Gains of Bacterial Flagellar Motility in a Fungal World

Abstract

The maintenance of energetically costly flagella by bacteria in non-water-saturated media, such as soil, still presents an evolutionary conundrum. Potential explanations have focused on rare flooding events allowing dispersal. Such scenarios, however, overlook bacterial dispersal along mycelia as a possible transport mechanism in soils. The hypothesis tested in this study is that dispersal along fungal hyphae may lead to an increase in the fitness of flagellated bacteria and thus offer an alternative explanation for the maintenance of flagella even in unsaturated soils. Dispersal along fungal hyphae was shown for a diverse array of motile bacteria. To measure the fitness effect of dispersal, additional experiments were conducted in a model system mimicking limited dispersal, using Pseudomonas putida KT2440 and its nonflagellated (⌬fliM) isogenic mutant in the absence or presence of Morchella crassipes mycelia. In the absence of the fungus, flagellar motility was beneficial solely under conditions of water saturation allowing dispersal, while under conditions limiting dispersal, the nonflagellated mutant exhibited a higher level of fitness than the wild-type strain. In contrast, in the presence of a mycelial network under conditions limiting dispersal, the flagellated strain was able to disperse using the mycelial network and had a higher level of fitness than the mutant. On the basis of these results, we propose that the benefit of mycelium-associated dispersal helps explain the persistence of flagellar motility in non-water-saturated environments.

Molecular mechanisms underlying the close association between soil Burkholderia and fungi

“…Karsten. Under the conditions used, the mycelium of Lyophyllum showed hydrophobicity, thus inhibiting the formation of a water film around the hyphae, which might be necessary for bacterial attachment and dispersal (Pion et al, 2013). However, Warmink et al (2011) showed that B. terrae BS001 could migrate together with Lyophyllum sp.…”

Mechanisms of Bacterial (Serratia marcescens) Attachment to, Migration along, and Killing of Fungal Hyphae

“…The sliding hypothesis can be tested with mutant strains defective in surfactant production (21). Interestingly, Pseudomonas putida bacteria lacking flagella lose their ability to migrate along hyphae, suggesting that unlike S. marcescens, they rely entirely on flagella to move along the fungal mycelium (22).…”

Mycelium-Like Networks Increase Bacterial Dispersal, Growth, and Biodegradation in a Model Ecosystem at Various Water Potentials

“…The dispersal of microorganisms is recognized as a key factor for soil ecological functions (1,(46)(47)(48), such as the promotion of microbial diversity or the turnover of chemicals. Bacterial dispersal along fungal mycelia has been shown for numerous bacterial species and fungi (18,49,50) and hence may be of special relevance in unsaturated soil systems. Fungi constitute up to 75% of the soil microbial biomass, with a length of 10 2 to 10 4 m hyphae per g of soil (12,51).…”

“…Glass fibers were used to simulate hyphae surrounded by liquid films (16,18) and to exclude effects of hyphal activities on bacterial growth and nutrition (38)(39)(40)(41) to avoid additional complexity that might mask effects attributable to the promotion of bacterial dispersal at a lowered ⌿ m .…”

“…Different studies using soil column experiments and simulation modeling showed that this phenomenon can enhance biodegradation of phenanthrene and glucose, respectively (15)(16)(17). However, studies to assess the benefits of dispersal networks were carried out with culture plates with different agar concentrations routinely used in standard bacterial motility assays (18)(19)(20). Indeed, these concentrations represent only a narrow range of ⌿ m values, which is insufficient for studying relevant environmental conditions, in particular in soils, where ⌿ m often falls to Ϫ1.5 MPa (21).…”