Elsevier

Environmental Pollution

Volume 282, 1 August 2021, 117003
Environmental Pollution

Exploring prevalence of potential pathogens and fecal indicators in geographically distinct river systems through comparative metagenomics

https://doi.org/10.1016/j.envpol.2021.117003Get rights and content

Highlights

  • Explores, compares the microbiome of Himalayan & Peninsular river systems in India.

  • Interplay between edaphic factors in framing bacterial microbiome discussed.

  • Potential pathogenic & fecal indicators in river analyzed.

  • Provides insights for public health risk prediction and strategic waste management.

  • 25 potentially pathogenic genera & 26 fecal/sewage indicator genera reported.

Abstract

Microbial communities are considered as vital members to reflect the health of a riverine system. Among them, pathogenic and fecal indicators imply health risks involved with potability of river water. The present study explores the diverse microbial communities, distribution pattern of potential pathogens, and fecal indicators between the geographically distinct Himalayan and Peninsular river systems of India. It also inquires into the environmental factors associated with community variance and distribution pattern of microbial indicators. The application of high-throughput amplicon sequencing approach unveiled significant demarcation (p < 0.004, Anosim R = 0.62) of samples suggesting unique microbial diversities in these two river sediments. Random forest analysis revealed Desulfobulbulus, PSB_M_3, and Opitutus in Himalayan, while DA101, Bacillus, and Streptomyces in the Peninsular as significant contributors to develop overall dissimilarity between the river systems. Permutational multivariate analysis of variance and co-occurrence network analysis were used to study the relationships between microbial taxa and environmental factors. Amongst the various studied environmental parameters, pH, K, Ca, Mg, Ba, and Al in the Himalayan and salinity, Na, temperature, and Th in the Peninsular significantly influenced shaping of distinct microbial communities. Furthermore, the potential pathogenic genera, including Flavobacterium, Clostridium, Arcobacter, Pseudomonas, and Bacillus were highly prevalent in both the river systems. Arcobacter, Clostridium, Acinetobacter, Bacteroides, and Caloramator were the prominent fecal indicators in these river systems. Our findings provide salient information about the crucial role and interplay between various environmental factors and anthropogenic influences in framing the microbiome of the distinct river systems in India. Moreover, assessing potential pathogenic and fecal indicators suggest the public health risk associated with untreated sewage discharge into these water sources. The detection of various F/S indicators and potentially pathogenic bacteria in Himalayan and Peninsular river systems emphasize the urgent need for future monitoring and management of major riverine systems in India.

Introduction

Microbes play a critical part in the functioning and balancing of an ecosystem. The sediments near riverbanks harbour unique microbial assemblages for performing the metabolic functions like biogeochemical and nutrient cycling, biophysical processes, and energy flow in the river ecosystems (Liu et al., 2011; Shade et al., 2012, Zhang et al., 2016). Microbial load in the sediments, and their sensitivity towards environmental cues and anthropogenic disturbances are often considered as indicators of river ecosystem health (Chen et al., 2018). Studies have shown that most anthropogenically disturbed river sites foster various pathogenic taxa and fecal indicators that impose serious health issues (Bojarczuk et al., 2018, Páll et al., 2013). Population explosion, industrialization, direct discharge of waste (agricultural, industrial, and fecal matter), and water scarcity are significant contributors to the present degradation of these ecosystems (Chakarvorty et al., 2015). Emergence of novel antibiotic resistant bacterial strains and its associated health risks urge us to explore the microbial community structure of the riverine ecosystems.

Waterborne diseases contribute to about 2.2 M annual deaths globally (Maramraj et al., 2020) and in India, 37.7 million people are affected by this (Ananth et al., 2018). Cholera, gastroenteritis, and diarrhoea break out annually during summer and rainy seasons due to low-quality drinking water and sanitation in the country (Jofre et al., 2009). Therefore, it is vital to monitor fecal contamination and pathogens in the river systems used for human consumption. Conventional monitoring studies rely heavily on the microbial culture-based enumeration of fecal/sewage (F/S) indicator bacteria and assessment of pathogenic bacteria (Srivastava et al., 2017; Vincy et al., 2017). However, since these methods target a few pathogens/fecal/sewage indicator bacteria, comprehensive range monitoring of water bodies is an essential prerequisite. High throughput amplicon sequencing (16S rRNA) through Next Generation Sequencing (NGS) approach could overcome these limitations in exploring the microbial communities and indicators. Few recent studies have utilized such platforms for monitoring various biomes like river (Vadde et al., 2019), shellfish growing areas (Leight et al., 2018) and dairy farm (Zhang et al., 2019a) validating its wide application.

Himalayan and Peninsular river systems of India differ in their origin, geographical aspects, and physicochemical characteristics. River Ganga-Yamuna of the Himalayan river system is amongst the heavily polluted rivers worldwide (Chaudhary and Walker, 2019, Malik et al., 2014). Likewise, Periyar river of the Peninsular river system is considered as exemplars of industrial pollution (Lakshmi and Madhu, 2020). Recently, metagenomics has been utilized to study the microbial diversity of some Indian rivers like Ganga- Yamuna (Reddy and Dubey, 2019; Samson et al., 2019), Godavari (Jani et al., 2018) and Cauvery (Suriya et al., 2017). Meanwhile, in the Periyar river, studies have primarily focused on determining the physicochemical parameters of water/sediments, isolation of heavy metals and antibiotic resistant microbes (Lakshmi and Madhu, 2020, Prasanth and Mahesh, 2016, Salas et al., 2017). Further, there lies a void in ascertaining the factors responsible for framing the distinct microbial communities and indicators in these ecosystems.

In this backdrop, the present study aims to utilize metagenomics to explore differences between the microbial communities in the Himalayan and Peninsular river systems. Association of microbiomes with diverse environmental factors in these rivers was also figured out. Additionally, abundance of microbial pollution indicators (fecal/sewage and pathogens) was also examined to reveal the health risks associated with these major river systems.

Section snippets

Sampling area description, design, and collection

Areas around the major metropolitan city landscapes with high domestic and industrial pollution, namely Delhi and Kochi for Himalayan and Peninsular rivers respectively, were chosen for the study. Capturing the patterns of microbial diversity and pathogenic taxa in this gradient of anthropogenically influenced areas were assured by sampling both upstream and downstream of the industrial belts. Since following the entire river course is not feasible due to the rivers’ extensive length, we tried

Environmental parameters

Physicochemical parameters like pH, temperature, salinity, and different major/minor elements in the sediments were estimated from the eleven samples and summarized in Table S2. The pH values (7.06 ± 0.5) indicated neutral to alkaline nature of the studied samples. Himalayan samples were significantly more alkaline than Peninsular samples (p < 0.01). Salinity values ranged within 1.65 ± 2.7, with Peninsular samples being slightly more saline in nature. The temperature in Peninsular samples was

Discussion

The recent explosion of metagenomics studies based on next-generation sequencing has immensely enabled exploring microbial communities of unique ecosystems ranging from gut microflora to deep seafloors (De et al., 2020; Grossart et al., 2020). The tool is slowly gaining momentum with increasing number of applications like surveillance of microbiome quality changes with ecological disturbances or pollution (Alves et al., 2018; Chen et al., 2019). One such monitoring application currently being

Conclusions

Overall, our study indicates that microbiomes are shaped through the significant influence of intrinsic and extrinsic factors existing in the Himalayan and Peninsular riverine ecosystems. Besides, detection of various potentially pathogenic and F/S associated indicators reveals the impending health risks owing to sewage and domestic pollution of these water bodies. The study recommends the urgency to devise effective strategies for proper management of domestic sewage and industrial effluents

Credit author statement

Aparna Chakkamadathil Rajeev: Conceptualization, Methodology, Investigation, Writing – original draft, Writing - Review & Editing, Validation, Formal analysis, Visualization, Software Nishi Sahu: Conceptualization, Methodology, Investigation, Writing – original draft, Writing - Review & Editing, Validation, Formal analysis, Visualization Kumar Arvind: Software, Formal analysis Maushumi Deori: Resources Tony Grace: Resources, Validation, Writing - Review & Editing Suma Arun Dev: Visualization,

Funding

Financial assistance for this study was provided by UGC, JNU DST-PURSE, and JNU UPE-II. The funders had no role in the study design, data collection, interpretation, or the decision to submit the work for publication.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We appreciate the late Vijay Pal Yadav contributions to the design and initial execution of (Peninsular river project) this research project. We also thank Krishna Kumar (IFS), former deputy director of Periyar Tiger Reserve, and P. S. Easa, former director, Kerala Forest Research Institute, for their help during the sample collection in Periyar Lake. We would like to appreciate the wholehearted support from Bishi E. Balan for sample collection (Peninsular samples). We would like to appreciate

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