title: Bacterial Dispersal Promotes Biodegradation in Heterogeneous Systems Exposed to Osmotic Stress.
abstract: Contaminant biodegradation in soils is hampered by the heterogeneous distribution of degrading communities colonizing isolated microenvironments as a result of the soil architecture. Over the last years, soil salinization was recognized as an additional problem especially in arid and semiarid ecosystems as it drastically reduces the activity and motility of bacteria. Here, we studied the importance of different spatial processes for benzoate biodegradation at an environmentally relevant range of osmotic potentials (ΔΨo) using model ecosystems exhibiting a heterogeneous distribution of the soil-borne bacterium Pseudomonas putida KT2440. Three systematically manipulated scenarios allowed us to cover the effects of (i) substrate diffusion, (ii) substrate diffusion and autonomous bacterial dispersal, and (iii) substrate diffusion and autonomous as well as mediated bacterial dispersal along glass fiber networks mimicking fungal hyphae. To quantify the relative importance of the different spatial processes, we compared these heterogeneous scenarios to a reference value obtained for each ΔΨo by means of a quasi-optimal scenario in which degraders were ab initio homogeneously distributed. Substrate diffusion as the sole spatial process was insufficient to counteract the disadvantage due to spatial degrader heterogeneity at ΔΨo ranging from 0 to -1 MPa. In this scenario, only 13.8-21.3% of the quasi-optimal biodegradation performance could be achieved. In the same range of ΔΨo values, substrate diffusion in combination with bacterial dispersal allowed between 68.6 and 36.2% of the performance showing a clear downwards trend with decreasing ΔΨo. At -1.5 MPa, however, this scenario performed worse than the diffusion scenario, possibly as a result of energetic disadvantages associated with flagellum synthesis and emerging requirements to exceed a critical population density to resist osmotic stress. Network-mediated bacterial dispersal kept biodegradation almost consistently high with an average of 70.7 ± 7.8%, regardless of the strength of the osmotic stress. We propose that especially fungal network-mediated bacterial dispersal is a key process to achieve high functionality of heterogeneous microbial ecosystems also at reduced osmotic potentials. Thus, mechanical stress by, for example, soil homogenization should be kept low in order to preserve fungal network integrity.
authors.affiliation: UFZ - Helmholtz Centre for Environmental Research, Department of Environmental MicrobiologyLeipzig, Germany; UFZ - Helmholtz Centre for Environmental Research, Department of Environmental BiotechnologyLeipzig, Germany.
authors.forename: Anja
authors.initials: A
authors.lastname: Worrich
authors.affiliation: UFZ - Helmholtz Centre for Environmental Research, Department of Environmental MicrobiologyLeipzig, Germany; UFZ - Helmholtz Centre for Environmental Research, Department of Ecological ModellingLeipzig, Germany.
authors.forename: Sara
authors.initials: S
authors.lastname: König
authors.affiliation: UFZ - Helmholtz Centre for Environmental Research, Department of Ecological Modelling Leipzig, Germany.
authors.forename: Thomas
authors.initials: T
authors.lastname: Banitz
authors.affiliation: UFZ - Helmholtz Centre for Environmental Research, Department of Environmental Microbiology Leipzig, Germany.
authors.forename: Florian
authors.initials: F
authors.lastname: Centler
authors.affiliation: UFZ - Helmholtz Centre for Environmental Research, Department of Ecological ModellingLeipzig, Germany; German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzig, Germany; Institute for Environmental Systems Research, University of OsnabrückOsnabrück, Germany.
authors.forename: Karin
authors.initials: K
authors.lastname: Frank
authors.affiliation: UFZ - Helmholtz Centre for Environmental Research, Department of Environmental Microbiology Leipzig, Germany.
authors.forename: Martin
authors.initials: M
authors.lastname: Thullner
authors.affiliation: UFZ - Helmholtz Centre for Environmental Research, Department of Environmental MicrobiologyLeipzig, Germany; German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzig, Germany.
authors.forename: Hauke
authors.initials: H
authors.lastname: Harms
authors.affiliation: UFZ - Helmholtz Centre for Environmental Research, Department of Environmental Biotechnology Leipzig, Germany.
authors.forename: Anja
authors.initials: A
authors.lastname: Miltner
authors.affiliation: UFZ - Helmholtz Centre for Environmental Research, Department of Environmental Microbiology Leipzig, Germany.
authors.forename: Lukas Y
authors.initials: LY
authors.lastname: Wick
authors.affiliation: UFZ - Helmholtz Centre for Environmental Research, Department of Environmental Biotechnology Leipzig, Germany.
authors.forename: Matthias
authors.initials: M
authors.lastname: Kästner
keywords: Pseudomonas putida; biodegradation; contaminants; diffusion; dispersal networks; heterogeneity; osmotic stress; spatial processes