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The Soil Flagellate Heteromita globosa Accelerates Bacterial Degradation of Alkylbenzenes through Grazing and Acetate Excretion in Batch Culture

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Abstract

The impact of grazing by soil flagellates Heteromita globosa on aerobic biodegradation of benzene by Pseudomonas strain PS+ was examined in batch culture. Growth of H. globosa on these bacteria obeyed Monod kinetics (μmax, 0.17 ± 0.03 h−1; Ks, 1.1 ± 0.2 × 107 bacteria mL−1) and was optimal at a bacteria/ flagellate ratio of 2000. Carbon mass balance showed that 5.2% of total [ring-U-14C]benzene fed to bacteria was subsequently incorporated into flagellate biomass. Growth-inhibiting concentrations (IC50) of alkylbenzenes (benzene, toluene, ethylbenzene) were inversely related with their octanol/ water partitioning coefficients, and benzene was least toxic for bacteria and flagellates with IC50 values of 4392 (± 167) μM and 2770 (± 653) μM, respectively. The first-order rate constant for benzene degradation (k1, 0.48 ± 0.12 day−1) was unaffected by the presence or absence of flagellates in cultures. However, the rate of benzene degradation by individual bacteria averaged three times higher in the presence of flagellates (0.73 ± 0.13 fmol cell−1 h−1) than in their absence (0.26 ± 0.03 fmol cell−1 h−1). Benzene degradation also coincided with higher levels of dissolved oxygen and a higher rate of nitrate reduction in the presence of flagellates (p < 0.02). Grazing by flagellates may have increased the availability of dissolved oxygen to a smaller surviving population of bacteria engaged in the aerobic reactions initiating benzene degradation. In addition, flagellates may also have increased the rate of nitrate reduction through the excretion of acetate as an additional electron donor for these bacteria. Indeed, acetate was shown to progressively accumulate in cultures where flagellates grazed on heat-killed bacteria. This study provided evidence that grazing flagellates stimulate bacterial degradation of alkylbenzenes and provide a link for carbon cycling to consumers at higher trophic levels. This may have important implications for bioremediation processes.

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Acknowledgments

The authors thank the New Energy and Industrial Technology Development Organization (NEDO) for funding this study under the project “Development of Technologies for Analyzing and Controlling the Mechanism of Biodegrading and Processing”, and also for providing a personal fellowship to R.G.M.

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Authors and Affiliations

  1. Marine Biotechnology Institute Co., Ltd., 3-75-1 Heita, Kamaishi City, Iwate, 026-0001, Japan

    R.G. Mattison

  2. Technology Center, Building Engineering Research Institute, Taisei Corporation, 344-1, Nase-cho, Totsuka-ku, Yokohama, 245-0051, Japan

    H. Taki

  3. Department of Biotechnology, National Institute of Technology and Evaluation, 2-5-8 Kazusakamatari, Kisarazu-shi, Chiba, 292-0818, Japan

    S. Harayama

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  1. R.G. Mattison
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Correspondence to R.G. Mattison.

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Mattison, R., Taki, H. & Harayama, S. The Soil Flagellate Heteromita globosa Accelerates Bacterial Degradation of Alkylbenzenes through Grazing and Acetate Excretion in Batch Culture. Microb Ecol 49, 142–150 (2005). https://doi.org/10.1007/s00248-003-0226-5

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  • DOI: https://doi.org/10.1007/s00248-003-0226-5

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