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Bottled Aqua Incognita: Microbiota Assembly and Dissolved

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Bottled Aqua Incognita: Microbiota Assembly and Dissolved bioRxiv preprint doi: https://doi.org/10.1101/154732; this version posted June 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Bottled aqua incognita: 2 Microbiota assembly and dissolved organic matter diversity 3 in natural mineral waters 4 5 Celine C. Lesaulnier1#, Craig W. Herbold1#, Claus Pelikan1, David Berry1, Cédric Gérard4, Xavier Le 6 Coz4, Sophie Gagnot4, Jutta Niggemann3, Thorsten Dittmar3, Gabriel A. Singer2#, and 7 Alexander Loy1* 8 9 1University of Vienna, Research Network Chemistry meets Microbiology, Department of Microbiology and 10 Ecosystem Science, Division of Microbial Ecology, Althanstrasse 14, A-1090 Vienna, Austria 11 2Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Department of Ecohydrology, 12 Müggelseedamm 310, D-12587 Berlin, Germany. 13 3University of Oldenburg, Institute for Chemistry and Biology of the Marine Environment, ICBM-MPI 14 Bridging Group for Marine Geochemistry, Carl-von-Ossietzky-Straße 9-11, D-26129 Oldenburg, Germany. 15 4Nestec Ltd., Route du Jorat 57, CH-1000 Lausanne 26, Switzerland 16 17 #Authors contributed equally to this study 18 *Corresponding author: Alexander Loy, University of Vienna, Research Network Chemistry meets 19 Microbiology, Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, 20 Althanstrasse 14, A-1090 Vienna, Austria; [email protected]; Tel. +43 1 4277 76605 21 22 Short title: Microbiota and DOM diversity in bottled waters 23 24 Key words: bottled water, microbial diversity, dissolved organic matter, Fourier transform ion cyclotron 25 resonance mass spectrometry, Aquabacterium, Curvibacter, Polaromonas 26 27 28 29 30 31 32 33 34 35 1 bioRxiv preprint doi: https://doi.org/10.1101/154732; this version posted June 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 36 ABSTRACT 37 Background: Non-carbonated natural mineral waters contain microorganisms that regularly grow after 38 bottling despite low concentrations of dissolved organic matter (DOM). Yet, the compositions of bottled 39 water microbiota and organic substrates that fuel microbial activity, and how both change after bottling, 40 are still largely unknown. 41 Results: We performed a multifaceted analysis of microbiota and DOM diversity in twelve natural mineral 42 waters from six European countries. 16S rRNA gene-based analyses showed that less than ten species-level 43 operational taxonomic units (OTUs) dominated the bacterial communities in the water phase and 44 associated with the bottle wall after a short phase of post-bottling growth. Members of the 45 betaproteobacterial genera Curvibacter, Aquabacterium, and Polaromonas (Comamonadaceae) grew in 46 most waters and represent ubiquitous, mesophilic, heterotrophic aerobes in bottled waters. Ultrahigh- 47 resolution mass spectrometry of DOM in bottled waters and their corresponding source waters identified 48 thousands of molecular formulae characteristic of mostly refractory, soil-derived DOM. 49 Conclusions. The bottle environment, including source water physicochemistry, selected for growth of a 50 similar low-diversity microbiota across various bottled waters. Relative abundance changes of hundreds of 51 multi-carbon molecules were related to growth of less than ten abundant OTUs. We thus speculate that 52 individual bacteria cope with oligotrophic conditions by simultaneously consuming diverse DOM molecules. 53 54 BACKGROUND 55 Bottled water, including natural mineral water, is an increasingly popular source of drinking water around 56 the world and represents a multi-billion-dollar industry. The European Union regulates the exploitation and 57 marketing of natural mineral waters to protect their unique characteristics and original purity. The latest EU 58 Directive 2009/54/EC defines natural mineral water as microbiologically wholesome water of underground 59 origin that is protected from all risk of pollution and can be clearly distinguished from other types of 60 drinking water e.g. by its characteristic content of minerals and trace elements. Furthermore, disinfection 61 or chemical treatment of natural mineral water is not permitted, yet it is routinely tested for its number of 62 cultivable bacteria including several marker organisms (Escherichia coli and other coliforms, faecal 63 streptococci, Pseudomonas aeruginosa, and sporulated sulfite-reducing anaerobes). The largely untreated 2 bioRxiv preprint doi: https://doi.org/10.1101/154732; this version posted June 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 64 nature of natural mineral waters allows that microorganisms from the source water aquifer and possibly 65 the bottling plant (i.e. pipelines, storage tanks) act as inoculum for the bottle environment. Within a few 66 days after bottling members of this ‘seed microbiota’ begin to grow during storage of natural mineral 67 waters at ambient temperature, with absolute cell counts reaching 105-106 cells/mL [1-3]. 68 Such microbial growth in non-carbonated bottled waters is a well-known fact, but the composition of the 69 bottled water microbiota and its post-bottling dynamics have thus far been investigated by molecular 70 techniques in only two natural mineral waters [2, 4]. These and numerous isolation-dependent studies [5-8] 71 have established that Alpha-, Beta-, and Gammaproteobacteria are the prevalent microorganisms in 72 bottled water. Beyond this, many fundamental questions regarding the microbial ecology of bottled waters 73 still remain poorly answered. How different is the microbiota in bottled waters from different sources? 74 How does the bottled water microbiota assemble? Are there differences between the free-living 75 community in the water phase (plankton microbiota) and the inner-bottle-surface-associated community 76 (biofilm microbiota)? 77 A persistent question that has puzzled researchers for decades is what substrates in bottled water may fuel 78 the observed sudden microbial growth [8]? Although autotrophic growth has been suggested [4], it is 79 commonly assumed that bottled water microorganisms mainly generate energy and multiply through 80 heterotrophic utilization of dissolved organic matter (DOM) available in the bottle environment [8]. Ground 81 water, treated drinking water, and oligotrophic surface freshwaters generally have low DOM 82 concentrations in the range of 0.5-5 mg carbon/L. Microorganisms metabolize only a minor fraction (0.01- 83 0.1 mg carbon/L) of this DOM pool while a larger refractory fraction remains untouched [9]. The 84 susceptibility of DOM to microbial turnover depends on its origin and diagenetic history, which define 85 chemical composition [10, 11], and its concentration, which defines the probability of microbial encounter 86 for a specific chemical structure [12]. DOM analytics have been dramatically advanced by the advent of 87 Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR-MS) with ultra-high mass resolution 88 allowing to accurately identify thousands of individual molecular formulae in a single environmental sample 89 [13]. While FT-ICR-MS has provided fundamental insights into the molecular diversity of DOM and its 90 turnover in various aquatic environments such as oceans [12-14], lakes [15], glaciers [11], and groundwater 91 [16, 17], analogous information is not available for bottled drinking water. 3 bioRxiv preprint doi: https://doi.org/10.1101/154732; this version posted June 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 92 Here, we simultaneously analyzed microbiota and DOM composition in twelve European non-carbonated 93 natural mineral waters and their corresponding source waters by multiplexed sequencing of bacterial 16S 94 rRNA gene amplicons, FT-ICR-MS, and complementary analysis of microbiota and physicochemical 95 parameters. Our approach included fine-scale temporal investigation of two representative bottled waters 96 over two months of incubation and detailed comparative analysis of all twelve bottled waters one day after 97 filling in polyethylene terephthalate (PET) bottles. We revealed corresponding patterns in DOM turnover 98 and microbial community development after bottling and thereby provide novel insights into the molecular 99 microbial and chemical ecology of this important drinking water source. 100 101 METHODS 102 103 Sampling and storage of natural mineral waters 104 We analyzed non-carbonated natural mineral waters retrieved from twelve European bottling plants of 105 well-derived mineral water in the years 2011 and 2012 (Supplementary Tables S1-S4). Samples from each 106 plant included bottled water and corresponding well water; the latter was taken before its entry into the 107 bottling plant from a sampling port located at the head of each source. Bottled water 6 receives water from
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