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      Spatial-Temporal Survey and Occupancy-Abundance Modeling To Predict Bacterial Community Dynamics in the Drinking Water Microbiome

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          ABSTRACT

          Bacterial communities migrate continuously from the drinking water treatment plant through the drinking water distribution system and into our built environment. Understanding bacterial dynamics in the distribution system is critical to ensuring that safe drinking water is being supplied to customers. We present a 15-month survey of bacterial community dynamics in the drinking water system of Ann Arbor, MI. By sampling the water leaving the treatment plant and at nine points in the distribution system, we show that the bacterial community spatial dynamics of distance decay and dispersivity conform to the layout of the drinking water distribution system. However, the patterns in spatial dynamics were weaker than those for the temporal trends, which exhibited seasonal cycling correlating with temperature and source water use patterns and also demonstrated reproducibility on an annual time scale. The temporal trends were driven by two seasonal bacterial clusters consisting of multiple taxa with different networks of association within the larger drinking water bacterial community. Finally, we show that the Ann Arbor data set robustly conforms to previously described interspecific occupancy abundance models that link the relative abundance of a taxon to the frequency of its detection. Relying on these insights, we propose a predictive framework for microbial management in drinking water systems. Further, we recommend that long-term microbial observatories that collect high-resolution, spatially distributed, multiyear time series of community composition and environmental variables be established to enable the development and testing of the predictive framework.

          IMPORTANCE

          Safe and regulation-compliant drinking water may contain up to millions of microorganisms per liter, representing phylogenetically diverse groups of bacteria, archaea, and eukarya that affect public health, water infrastructure, and the aesthetic quality of water. The ability to predict the dynamics of the drinking water microbiome will ensure that microbial contamination risks can be better managed. Through a spatial-temporal survey of drinking water bacterial communities, we present novel insights into their spatial and temporal community dynamics and recommend steps to link these insights in a predictive framework for microbial management of drinking water systems. Such a predictive framework will not only help to eliminate microbial risks but also help to modify existing water quality monitoring efforts and make them more resource efficient. Further, a predictive framework for microbial management will be critical if we are to fully anticipate the risks and benefits of the beneficial manipulation of the drinking water microbiome.

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          Most cited references46

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          Annually reoccurring bacterial communities are predictable from ocean conditions.

          Factors influencing patterns in the distribution and abundance of plant and animal taxa modulate ecosystem function and ecosystem response to environmental change, which is often taken to infer low functional redundancy among such species, but such relationships are poorly known for microbial communities. Using high-resolution molecular fingerprinting, we demonstrate the existence of extraordinarily repeatable temporal patterns in the community composition of 171 operational taxonomic units of marine bacterioplankton over 4.5 years at our Microbial Observatory site, 20 km off the southern California coast. These patterns in distribution and abundance of microbial taxa were highly predictable and significantly influenced by a broad range of both abiotic and biotic factors. These findings provide statistically robust demonstration of temporal patterning in marine bacterial distribution and abundance, which suggests that the distribution and abundance of bacterial taxa may modulate ecosystem function and response and that a significant subset of the bacteria exhibit low levels of functional redundancy as documented for many plant and animal communities.
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            The seasonal structure of microbial communities in the Western English Channel.

            Very few marine microbial communities are well characterized even with the weight of research effort presently devoted to it. Only a small proportion of this effort has been aimed at investigating temporal community structure. Here we present the first report of the application of high-throughput pyrosequencing to investigate intra-annual bacterial community structure. Microbial diversity was determined for 12 time points at the surface of the L4 sampling site in the Western English Channel. This was performed over 11 months during 2007. A total of 182 560 sequences from the V6 hyper-variable region of the small-subunit ribosomal RNA gene (16S rRNA) were obtained; there were between 11 327 and 17 339 reads per sample. Approximately 7000 genera were identified, with one in every 25 reads being attributed to a new genus; yet this level of sampling far from exhausted the total diversity present at any one time point. The total data set contained 17 673 unique sequences. Only 93 (0.5%) were found at all time points, yet these few lineages comprised 50% of the total reads sequenced. The most abundant phylum was Proteobacteria (50% of all sequenced reads), while the SAR11 clade comprised 21% of the ubiquitous reads and approximately 12% of the total sequenced reads. In contrast, 78% of all operational taxonomic units were only found at one time point and 67% were only found once, evidence of a large and transient rare assemblage. This time series shows evidence of seasonally structured community diversity. There is also evidence for seasonal succession, primarily reflecting changes among dominant taxa. These changes in structure were significantly correlated to a combination of temperature, phosphate and silicate concentrations.
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              Use of propidium monoazide for live/dead distinction in microbial ecology.

              One of the prerequisites of making ecological conclusions derived from genetic fingerprints is that bacterial community profiles reflect the live portion of the sample of interest. Propidium monoazide is a membrane-impermeant dye that selectively penetrates cells with compromised membranes, which can be considered dead. Once inside the cells, PMA intercalates into the DNA and can be covalently cross-linked to it, which strongly inhibits PCR amplification. By using PCR after PMA treatment, the analysis of bacterial communities can theoretically be limited to cells with intact cell membranes. Four experiments were performed to study the usefulness of PMA treatment of mixed bacterial communities comprising both intact and compromised cells in combination with end-point PCR by generating community profiles from the following samples: (i) defined mixtures of live and isopropanol-killed cells from pure cultures of random environmental isolates, (ii) wastewater treatment plant influent spiked with defined ratios of live and dead cells, (iii) selected environmental communities, and (iv) a water sediment sample exposed to increasing heat stress. Regions of 16S rRNA genes were PCR amplified from extracted genomic DNA, and PCR products were analyzed by using denaturing gradient gel electrophoresis (DGGE). Results from the first two experiments show that PMA treatment can be of value with end-point PCR by suppressing amplification of DNA from killed cells. The last two experiments suggest that PMA treatment can affect banding patterns in DGGE community profiles and their intensities, although the intrinsic limitations of end-point PCR have to be taken into consideration.
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                Author and article information

                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society of Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                27 May 2014
                May-Jun 2014
                : 5
                : 3
                : e01135-14
                Affiliations
                [ a ]Infrastructure and Environment Research Division, School of Engineering, University of Glasgow, Glasgow, United Kingdom
                [ b ]Department of Civil and Environmental Engineering, University of Michigan, Ann Arbor, Michigan, USA
                Author notes
                Address correspondence to Lutgarde Raskin, raskin@ 123456umich.edu .

                Editor Mary Ann Moran, University of Georgia

                This article is a direct contribution from a member of the American Academy of Microbiology.

                Article
                mBio01135-14
                10.1128/mBio.01135-14
                4045074
                24865557
                88a1f6d8-48bb-414c-b2bc-303047e576f4
                Copyright © 2014 Pinto et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 3.0 Unported license.

                History
                : 6 April 2014
                : 25 April 2014
                Page count
                Pages: 13
                Categories
                Research Article
                Custom metadata
                May/June 2014

                Life sciences
                Life sciences

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