Dataset Information

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 (??o) 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 ??o 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 ??o 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 ??o 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 ??o. 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.

SUBMITTER: Worrich A

PROVIDER: S-EPMC4971104 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Bacterial Dispersal Promotes Biodegradation in Heterogeneous Systems Exposed to Osmotic Stress.

Worrich Anja A König Sara S Banitz Thomas T Centler Florian F Frank Karin K Thullner Martin M Harms Hauke H Miltner Anja A Wick Lukas Y LY Kästner Matthias M

Frontiers in microbiology 20160803

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 ...[more]

PMID: 27536297

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Project description:The rate, timing, and mode of species dispersal is recognized as a key driver of the structure and function of communities of macroorganisms, and may be one ecological process that determines the diversity of microbiomes. Many previous studies have quantified the modes and mechanisms of bacterial motility using monocultures of a few model bacterial species. But most microbes live in multispecies microbial communities, where direct interactions between microbes may inhibit or facilitate dispersal through a number of physical (e.g., hydrodynamic) and biological (e.g., chemotaxis) mechanisms, which remain largely unexplored. Using cheese rinds as a model microbiome, we demonstrate that physical networks created by filamentous fungi can impact the extent of small-scale bacterial dispersal and can shape the composition of microbiomes. From the cheese rind of Saint Nectaire, we serendipitously observed the bacterium Serratia proteamaculans actively spreads on networks formed by the fungus Mucor. By experimentally recreating these pairwise interactions in the lab, we show that Serratia spreads on actively growing and previously established fungal networks. The extent of symbiotic dispersal is dependent on the fungal network: diffuse and fast-growing Mucor networks provide the greatest dispersal facilitation of the Serratia species, while dense and slow-growing Penicillium networks provide limited dispersal facilitation. Fungal-mediated dispersal occurs in closely related Serratia species isolated from other environments, suggesting that this bacterial-fungal interaction is widespread in nature. Both RNA-seq and transposon mutagenesis point to specific molecular mechanisms that play key roles in this bacterial-fungal interaction, including chitin utilization and flagellin biosynthesis. By manipulating the presence and type of fungal networks in multispecies communities, we provide the first evidence that fungal networks shape the composition of bacterial communities, with Mucor networks shifting experimental bacterial communities to complete dominance by motile Proteobacteria. Collectively, our work demonstrates that these strong biophysical interactions between bacterial and fungi can have community-level consequences and may be operating in many other microbiomes.

Project description:Soybean (Glycine max (L.) Merr.) is important to the global food industry; however, its productivity is affected by abiotic stresses such as osmosis, flooding, heat, and cold. Here, we evaluated the bioactive extracts of two biostimulant bacterial strains, Bacillus butanolivorans KJ40 and B. siamensis H30-3, for their ability to convey tolerance to osmotic stress in soybean seeds during germination. Soybean seeds were dip-treated in extracts of KJ40 (KJ40E) or H30-3 (H30-3E) and incubated with either 0% or 20% polyethylene glycol 6000 (PEG), simulating drought-induced osmotic stress. We measured malondialdehyde content as a marker for lipid peroxidation, as well as the activity of antioxidant enzymes, including catalase, glutathione peroxidase, and glutathione reductase, together with changes in sugars content. We also monitored the expression of genes involved in the gibberellic acid (GA)-biosynthesis pathway, and abscisic acid (ABA) signaling. Following osmotic stress in the extract-treated seeds, malondialdehyde content decreased, while antioxidant enzyme activity increased. Similarly, the expression of GA-synthesis genes, including GmGA2ox1 and GmGA3 were upregulated in KJ40E-dipped seeds at 12 or 6 h after treatment, respectively. The ABA signaling genes GmABI4 and GmDREB1 were upregulated in H30-3E- and KJ40E-treated seeds at 0 and 12 h after treatment under osmotic stress; however, GmABI5, GmABI4, and GmDREB1 levels were also elevated in the dip-treated seeds in baseline conditions. The GA/ABA ratio increased only in KJ40E-treated seeds undergoing osmotic stress, while glucose content significantly decreased in H30-3E-treated seeds at 24 h after treatment. Collectively, our findings indicated that dip-treatment of soybean seeds in KJ40E and H30-3E can enhance the seeds' resistance to osmotic stress during germination, and ameliorate cellular damage caused by secondary oxidative stress. This seed treatment can be used agriculturally to promote germination under drought stress and lead to increase crop yield and quality.

Dataset Information

Bacterial Dispersal Promotes Biodegradation in Heterogeneous Systems Exposed to Osmotic Stress.

Publications

Bacterial Dispersal Promotes Biodegradation in Heterogeneous Systems Exposed to Osmotic Stress.

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