Microbial water quality is currently monitored in the EU and throughout much of the world by identifying and enumerating specific groups of ‘faecal indicator bacteria’ (FIB), such as faecal coliforms and intestinal enterococci.
However, although these FIB are shed by all warm-blooded mammals and indicate the presence of faecal contamination (and likely the presence of certain pathogens), they tend to be less reliable indicators of viral pathogens, such as norovirus or adenovirus. Moreover, their inability to distinguish human from non-human sources of pollution in surface waters and groundwaters hampers the task of (i) establishing the level of risk to public health; (ii) determining responsibility for remediation; and (iii) identifying and targeting the most effective mitigation measures. Consequently, such limitations have driven global efforts to develop tools to identify the ‘origin of faeces’ and has led to the emergence of the field of microbial source tracking (MST) during the last 25 years.
Microbial source tracking
Researchers from the Environment & Public Health Research and Enterprise Group at the University of Brighton (in collaboration with colleagues from Barcelona University) have been at the forefront of this burgeoning field, developing novel low-cost bacteriophage-based MST approaches, with which to tackle a range of pressing issues affecting our water resources. The method is based on the detection of bacteriophage (phage) that attack common groups of bacteria, such as Bacteroides spp. found in our guts. Whilst high numbers of these obligate anaerobic bacteria are shed in our faeces, they do not survive for long once out in the environment. Fortunately, the phage which infect them fare much better once outside of the human gut and are not only highly host-specific but can also survive the journey through wastewater treatment plants. This means they have the capacity to indicate the presence of contamination from inputs such as treated wastewater effluents, sewer overflows and leaking septic tanks. Researchers in our group have also identified groups of phages that are restricted to certain non-human pollution sources, such as cattle and pigs. Our longer-term goal is to develop a ‘toolbox’ of phage-based markers, which will allow us to rapidly identify inputs from human, agricultural and wildlife sources.
Protecting water resources and human health
Interestingly, these phage-based tools are not only helping improve our understanding of the origin of different pollution sources, but are also shedding light on the very nature of phage–host interactions, on the behaviour of enteric viral pathogens in the environment and through engineered treatment systems (for example, wastewater treatment plants). For example, working with the UK water industry (Thames, South East and Southern Water), the international NGO Médecins Sans Frontières (MSF) and numerous global research institutions we have successfully used phage to: (i) identify human contamination of river waters used for drinking water abstraction and recreation; (ii) elucidate human and non-human drivers of eutrophication (for example, harmful algal blooms) in drinking water reservoirs; (iii) assess the efficacy of emerging full-scale water reuse technologies used for irrigation and potential augmentation of potable water supplies; (iv) determine contamination sources impacting shellfisheries; (v) assess the efficacy of approaches for the containment and safe handling of human excreta in emergency settings (with MSF); (vi) understand the human-to-human environmental transmission of typhoid fever in urban slums in India (Bill & Melinda Gates Foundation); and (vii) understand cattle-to-human transmission of childhood diarrhoea in rural Kenya (Medical Research Council).
Wastewater reuse in South East London
Working with Thames Water, we monitored pathogen and phage removal through the Old Ford wastewater reuse system [Membrane Bio Reactor (MBR)] at the former Olympic Park in East London (used at the time for park irrigation). We also challenged the MBR under ‘worst-case scenario’ conditions by spiking high titres of known phage into the system. Our findings highlighted what changes to the treatment system would be needed in the future in order to ensure potable quality (with respect to microbiological parameters) and helped to satisfy an International Panel of Experts that MBR technologies have the potential to adequately protect human health and reduce environmental contamination.
Reservoir protection, South East England
Working with South East Water, we have been elucidating the contribution of human faecal pollution sources to eutrophication processes responsible for algal blooms (Cyanobacteria) at two of their reservoirs in South East England. The catchments draining into each reservoir were assessed in terms of point and diffuse pollution inputs and categorised in terms of nutrient loading (nitrates and phosphates). The findings revealed which tributaries (and pollution sources) are driving the nutrient loading and are helping to target mitigation and remediation measures where they are most needed. Consequently, this information can be used to better protect the health of consumers, water users and the environment.
Contamination and disease prevention
Finally, phage-based methods are also being used to understand high-risk contamination pathways in low-income and emergency settings in India, Haiti and sub-Saharan Africa. For instance, we have used phage to help determine the efficacy of chlorine and lime-based methods for the safe containment and handling of human excreta in cholera treatment centres, Ebola treatment centres and refugee camps. These approaches are ensuring the NGOs can protect patients, staff and the environment from contamination and onward waterborne disease transmission. Phage are also helping us to identify human faecal transmission routes and should ultimately help prevent the environmental transmission of Salmonella Typhi and Salmonella Paratyphi A in Indian megaslums (Kolkata). Whilst direct pathogen detection is possible, high cost and technological difficulties mean that routine environmental surveillance can be challenging and/or prohibitively expensive. However, human-specific phage can help highlight hotspots of human contamination within the environment and with targeted application can improve more expensive approaches including pathogen detection. This project is part of a wider Gates Foundation initiative to eliminate typhoid as a public health problem by 2035.
The modern ‘age of phage’
To summarise, we are fortunate to be living in an exciting ‘age of phage’, where rapid advancements in metagenomic, metabolomic and bioinformatic technologies are fuelling improvements in our understanding of phage behaviour, abundance, diversity and function. What we as microbiologists do with this wealth of information remains to be seen – but one thing that is already clear is that phage can be used as a force for good when it comes to protecting both environmental and public health. By enhancing our ability to effectively target and mitigate environmental contamination at source, they are helping us to reduce the burden of waterborne disease and prevent the further degradation of our limited water resources.
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