The Role of Hydrophobicity and Surface Receptors at Hyphae of Lyophyllum sp. Strain Karsten in the Interaction with Burkholderia terrae BS001 – Implications for Interactions in Soil

Abstract

The soil bacterium Burkholderia terrae strain BS001 can interact with varying soil fungi, using mechanisms that range from the utilization of carbon/energy sources such as glycerol to the ability to reach novel territories in soil via co-migration with growing fungal mycelia. Here, we investigate the intrinsic properties of the B. terrae BS001 interaction with the basidiomycetous soil fungus Lyophyllum sp. strain Karsten. In some experiments, the ascomycetous Trichoderma asperellum 302 was also used. The hyphae of Lyophyllum sp. strain Karsten were largely hydrophilic on water-containing media versus hydrophobic when aerial, as evidenced by contact angle analyses (CA). Co-migration of B. terrae strain BS001 cells with the hyphae of the two fungi occurred preferentially along the - presumably hydrophilic - soil-dwelling hyphae, whereas aerial hyphae did not allow efficient migration, due to reduced thickness of their surrounding mucous films. Moreover, the cell numbers over the length of the hyphae in soil showed an uneven distribution, i.e., the CFU numbers increased from minima at the inoculation point to maximal numbers in the middle of the extended hyphae, then decreasing toward the terminal side. Microscopic analyses of the strain BS001 associations with the Lyophyllum sp. strain Karsten hyphae in the microcosms confirmed the presence of B. terrae BS001 cells on the mucous matter that was present at the hyphal surfaces of the fungi used. Cell agglomerates were found to accumulate at defined sites on the hyphal surfaces, which were coined ‘fungal-interactive’ hot spots. Evidence was further obtained for the contention that receptors for a physical bacterium-fungus interaction occur at the Lyophyllum sp. strain Karsten hyphal surface, in which the specific glycosphingolipid ceramide monohexoside (CMH) plays an important role. Thus, bacterial adherence may be mediated by heterogeneously distributed fungal-specific receptors, implying the CMH moieties. This study sheds light on the physical aspects of the B. terrae BS001 – Lyophyllum sp. strain Karsten interaction, highlighting heterogeneity along the hyphae with respect to hydrophobicity and the presence of potential anchoring sites.

Mechanisms and ecological implications of the movement of bacteria in soil

“…We further found that only soil-dwelling hyphae, which were hydrophilic, can support bacterial migration. In contrast, aerial hyphae, which are more hydrophobic, did not allow efficient migration (Vila et al, 2016). Overall, on the basis of our findings, and in line with findings by Furuno et al (2010), we posit that a water film formed around the soil-borne fungal hyphae is critical for the occurrence of bacterial swimming motility driven co-migration along the fungal highway.…”

“…3 Low soil pH strongly restricts bacterial survival and dispersal in mycosphere (Yang et al, 2018). 4 Bacterial cells disperse along with hydrophilic fungal hyphae, not with hydrophobic hyphae (Vila et al, 2016). 5 Bacterial growth/death is associated with water availability (water activity).…”

The pleiotropic functions of intracellular hydrophobins in aerial hyphae and fungal spores

“…These layers significantly decrease the interfacial tension, thus allowing the hyphae to breach the liquid surface and grow into the air by forming buoyant colonies. Fruiting bodies, aerial hyphae and spores are also largely coated by HFBs to reduce wetting, provide resilience to environmental stresses [1,11], promote the adhesion of spores and hyphae to hydrophobic surfaces or interactions with symbiotic partners [4], and influence growth and development [12][13][14].…”

Intracellular accumulation and secretion of hydrophobin-enriched vesicles aid the rapid sporulation of molds

“…Therefore, for reproduction and dispersal, fungi need to rapidly grow out of the substrate and form aerial and hydrophobic sporogenic structures (e.g., fruiting bodies, sporangia, and conidiophores) and spores 1,2 catching suitable dispersal conditions. The hydrophobicity of the spore or hyphal cell wall also influences their adhesion to the substrate and their interactions with symbiotic partners 3,4 . Thus, the ability to modulate the hydrophobicity of the body surface and cross the hydrophilic/hydrophobic (i.e., water/air) interface is crucial for fungal lifestyle 5 .…”

“…These layers significantly decrease the interfacial tension, thus allowing the hyphae to breach the liquid surface and grow into the air. Fruiting bodies, aerial hyphae or spores are also largely coated by HFBs to reduce wetting, provide resilience to environmental stresses 2,12 , promote the adhesion of spores and hyphae to hydrophobic surfaces or interactions with symbiotic partners 4 , and influence growth and development 13,14,15 .…”