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

Abstract

e Fungal mycelia serve as effective dispersal networks for bacteria in water-unsaturated environments, thereby allowing bacteria to maintain important functions, such as biodegradation. However, poor knowledge exists on the effects of dispersal networks at various osmotic (⌿ o ) and matric (⌿ m ) potentials, which contribute to the water potential mainly in terrestrial soil environments. Here we studied the effects of artificial mycelium-like dispersal networks on bacterial dispersal dynamics and subsequent effects on growth and benzoate biodegradation at ⌬⌿ o and ⌬⌿ m values between 0 and ؊1.5 MPa. In a multiple-microcosm approach, we used a green fluorescent protein (GFP)-tagged derivative of the soil bacterium Pseudomonas putida KT2440 as a model organism and sodium benzoate as a representative of polar aromatic contaminants. We found that decreasing ⌬⌿ o and ⌬⌿ m values slowed bacterial dispersal in the system, leading to decelerated growth and benzoate degradation. In contrast, dispersal networks facilitated bacterial movement at ⌬⌿ o and ⌬⌿ m values between 0 and ؊0.5 MPa and thus improved the absolute biodegradation performance by up to 52 and 119% for ⌬⌿ o and ⌬⌿ m , respectively. This strong functional interrelationship was further emphasized by a high positive correlation between population dispersal, population growth, and degradation. We propose that dispersal networks may sustain the functionality of microbial ecosystems at low osmotic and matric potentials.

Catch me if you can: dispersal and foraging ofBdellovibrio bacteriovorus109J along mycelia

“…Our findings and their dimension, however, suggest that mycelial networks in natural habitats are locations of similar interactions. This is corroborated by the fact that dispersal networks in soil and other habitats influence multifarious functions relying on bacterial mobility such as biodegradation (Wick et al, 2007a;Otto et al, 2016;Worrich et al, 2016), oxalate turnover (Martin et al, 2012) or food spoilage (Lee et al, 2014). Hence, it is most likely that BALOs would use available mycelia for their dispersal also in natural settings.…”

Bacterial Dispersal Promotes Biodegradation in Heterogeneous Systems Exposed to Osmotic Stress

“…In the present study, bacterial movement through the agar matrix and along the dispersal networks was found to counteract the disadvantage due to spatial degrader heterogeneity at different osmotic potentials. The counteraction ability was higher in case of glass fiber networks, which had been shown to accelerate bacterial dispersal processes earlier (Banitz et al, 2011a ; Worrich et al, 2016 ). Glass fibers were used to simulate hyphae surrounded by liquid films (Banitz et al, 2011b ; Pion et al, 2013a ) and to exclude effects of hyphal activities on bacterial growth and nutrition (Furuno et al, 2012 ; Banitz et al, 2013 ; Pion et al, 2013b ; Schamfuß et al, 2013 ).…”

“…Salinity is known to affect bacterial dispersal and thus we analyzed how the counteracting effects change with decreasing osmotic potentials and if there is some kind of threshold at which not the spatial processes but rather the physiological limitations control biodegradation efficiency. The soil bacterium P. putida KT2440 was chosen because of its well-characterized motility behavior (Dechesne et al, 2010b ), which recently was investigated also under osmotic stress conditions (Worrich et al, 2016 ). In our study, sodium benzoate served as a representative of polar, aromatic contaminants (e.g., pesticides) as its physicochemical properties are similar to those of 2,4-D, dicamba or fluroxypyr (Dechesne et al, 2010a ).…”

“…Globally, more than 831 million hectares of land are affected by salt at levels causing osmotic stress in bacteria (Martinez-Beltran and Manzur, 2005 ). Recently, it was shown that the presence of mycelium-like networks improved dispersal, growth, and biodegradation under environmental stress conditions induced by lowered water potentials (Worrich et al, 2016 ). However, to what extent spatial processes like bacterial dispersal, network-mediated bacterial dispersal, or substrate diffusion may counteract the disadvantage due to a heterogeneous degrader distribution at different osmotic potentials remains unclear.…”

Mycelia as a focal point for horizontal gene transfer among soil bacteria

“…By connecting air-filled space between water-filled pores36, fungi also provide efficient dispersal networks (‘fungal highways’19) for random or directed extra-hyphal movement of otherwise immobilised bacteria37. Mycelia thereby facilitate the access of bacteria to suitable microhabitats for growth20, enable efficient contaminant biodegradation38 or increase the functional stability in systems exposed to osmotic stress39.…”