that B. terrae BS001, from a stress-induced state, resulting from the soil extract agar milieu, responds positively to fungal hyphae that encroach upon it, in a temporally dynamic manner. The response is characterized by phases in which the modulation of (1) chemotaxis, (2) metabolic activity, and (3) oxidative stress responses are key mechanisms.Electronic supplementary materialThe online version of this article (doi:10.1007/s00248-016-0885-7) contains supplementary material, which is available to authorized users.

Migration of Paraburkholderia terrae BS001 Along Old Fungal Hyphae in Soil at Various pH Levels

“…The protective effect was akin to that previously found for the G soil. Although we lack evidence for this, it is possible that the fungus—by providing nutrients such as glycerol and oxalate [12, 27]—furnished energy and carbon sources to the inoculant cells which subsequently were able to better establish and survive in the system. The effect regarding the pH raises is discussed below.…”

“…As flagellar motility has been reported to be driven by either the proton-motive or the sodium-motive force [8, 9], bacterial translocation may be spurred (on semi-solid agar) by pH decreases, as shown in recent reports [4, 10]. On another notice, factors that drive chemotaxis (e.g., particular fungal exudates) have also been found to modulate bacterial motility [11, 12], with an abundant local nutrient supply suppressing such movement [13]. …”

Microbial indicators for soil quality

“…Its huge genome was found to be highly adaptable due to a very high number of genomic islands interspersed in a genomic backbone (Haq et al 2014). Several of the genetic systems of this organism were found to have key roles in the interaction with soil fungi, an example of this being a five-gene cluster -predicted to encode a response to fungal-released carbon compounds next to a toxic oxygen radical dissipation mechanism -with raised ad-fungus activity (Haq et al 2017). This latter gene cluster may constitute an excellent candidate that reports on bacteria interacting with fungi in the soil, a key facet of microbiome connectedness.…”

Mechanism of interaction of an endofungal bacterium Serratia marcescens D1 with its host and non-host fungi

“…Burkholderia terrae shows chemotaxis, metabolic activity and oxidative stress responses during its interaction with the host fungus Lyophyllum sp. [19]. In a recent study on Burkholderia rhizoxinica, involvement of novel pyrrole-substituted depsipeptides (endopyrroles) have been discovered [20].…”