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Biofilm formation enables free-living nitrogen-fixing rhizobacteria to fix nitrogen under aerobic conditions.

ABSTRACT: The multicellular communities of microorganisms known as biofilms are of high significance in agricultural setting, yet it is largely unknown about the biofilm formed by nitrogen-fixing bacteria. Here we report the biofilm formation by Pseudomonas stutzeri A1501, a free-living rhizospheric bacterium, capable of fixing nitrogen under microaerobic and nitrogen-limiting conditions. P. stutzeri A1501 tended to form biofilm in minimal media, especially under nitrogen depletion condition. Under such growth condition, the biofilms formed at the air-liquid interface (termed as pellicles) and the colony biofilms on agar plates exhibited nitrogenase activity in air. The two kinds of biofilms both contained large ovoid shape 'cells' that were multiple living bacteria embedded in a sac of extracellular polymeric substances (EPSs). We proposed to name such large 'cells' as A1501 cyst. Our results suggest that the EPS, especially exopolysaccharides enabled the encased bacteria to fix nitrogen while grown under aerobic condition. The formation of A1501 cysts was reversible in response to the changes of carbon or nitrogen source status. A1501 cyst formation depended on nitrogen-limiting signaling and the presence of sufficient carbon sources, yet was independent of an active nitrogenase. The pellicles formed by Azospirillum brasilense, another free-living nitrogen-fixing rhizobacterium, which also exhibited nitrogenase activity and contained the large EPS-encapsuled A1501 cyst-like 'cells'. Our data imply that free-living nitrogen-fixing bacteria could convert the easy-used carbon sources to exopolysaccharides in order to enable nitrogen fixation in a natural aerobic environment.

SUBMITTER: Wang D

PROVIDER: S-EPMC5520150 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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Biofilm formation enables free-living nitrogen-fixing rhizobacteria to fix nitrogen under aerobic conditions.

Wang Di D Xu Anming A Elmerich Claudine C Ma Luyan Z LZ

The ISME journal 20170324 7

The multicellular communities of microorganisms known as biofilms are of high significance in agricultural setting, yet it is largely unknown about the biofilm formed by nitrogen-fixing bacteria. Here we report the biofilm formation by Pseudomonas stutzeri A1501, a free-living rhizospheric bacterium, capable of fixing nitrogen under microaerobic and nitrogen-limiting conditions. P. stutzeri A1501 tended to form biofilm in minimal media, especially under nitrogen depletion condition. Under such g ...[more]

PMID: 28338674

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Project description:Biological nitrogen fixation requires large amounts of energy in the form of ATP and low potential electrons to overcome the high activation barrier for cleavage of the dinitrogen triple bond. The model aerobic nitrogen-fixing bacteria, Azotobacter vinelandii, generates low potential electrons in the form of reduced ferredoxin (Fd) and flavodoxin (Fld) using two distinct mechanisms via the enzyme complexes Rnf and Fix. Both Rnf and Fix are expressed during nitrogen fixation, but deleting either rnf1 or fix genes has little effect on diazotrophic growth. However, deleting both rnf1 and fix eliminates the ability to grow diazotrophically. Rnf and Fix both use NADH as a source of electrons, but overcoming the energetics of NADH's endergonic reduction of Fd/Fld is accomplished through different mechanisms. Rnf harnesses free energy from the chemiosmotic potential, whereas Fix uses electron bifurcation to effectively couple the endergonic reduction of Fd/Fld to the exergonic reduction of quinone. Different reaction stoichiometries and condition-specific differential gene expression indicate specific roles for the two reactions. This work's complementary physiological studies and thermodynamic modeling reveal how Rnf and Fix balance redox homeostasis in various conditions. Specifically, the Fix complex is required for efficient growth under low oxygen concentrations, while Rnf is presumed to maintain reduced Fd/Fld production for nitrogenase under standard conditions. This work provides a framework for understanding how the production of low potential electrons sustains robust nitrogen fixation in various conditions. IMPORTANCE The availability of fixed nitrogen is critical for life in many ecosystems, from extreme environments to agriculture. Due to the energy demands of biological nitrogen fixation, organisms must tailor their metabolism during diazotrophic growth to deliver the energy requirements to nitrogenase in the form of ATP and low potential electrons. Therefore, a complete understanding of diazotrophic energy metabolism and redox homeostasis is required to understand the impact on ecological communities or to promote crop growth in agriculture through engineered diazotrophs.

Project description:Nitrogen (N) deficiency limits crop productivity. In this study, rhizoengineering with biofilm producing rhizobacteria (BPR) contributing to productivity, physiology, and bioactive contents in tomato was examined under N-deficient field conditions. Here, different BPR including Leclercia adecarboxylata ESK12, Enterobacter ludwigii ESK17, Glutamicibacter arilaitensis ESM4, E. cloacae ESM12, Bacillus subtilis ESM14, Pseudomonas putida ESM17 and Exiguobacterium acetylicum ESM24 were used for the rhizoengineering of tomato plants. Rhizoengineered plants showed significant increase in growth attributes (15.73%-150.13 %) compared to the control plants. However, production of hydrogen peroxide (21.49-59.38 %), electrolyte leakage (19.5-38.07 %) and malondialdehyde accumulation (36.27-46.31 %) were increased remarkably more in the control plants than the rhizoengineered plants, thus N deficiency induced the oxidative stress. Compared to the control, photosynthetic rate, leaf temperature, stomatal conductance, intrinsic and instantaneous water use efficiency, relative water content, proline and catalase activity were incredibly enhanced in the rhizoengineered plants, suggesting both non-enzymatic and enzymatic antioxidant systems might protect tomato plants from oxidative stress under N-deficient field conditions. Yield (10.24-66.21 %), lycopene (4.8-7.94 times), flavonoids (52.32-110.46 %), phenolics (9.79-23.5 %), antioxidant activity (34.09-86.36 %) and certain minerals were significantly increased in the tomatoes from rhizoengineered plants. The principal component analysis (PCA) revealed that tomato plants treated with BPR induced distinct profiles compared to the control. Among all the applied BPR strains, ESM4 and ESM14 performed better in terms of biomass production, while ESK12 and ESK17 showed better results for reducing oxidative stress and increasing bioactive compounds in tomato, respectively. Thus, rhizoengineering with BPR can be utilized to mitigate the oxidative damage and increase the productivity and bioactive compounds in tomato under N-deficient field conditions.

Dataset Information

Biofilm formation enables free-living nitrogen-fixing rhizobacteria to fix nitrogen under aerobic conditions.

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Biofilm formation enables free-living nitrogen-fixing rhizobacteria to fix nitrogen under aerobic conditions.

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