Ammonia-Oxidizing Bacteria in Biofilters Removing. Trihalomethanes are Related to Nitrosomonas oligotropha

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1 AEM Accepts, published online ahead of print on January 0 Appl. Environ. Microbiol. doi:0./aem.0-0 Copyright 0, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved. AOB in Filters Removing THMs Related to N. oligotropha Ammonia-Oxidizing Bacteria in Biofilters Removing Trihalomethanes are Related to Nitrosomonas oligotropha Authors: David G. Wahman *, Mary Jo Kirisits, Lynn E. Katz, and Gerald E. Speitel Jr. United States Environmental Protection Agency, Office of Research and Development, Cincinnati, OH University of Texas at Austin, Department of Civil, Architectural, and Environmental Engineering, Austin, TX * Corresponding author, Mailing address: United States Environmental Protection Agency, W. Martin Luther King Dr., Cincinnati, OH. Phone: () -. Fax: () -. wahman.david@epa.gov 0 ABSTRACT Ammonia-oxidizing bacteria (AOB) in nitrifying biofilters degrading four regulated trihalomethanes - trichloromethane, bromodichloromethane, dibromochloromethane, and tribromomethane - were related to Nitrosomonas oligotropha. N. oligotropha is associated with chloraminated drinking water systems, and their presence in the biofilters might indicate that trihalomethane tolerance is another reason they dominate in chloraminated systems. Keywords: Trihalomethanes; Cometabolism; Nitrification; Disinfection by-products; Drinking water

2 0 0 No evidence indicates trihalomethanes (THMs) support microbial growth, but previous research demonstrated that four regulated THMs - trichloromethane (TCM), bromodichloromethane (BDCM), dibromochloromethane (DBCM), and tribromomethane (TBM) - were cometabolized in batch culture () by Nitrosomonas europaea (an ammoniaoxidizer) and in batch culture () and lab-scale biofilters (, ) by mixed-culture nitrifiers. The current research extended process evaluation by analyzing the ammonia-oxidizing bacteria (AOB) present in biofilters through quantitative real-time PCR (qpcr) and amoa gene sequence analysis. Duplicate anthracite biofilters (-min empty-bed contact time;. gallons min - ft - surface loading rate) were seeded with one of two mixed-cultures (). Trains A and B were seeded with a sample collected from Lake Austin in Austin, Texas (Lake Austin) and Trains C and D were seeded with an enriched nitrifier culture initially dominated by Nitrosomonas oligotropha (N. oligotropha enrichment, provided by Dr. Noguera, University of Wisconsin). Trains were fed mg N/L TOTNH [sum of ammonia-nitrogen (NH -N) and ammoniumnitrogen (NH + -N)]. The three operational periods were based on influent THM concentrations: Period I-TCM/DBCM (0 µg/l TCM and µg/l DBCM), Period II-DBCM ( µg/l DBCM), and Period III-All THMs ( µg/l each of TCM, DBCM, BDCM, and TBM). THM removals are summarized in Table for each period; all biofilters removed THMs with removals ranging from -% (Table ). At Period II s end, backwash water was collected for batch kinetic tests conducted as described previously (). Because backwash water may have contained extracellular material, attachment media, or non-nitrifying organisms, a biomass-independent analysis was required.

3 To accomplish this, a previously described () simplified THM cometabolism model (Equation ) was used: S S kthm TOTNH THM k TOTNH THM 0 = e () 0 0 where S THM0 is the initial THM concentration (µg/l THM); S THM is the final THM concentration (µg/l THM); TOTNH is the initial TOTNH minus final TOTNH (mg N/L); and k THM /k TOTNH is the ratio of THM and TOTNH rate constants (L/mg TOTNH ). The k THM /k TOTNH ratio represents the THM removal efficiency, relating THM to ammonia removal. For comparison purposes, biofilter k THM /k TOTNH ratios were calculated by pooling operational data for duplicate trains [where biofilter THM removal was not statistically different between duplicate trains based on Tukey s paired comparison method with a two-sided % confidence interval of the Studentized Range Statistic (, )]. The backwash batch kinetic test k THM /k TOTNH ratios (Figure ) provided another confirmation that the biofilters were able to degrade THMs (initial concentrations: 0-0 µg/l each THM and mg N/L TOTNH ). At Period III s end, biofilter DNA was isolated using the UltraClean Soil DNA isolation kit (MO BIO Laboratories, Inc., Carlsbad, CA). Biofilters were divided into equally spaced vertical sections (influent end designated Section and effluent end designated Section ). The amoa qpcr method of Regan et al. () was used to assess AOB relative abundance in three general classes: () non-oligotropha Nitrosomonas, () Nitrosospira, and () N. oligotropha. Only N. oligotropha was detected (data not shown), indicating that this is the dominant AOB present. Subsequently, amoa genes from Trains A and C were cloned and sequenced to supplement qpcr results. For cloning, amoa was amplified (), the amplicon purified using the

4 0 0 QIAquick PCR purification kit (Qiagen, Valencia, CA), and cloned using the TOPO TA Cloning Kit for Sequencing (Invitrogen, Carlsbad, CA). The clones were screened for inserts by PCR with M forward and reverse primers. Amplicon was sequenced using Big Dye sequencing chemistry (Applied Biosystems, Foster City, CA). Using MEGA (), -bp sequences (primer sequences removed) were generated, and DOTUR was used to identify amoa gene sequences with more than % similarity () into operational taxonomic units (OTUs). Analyses of cloned amoa gene sequences found two OTUs (GenBank accession numbers HQ and HQ) that were present in both trains (Table ). These OTUs were incorporated into a phylogenetic tree (Figure ) constructed in MEGA by the neighbor-joining method using 0,000 bootstrap replicates. The sequence analysis confirmed the qpcr results as these two OTUs were related to N. oligotropha whether the phylogenetic tree was generated based on amoa gene sequences (data not shown) or on deduced amino acid sequences from the amoa gene sequences (Figure ). Considering deduced amino acid sequences, the Biofilter OTU consensus sequence was a 00% match to samples taken from a wastewater treatment plant activated sludge and membrane bioreactor and to Nitrosomonas NL and NM, and the Biofilter OTU consensus sequence was a 00% match to an environmental sample taken from a chloraminated drinking water distribution system. Taken together, the qpcr and gene sequence analyses show that the dominant AOB in the biofilters used for THM removal were related to N. oligotropha. AOB related to N. oligotropha have been reported as the dominant AOB in chloraminated drinking water systems (-). Because these systems contain THMs at levels similar to those used in our biofilter experiments, it is possible that one reason for the presence of AOB related to N. oligotropha in chloraminated drinking water systems is their ability to tolerate THMs. This is supported by Bayer () who

5 0 found that the transformation capacities (including an N. oligotropha dominated culture) were greater than those for N. europaea (). Overall, four regulated THMs found in treated drinking water were degraded in biofilters seeded with Lake Austin and N. oligotropha enrichment cultures. The ability of the biofilter biomass to remove THMs was verified in batch kinetic tests. amoa qpcr and gene sequence analyses demonstrated that the biofilter AOB were related to N. oligotropha. Their presence in biofilters removing THMs suggests that one potential reason for their dominance in these systems is their THM tolerance. Future research should broaden the nitrifier community analysis to include ammonia-oxidizing archaea as they are being reported in drinking water systems (, ). The authors thank Dr. John M. Regan and Dr. Daniel R. Noguera. Research was funded by AwwaRF. Any opinions expressed are those of the authors and do not necessarily reflect the views of U.S. Environmental Protection Agency or AwwaRF; therefore, no official endorsement should be inferred. Any mention of trade names or commercial products does not constitute endorsement or recommendation for use.

6 References. Bayer, B. M., and G. E. Speitel, Jr. 00. Significance of trihalomethanes in preventing distribution system nitrification, American Water Works Assocation Annual Conference Proceedings, Toronto, Ontario, Canada.. Berthouex, P. M., and L. C. Brown. 00. Statistics for environmental engineers. Lewis Publishers, Boca Raton.. Felsenstein, J.. Confidence limits on phylogenies: An approach using the bootstrap. Evolution :-. 0. Harter, H. L. 0. Tables of range and studentized range. Ann. Math Stat. :-.. Jones, D. T., W. R. Taylor, and J. M. Thornton.. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. :-.. Kasuga, I., H. Nakagaki, F. Kurisu, and H. Furumai. 00. Predominance of ammonia-oxidizing archaea on granular activated carbon used in a full-scale advanced drinking water treatment plant. Water Res. :0-0.. Regan, J. M., A.-Y. Cho, S. Kim, and C. D. Smith. 00. Monitoring ammoniaoxidizing bacteria in chloraminated distribution systems. Awwa Research Foundation, Denver, Colorado. 0. Regan, J. M., G. W. Harrington, H. Baribeau, R. D. Leon, and D. R. Noguera. 00. Diversity of nitrifying bacteria in full-scale chloraminated distribution systems. Water Res. :-0.. Regan, J. M., G. W. Harrington, and D. R. Noguera. 00. Ammonia- and nitriteoxidizing bacterial communities in a pilot-scale chloraminated drinking water distribution system. Appl. Environ. Microbiol. :-. 0. Saitou, N., and M. Nei.. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. :0-.

7 . Schloss, P. D., and J. Handelsman. 00. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. :0-0.. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 00. MEGA: Molecular evolutionary genetics analysis (MEGA) software version.0. Mol. Biol. Evol. :-.. van der Wielen, P. W. J. J., S. Voost, and D. van der Kooij. 00. Ammonia-oxidizing bacteria and archaea in groundwater treatment and drinking water distribution systems. Appl. Environ. Microbiol. :-. 0. Wahman, D. G., A. E. Henry, L. E. Katz, and G. E. Speitel, Jr. 00. Cometabolism of trihalomethanes by mixed culture nitrifiers. Water Res. 0:-.. Wahman, D. G., L. E. Katz, and G. E. Speitel, Jr. 00. Cometabolism of trihalomethanes by Nitrosomonas europaea. Appl. Environ. Microbiol. :0-.. Wahman, D. G., L. E. Katz, and G. E. Speitel, Jr. 00. Performance and biofilm activity of nitrifying biofilters removing trihalomethanes. Water Res. doi:0.0/j.watres Wahman, D. G., L. E. Katz, and G. E. Speitel, Jr. 00. Trihalomethane cometabolism by a mixed-culture nitrifying biofilter. J. Am. Water Works Ass. :-0.

8 Table. Biofilter performance (mean ± standard deviation). Trains were nominally fed mg N/L TOTNH [sum of ammonia-nitrogen (NH -N) and ammonium-nitrogen (NH + -N)]. The three operational periods were based on influent THM concentrations: Period I- TCM/DBCM (0 µg/l TCM and µg/l DBCM), Period II-DBCM ( µg/l DBCM), and Period III-All THMs ( µg/l each of TCM, BDCM, DBCM, and TBM). Train Period No. of Samples 0- TOTNH (mg N/L) Percent Removals TCM BDCM DBCM TBM I.±0..±. ±. A II.±0. ±. III.±0. ±. ±. ±. ±. I.±0..±. ±. B II.0±0. ±.0 III.±0. ±. ±.0 ±. ±. I.±0..±.0 ±.0 C II.±0. ±.0 III.±0. ±. ±. ±.0 ±. I.0±0..±. ±. D II.±0. 0±. III.±. ±. ±. ±. ±. 0- TOTNH = TOTNH removed through biofilter (mg N/L) TCM = trichloromethane BDCM = bromodichloromethane DBCM = dibromochloromethane TBM = tribromomethane

9 Table. amoa gene sequences and OTU biofilter sample summary. The influent end of the biofilter was designated as Section, with the numbering progressing down the length of the biofilter in equal lengths such that the effluent end was designated as Section. Each section was divided into three subsamples that were used for DNA extraction, resulting in triplicate extractions for each section. For the extractions, the mass of dry anthracite used was 0.0 ± 0.0 grams per extraction (wet anthracite moisture content ± 0.%). Sample No. of Biofilter OTU Sequences No. of Biofilter OTU Sequences A (Influent End) 0 A A A (Effluent End) 0 A Total C (Influent End) 0 C 0 C C (Effluent End) 0 C Total A & C Total 0

10 Figure. Backwash batch kinetic test k THM /k TOTNH ratios and associated % confidence limits. A, B, C, and D correspond to experiments conducted with backwash from Trains A, B, C, and D, respectively. For comparison purposes, k THM /k TOTNH ratios were also calculated using Equation and biofilter performance data (LA = Lake Austin and NO = N. oligotropha enrichment). 0 Figure. Phylogenetic tree based on deduced amino acid sequences of the amoa gene sequences of AOB. The evolutionary history was inferred using the Neighbor-Joining method (0). The percentage of replicate trees (those >0%) in which the associated taxa clustered together in the bootstrap test (0,000 replicates) are shown next to the branches (). The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. The evolutionary distances were computed using the JTT matrix-based method () and are in the units of the number of amino acid substitutions per site. Between parenthesis: sequence number belonging to that OTU/total sequence number. 0

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