Effect of disinfectant, water age, and pipe materials on bacterial and eukaryotic community structure in drinking water biofilm.

Availability of safe, pathogen-free drinking water is vital to public health; however, it is impossible to deliver sterile drinking water to consumers. Recent microbiome research is bringing new understanding to the true extent and diversity of microbes that inhabit water distribution systems. The purpose of this study was to determine how water chemistry in main distribution lines shape the microbiome in drinking water biofilms and to explore potential associations between opportunistic pathogens and indigenous drinking water microbes. Effects of disinfectant (chloramines, chlorine), water age (2.3 days, 5.7 days), and pipe material (cement, iron, PVC) were compared in parallel triplicate simulated water distribution systems. Pyrosequencing was employed to characterize bacteria and terminal restriction fragment polymorphism was used to profile both bacteria and eukaryotes inhabiting pipe biofilms. Disinfectant and water age were both observed to be strong factors in shaping bacterial and eukaryotic community structures. Pipe material only influenced the bacterial community structure (ANOSIM test, P < 0.05). Interactive effects of disinfectant, pipe material, and water age on both bacteria and eukaryotes were noted. Disinfectant concentration had the strongest effect on bacteria, while dissolved oxygen appeared to be a major driver for eukaryotes (BEST test). Several correlations of similarity metrics among populations of bacteria, eukaryotes, and opportunistic pathogens, as well as one significant association between mycobacterial and proteobacterial operational taxonomic units, provides insight into means by which manipulating the microbiome may lead to new avenues for limiting the growth of opportunistic pathogens (e.g., Legionella) or other nuisance organisms (e.g., nitrifiers).

[1]  A. Warren,et al.  Direct toxicity assessment of two soils amended with sewage sludge contaminated with heavy metals using a protozoan (Colpoda steinii) bioassay. , 1997 .

[2]  J. Peplies,et al.  Identification and phylogeny of eukaryotic 18S rDNA phylotypes detected in chlorinated finished drinking water samples from three Parisian surface water treatment plants , 2009, Letters in applied microbiology.

[3]  J. Tay,et al.  Metabolic response of biofilm to shear stress in fixed‐film culture , 2001, Journal of applied microbiology.

[4]  Y. Martinez,et al.  A study on the susceptibility of the model legume plant Medicago truncatula to the soil-borne pathogen Fusarium oxysporum , 2010, European Journal of Plant Pathology.

[5]  M. Edwards,et al.  Implications of nutrient release from iron metal for microbial regrowth in water distribution systems. , 2005, Water research.

[6]  John M. Regan,et al.  Ammonia- and Nitrite-Oxidizing Bacterial Communities in a Pilot-Scale Chloraminated Drinking Water Distribution System , 2002, Applied and Environmental Microbiology.

[7]  M. Vieira,et al.  Interaction of legionella pneumophila and helicobacter pylori with bacterial species isolated from drinking water biofilms , 2011, BMC Microbiology.

[8]  Min Yang,et al.  Pyrosequencing analysis of eukaryotic and bacterial communities in faucet biofilms. , 2012, The Science of the total environment.

[9]  G. Bitton.  Drinking Water Distribution Systems: Biofilm Microbiology , 2014 .

[10]  A. Martín-González,et al.  Evaluation of heavy metal acute toxicity and bioaccumulation in soil ciliated protozoa. , 2006, Environment international.

[11]  J. Isaac-Renton,et al.  Characteristics of an Acanthamoeba keratitis outbreak in British Columbia between 2003 and 2007. , 2012, Ophthalmology.

[12]  E. Anaissie,et al.  The hospital water supply as a source of nosocomial infections: a plea for action. , 2002, Archives of internal medicine.

[13]  P. Borella,et al.  Ecological behaviour of three serogroups of Legionella pneumophila within a model plumbing system , 2011, Biofouling.

[14]  B. Rittman,et al.  The effect of shear stress on biofilm loss rate. , 1982, Biotechnology and bioengineering.

[15]  Taeho Lee,et al.  Microbial diversity in biofilms on water distribution pipes of different materials. , 2010, Water science and technology : a journal of the International Association on Water Pollution Research.

[16]  M. Lechevallier,et al.  Survival of Mycobacterium avium in a model distribution system. , 2004, Water research.

[17]  Y. Lévi,et al.  Amoebae in domestic water systems: resistance to disinfection treatments and implication in Legionella persistence , 2004, Journal of applied microbiology.

[18]  Michael Mitzenmacher,et al.  Detecting Novel Associations in Large Data Sets , 2011, Science.

[19]  C. Steiner,et al.  Nontuberculous Mycobacteria–associated Lung Disease in Hospitalized Persons, United States, 1998–2005 , 2009, Emerging infectious diseases.

[20]  L. Forney,et al.  Molecular microbial ecology: land of the one-eyed king. , 2004, Current opinion in microbiology.

[21]  Amy Pruden,et al.  Probiotic approach to pathogen control in premise plumbing systems? A review. , 2013, Environmental science & technology.

[22]  M. Friedrich,et al.  Formation of Pseudo-Terminal Restriction Fragments, a PCR-Related Bias Affecting Terminal Restriction Fragment Length Polymorphism Analysis of Microbial Community Structure , 2003, Applied and Environmental Microbiology.

[23]  Michael J Beach,et al.  Surveillance for waterborne disease outbreaks associated with drinking water---United States, 2007--2008. , 2011, Morbidity and mortality weekly report. Surveillance summaries.

[24]  Marsha Pryor,et al.  Introduction of Monochloramine into a Municipal Water System: Impact on Colonization of Buildings by Legionella spp , 2006, Applied and Environmental Microbiology.

[25]  K. Schleifer,et al.  Microbiological safety of drinking water. , 2000, Annual review of microbiology.

[26]  Hans H. Cheng,et al.  Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA , 1997, Applied and environmental microbiology.

[27]  A. Vantarakis,et al.  Environmental Mycobacteria in Drinking Water Before and After Replacement of the Water Distribution Network , 2000 .

[28]  Anders F. Andersson,et al.  Short-Term Antibiotic Treatment Has Differing Long-Term Impacts on the Human Throat and Gut Microbiome , 2010, PloS one.

[29]  L. Tranvik,et al.  Unraveling assembly of stream biofilm communities , 2012, The ISME Journal.

[30]  Marsha A. Pryor,et al.  Effect of GAC pre-treatment and disinfectant on microbial community structure and opportunistic pathogen occurrence. , 2013, Water research.

[31]  R. Wadowsky,et al.  Satellite growth of Legionella pneumophila with an environmental isolate of Flavobacterium breve , 1983, Applied and environmental microbiology.

[32]  Sherline H Lee,et al.  Surveillance for waterborne-disease outbreaks associated with recreational water--United States, 2001-2002. , 2004, Morbidity and mortality weekly report. Surveillance summaries.

[33]  Mark W. LeChevallier,et al.  Pyrosequencing Analysis of Bacterial Biofilm Communities in Water Meters of a Drinking Water Distribution System , 2010, Applied and Environmental Microbiology.

[34]  N. Ashbolt,et al.  Differential growth of Legionella pneumophila strains within a range of amoebae at various temperatures associated with in‐premise plumbing , 2011, Letters in applied microbiology.

[35]  Young-June Choi,et al.  Effects of diverse water pipe materials on bacterial communities and water quality in the annular reactor. , 2011, Journal of microbiology and biotechnology.

[36]  P. Borella,et al.  Effect of Bacterial Interference on Biofilm Development by Legionella pneumophila , 2008, Current Microbiology.

[37]  Ramon G. Lee,et al.  Disinfecting Biofilms in a Model Distribution System , 1990 .

[38]  Nicholas J Ashbolt,et al.  Do free-living amoebae in treated drinking water systems present an emerging health risk? , 2011, Environmental science & technology.

[39]  T. Lueders,et al.  An optimised PCR/T-RFLP fingerprinting approach for the investigation of protistan communities in groundwater environments. , 2008, Journal of microbiological methods.

[40]  F. Brockman,et al.  Effect of PCR template concentration on the composition and distribution of total community 16S rDNA clone libraries , 1997, Molecular ecology.

[41]  H. Badali,et al.  Molecular characterisation and pathogenicity of Phaeoacremonium spp. associated with esca disease of grapevine in Northern Iran , 2013 .

[42]  N. Ashbolt,et al.  Eukaryotic diversity in premise drinking water using 18S rDNA sequencing: implications for health risks , 2013, Environmental Science and Pollution Research.

[43]  Patrick D. Schloss,et al.  Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies , 2011, PloS one.

[44]  M. Meckes,et al.  Population diversity in model potable water biofilms receiving chlorine or chloramine residual , 2005, Biofouling.

[45]  W. Verstraete,et al.  Inhibition of Legionella pneumophila by Bacillus sp. , 2007 .

[46]  A. McBain,et al.  Protozoan grazing and its impact upon population dynamics in biofilm communities , 2005, Journal of applied microbiology.

[47]  W. Liesack,et al.  The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations , 1997, Applied and environmental microbiology.

[48]  P. Servais,et al.  Impacts of pipe materials on densities of fixed bacterial biomass in a drinking water distribution system , 2000 .

[49]  H. Smidt,et al.  Free-Living Protozoa in Two Unchlorinated Drinking Water Supplies, Identified by Phylogenic Analysis of 18S rRNA Gene Sequences , 2009, Applied and Environmental Microbiology.

[50]  F. Ollevier,et al.  Impact of Non-Legionella Bacteria on the Uptake and Intracellular Replication of Legionella pneumophila in Acanthamoeba castellanii and Naegleria lovaniensis , 2005, Microbial Ecology.

[51]  M. Horn,et al.  Mycobacterium avium Infections of Acanthamoeba Strains: Host Strain Variability, Grazing-Acquired Infections, and Altered Dynamics of Inactivation with Monochloramine , 2010, Applied and Environmental Microbiology.

[52]  A. Pruden,et al.  Molecular Survey of the Occurrence of Legionella spp., Mycobacterium spp., Pseudomonas aeruginosa, and Amoeba Hosts in Two Chloraminated Drinking Water Distribution Systems , 2012, Applied and Environmental Microbiology.

[53]  G. Andersen,et al.  Microbial Community Dynamics of an Urban Drinking Water Distribution System Subjected to Phases of Chloramination and Chlorination Treatments , 2012, Applied and Environmental Microbiology.

[54]  P. Bishop,et al.  Free chlorine and monochloramine application to nitrifying biofilm: comparison of biofilm penetration, activity, and viability. , 2011, Environmental science & technology.

[55]  Vicente Gomez-Alvarez,et al.  Metagenomic Analyses of Drinking Water Receiving Different Disinfection Treatments , 2012, Applied and Environmental Microbiology.

[56]  A. Pruden,et al.  Effect of disinfectant, water age, and pipe material on occurrence and persistence of Legionella, mycobacteria, Pseudomonas aeruginosa, and two amoebas. , 2012, Environmental science & technology.

[57]  J. Vanbriesen,et al.  Temporal Variability of Bacterial Diversity in a Chlorinated Drinking Water Distribution System , 2012 .

[58]  J. Beman,et al.  Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Ameet J Pinto,et al.  Bacterial community structure in the drinking water microbiome is governed by filtration processes. , 2012, Environmental science & technology.