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Groundwater Microbial Diversity and Antibiotic Resistance Linked to Human Population Density in Yucatan Peninsula, Mexico

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Groundwater Microbial Diversity and Antibiotic Resistance Linked to Human Population Density in Yucatan Peninsula, Mexico Canadian Journal of Microbiology Groundwater microbial diversity and antibiotic resistance linked to human population density in Yucatan Peninsula, Mexico Journal: Canadian Journal of Microbiology Manuscript ID cjm-2019-0173.R2 Manuscript Type: Article Date Submitted by the 24-Sep-2019 Author: Complete List of Authors: Moore, Anni; Morningside College, Biology and Chemistry Lenczewski, Melissa; Northern Illinois University, Geology and Environmental Geosciences Leal-Bautista,Draft Rosa Maria; Centro de Investigación Científica de Yucatán Duvall, Melvin; Northern Illinois University, Biological Sciences Keyword: antibiotic resistance, karst, groundwater, microbial communities Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/cjm-pubs Page 1 of 50 Canadian Journal of Microbiology 1 1 Groundwater microbial diversity and antibiotic resistance linked to human population 2 density in Yucatan Peninsula, Mexico 3 4 5 Anni Moore,a* Melissa Lenczewskib#, Rosa Maria Leal-Bautistac, and Melvin Duvalla,d 6 7 Department of Biological Science, Northern Illinois University, DeKalb, IL USAa 8 Department of Geology and Environmental Geosciences, Northern Illinois University, 9 DeKalb, IL, USAb 10 Water Science Unit, Centro de Investigacion Cientifica de Yucatan, Cancun, QR, Mexicoc 11 Institute for the Study of the Environment,Draft Sustainability, and Energy, Northern Illinois 12 University, DeKalb, IL USAd 13 # Corresponding Author https://mc06.manuscriptcentral.com/cjm-pubs Canadian Journal of Microbiology Page 2 of 50 2 14 ABSTRACT 15 Microbial community composition in selected karst groundwater sites in the Yucatan 16 Peninsula, Mexico was assessed to determine the environmental variables influencing 17 groundwater microbial diversity. The karst aquifer system is a groundwater dependent 18 ecosystem and is the world’s second largest underwater karst cave system. The area’s 19 geology allows precipitation to infiltrate into the groundwater system and prevents 20 accumulation of surface water; as such, groundwater is the only source of fresh water on the 21 peninsula. The sampling locations consisted of three karst sinkholes that extend through the 22 freshwater zone into the saline water, and an abandoned drinking water well of an ocean-side 23 resort during the dry and rainy seasons. The analysis showed that highly diverse microbial 24 communities are present in the YucatanDraft groundwater, sustained by permanently warm 25 temperatures and high nutrient input from human activity. Proximity to densely populated 26 areas, such as tourist resorts, is the most important factor influencing both diversity, presence 27 of fecal bacteria, and antibiotic resistance profile. 28 29 Key Words: microbial communities, karst, groundwater, antibiotic resistance 30 31 https://mc06.manuscriptcentral.com/cjm-pubs Page 3 of 50 Canadian Journal of Microbiology 3 32 INTRODUCTION 33 34 Yucatan Peninsula, Mexico, lacks surface water, and is completely dependent on groundwater 35 for its freshwater needs. At the same time, the Yucatan aquifer is also extremely vulnerable to 36 pollution due to the karst geology and the increased population and tourism that often lacks 37 adequate sewage treatment and disposal options. As a result, the fresh groundwater in most 38 parts of the peninsula is now unsuitable for human consumption. 39 40 The geological features that contribute to the vulnerability of the aquifer are the highly 41 permeable bedrock and inadequate soil covering. The bedrock consists of karstified soft and 42 porous marine carbonate rocks, formingDraft a highly cavernous terrain (Perry et al. 2009). Its 43 permeability is enhanced further by extensive fracturing of the terrain, allowing saltwater flow 44 into the cave system and resulting in subsurface erosion, collapse of the cave roofs, and 45 formation of an extensive network of caves and karst sinkholes (Perry et al. 2009; Gines and 46 Gines 2007). The mean depth of the soil cover of the peninsula is 7.2 cm (White and Hood 47 2004), which allows water at the surface to infiltrate quickly and directly into the aquifer 48 (Perry et al. 2003). The lack of sufficient soil cover together with the karst cannot provide 49 sufficient filtering of contaminants (chemical or biological) into the aquifer. 50 51 The aquifer of the peninsula is characterized by a thin freshwater lens overlaying the 52 seawater-derived saline layer (Lefticaru et al. 2006). This permanent stratification is sustained 53 due to the density difference between the fresh and saline waters, and a narrow mixing zone 54 (interface) exists between the two. The thickness of the freshwater layer varies throughout the https://mc06.manuscriptcentral.com/cjm-pubs Canadian Journal of Microbiology Page 4 of 50 4 55 peninsula from less than 10 m near the coast to over 60 m in the center of the peninsula. The 56 aquifer can easily be accessed through the karst sinkholes locally called cenotes that penetrate 57 deep into the saline layer of the aquifer. 58 59 The main threat to the aquifer comes from human activities. While the lack of large-scale 60 industrial development has kept the aquifer free from various industrial pollutants, the aquifer 61 of Yucatan Peninsula is threatened mainly by municipal human waste. This has become an 62 especially acute problem since the planned development of major tourist destinations on the 63 Caribbean coast caused the population of eastern state of Quintana Roo to explode from 64 88,150 in 1970 (Instituto Nacional de Estadística, Geografía e Informática 2001) to 1.326 65 million in 2010 (Instituto Nacional de DraftEstadística y Geografía 2013) with 17 million tourists 66 in 2017 (Instituto Nacional de Estadística y Geografía 2019). While this kind of planned 67 development has economically benefited the local population, the development of adequate 68 wastewater treatment has not kept up with the development of tourist resorts. 69 70 As a result, the freshwater aquifer, which is the only source of drinking water for the 71 peninsula, is most notably contaminated with fecal bacteria, which has great health and 72 economic impacts on the population (Pacheco et al. 2000). While the aquifer is well 73 characterized geochemically, no studies have looked at the native groundwater microbial 74 communities, their response to pollution, and their potential to deal with the high nutrient load 75 introduced into the aquifer. This information will provide both an overview of the 76 biogeochemical interactions in the aquifer and should help improve groundwater 77 management. https://mc06.manuscriptcentral.com/cjm-pubs Page 5 of 50 Canadian Journal of Microbiology 5 78 79 This study aims to investigate the overall microbial diversity and genomic potential in the 80 groundwater, to determine which environmental variables drive the overall diversity, how 81 these factors influence the presence of fecal indicator bacteria, pathogens, cyanobacteria, and, 82 at the genomic level, antimicrobial and heavy metal resistance, and bacterial degradation of 83 aromatic hydrocarbons. 84 85 86 Draft https://mc06.manuscriptcentral.com/cjm-pubs Canadian Journal of Microbiology Page 6 of 50 6 87 MATERIALS AND METHODS: 88 89 Sampling sites 90 91 Three cenotes (Cenote X, U, and C) and an abandoned drinking water well were sampled in 92 the Yucatan Peninsula (Figure 1 and Table 1). Cenote X is located in a remote area, 93 surrounded by woods and agricultural fields. The freshwater layer of Cenote X is 94 characterized by eutrophic growth during the hot, rainy season, and turnover event in October 95 or November when the warm surface layer of water begins to cool, becomes denser, and 96 sinks, bringing the clear freshwater up from deeper layers. The dry season is characterized by 97 relatively clear freshwater layer. The edgeDraft of the cenote is lined by trees, allowing vegetation 98 input. Cenote U is also located in a remote area, surrounded by woods and agricultural fields, 99 and it serves as a water source for the surrounding farms. Cenote U is in a partially collapsed 100 cave, limiting the vegetation input. Cenote U is characterized by clear water throughout the 101 year. Cenote C is located at the closed territory of a limestone quarry without public access to 102 the water. The nearest resort and the coast are about 3 km distant, and the nearest town about 103 8 km east of the cenote. The groundwater flow is towards the sea, and there are no towns 104 located within the 20 km ‘upstream’ from the cenote, although there are a few single houses 105 about 10-15 km west and northwest of the site. Cenote C is partially covered with a limestone 106 ledge (uncollapsed part of the former cave roof), limiting the vegetation input. Cenote C is 107 characterized by exceptionally clear water during both dry and rainy seasons. 108 https://mc06.manuscriptcentral.com/cjm-pubs Page 7 of 50 Canadian Journal of Microbiology 7 109 The abandoned well is located on the campus of a busy tourist resort and was abandoned 110 because of saline water intrusion. The well is located about 0.5 km from the coast. It is 111 completely covered with no light or vegetation input, and no public access. The resort 112 operates its own moving bed biofilm reactor type wastewater treatment facility. This 113 technology is compact and convenient to operate, although its efficiency of nutrient removal 114 (COD, BOD, phosphate and nitrate) is half of the fixed-bed bioreactor (Choi, Lee, and Lee 115 2012). The volume of sewage handled by this specific facility and the output volume are not 116 available. The effluent of these treatment facilities (owned by the hotel group in multiple 117 tropical locations globally) has traditionally been used by that hotel chain for irrigation 118 purposes (50%) and deposited into injection wells (50%) (National Environment and Planning 119 Agency 2008). Draft 120 121 Water Sampling 122 123 Water samples were obtained from the four sites during two dry seasons (December 2008 or 124 March 2009), and one rainy season (July 2009).
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