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Applied and Environmental Microbiology, June 2006, p. 4283-4292, Vol. 72, No. 6
0099-2240/06/$08.00+0     doi:10.1128/AEM.00241-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Nitrification in a Biofilm at Low pH Values: Role of In Situ Microenvironments and Acid Tolerance

Microsensor Group, Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany,¹ Faculty of Civil and Environmental Engineering, Technion—Israel Institute of Technology, Technion City, Haifa 32000, Israel²

Received 31 January 2006/ Accepted 20 March 2006

The sensitivity of nitrifying bacteria to acidic conditions is a well-known phenomenon and generally attributed to the lack and/or toxicity of substrates (NH₃ and HNO₂) with decreasing pHs. In contrast, we observed strong nitrification at a pH around 4 in biofilms grown on chalk particles and investigated the following hypotheses: the presence of less acidic microenvironments and/or the existence of acid-tolerant nitrifiers. Microelectrode measurements (in situ and under various experimental conditions) showed no evidence of a neutral microenvironment, either within the highly active biofilm colonizing the chalk surface or within a control biofilm grown on a nonbuffering (i.e., sintered glass) surface under acidic pH. A 16S rRNA approach (clone libraries and fluorescence in situ hybridizations) did not reveal uncommon nitrifying (potentially acid-tolerant) strains. Instead, we found a strongly acidic microenvironment, evidence for a clear adaptation to the low pH in situ, and the presence of nitrifying populations related to subgroups with low K_ms for ammonia (Nitrosopira spp., Nitrosomonas oligotropha, and Nitrospira spp.). Acid-consuming (chalk dissolution) and acid-producing (ammonia oxidation) processes are equilibrated on a low-pH steady state that is controlled by mass transfer limitation through the biofilm. Strong affinity to ammonia and possibly the expression of additional functions, e.g., ammonium transporters, are adaptations that allow nitrifiers to cope with acidic conditions in biofilms and other habitats.