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Applied and Environmental Microbiology, May 2005, p. 2520-2529, Vol. 71, No. 5
0099-2240/05/$08.00+0     doi:10.1128/AEM.71.5.2520-2529.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Succession of Internal Sulfur Cycles and Sulfur-Oxidizing Bacterial Communities in Microaerophilic Wastewater Biofilms

Department of Urban and Environmental Engineering, Graduate School of Engineering, Hokkaido University, Sapporo 060-8628, Japan,¹ Department of Environmental and Civil Engineering, Hachinohe Institute of Technology, Hachinohe 031-8501, Japan²

Received 22 July 2004/ Accepted 2 December 2004

The succession of sulfur-oxidizing bacterial (SOB) community structure and the complex internal sulfur cycle occurring in wastewater biofilms growing under microaerophilic conditions was analyzed by using a polyphasic approach that employed 16S rRNA gene-cloning analysis combined with fluorescence in situ hybridization, microelectrode measurements, and standard batch and reactor experiments. A complete sulfur cycle was established via S⁰ accumulation within 80 days in the biofilms in replicate. This development was generally split into two phases, (i) a sulfur-accumulating phase and (ii) a sulfate-producing phase. In the first phase (until about 40 days), since the sulfide production rate (sulfate-reducing activity) exceeded the maximum sulfide-oxidizing capacity of SOB in the biofilms, H₂S was only partially oxidized to S⁰ by mainly Thiomicrospira denitirificans with NO₃^– as an electron acceptor, leading to significant accumulation of S⁰ in the biofilms. In the second phase, the SOB populations developed further and diversified with time. In particular, S⁰ accumulation promoted the growth of a novel strain, strain SO07, which predominantly carried out the oxidation of S⁰ to SO₄^2– under oxic conditions, and Thiothrix sp. strain CT3. In situ hybridization analysis revealed that the dense populations of Thiothrix (ca. 10⁹ cells cm^–3) and strain SO07 (ca. 10⁸ cells cm^–3) were found at the sulfur-rich surface (100 µm), while the population of Thiomicrospira denitirificans was distributed throughout the biofilms with a density of ca. 10⁷ to 10⁸ cells cm^–3. Microelectrode measurements revealed that active sulfide-oxidizing zones overlapped the spatial distributions of different phylogenetic SOB groups in the biofilms. As a consequence, the sulfide-oxidizing capacities of the biofilms became high enough to completely oxidize all H₂S produced by SRB to SO₄^2– in the second phase, indicating establishment of the complete sulfur cycle in the biofilms.

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