Genomics and eDNA provide a holistic understanding of microbial communities and zoonoses in Aotearoa's waters : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Ecology at Massey University, Palmerston North, New Zealand
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2024-03-18
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Massey University
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Abstract
In Aotearoa, water quality and freshwater ecosystem health is declining. Much of that decline has been blamed on livestock farming and is quantified by using invertebrate communities or Escherichia coli levels. However, the wider microbial community, particularly archaea and eukaryotes, have been overlooked in the current ecosystem health measures. Some of the more well-known impacts of microorganisms on waterways are sporadically measured (e.g., algae blooms, drinking water contamination by faeces, and shellfish toxins) but the drivers of their community structure, both individually and as a whole, in Aotearoa is poorly understood. This thesis is a start at rectifying this knowledge gap.
The studies in this thesis were approached with a One Health perspective and provide a quantitative, holistic analysis of microbial communities by investigating three significant challenges facing Aotearoa’s freshwater ecosystems. Those challenges - the spread of waterborne disease, eutrophication, and microbial biogeochemical cycling - were investigated using microbiological cultures and environmental DNA, analysed with metagenomic and other molecular methods.
I was able to determine that targeted testing for genetic loci associated with antimicrobial resistance and Shiga toxin-producing E. coli virulence was a useful in monitoring three Canterbury waterways for human health. Furthermore, enteropathogenic human and bovine strains of E. coli appeared unresponsive to in-stream nitrate-nitrogen concentrations of 0, 1, and 3 mg/L and native in-stream biota in microcosms. However, environmentally sourced E.coli imported as part of the in-stream biota survived longer in NO3-N concentrations of 1 and 3 mg /L than at 0 mg/L.
Microorganism groups (e.g., archaea, bacteria, and microbial eukaryotes) responded to different environmental, spatio-temporal, and physico-chemical drivers depending on taxonomic level. As a group, lotic pressures and dispersal outweighed other drivers in community structuring. Archaeal communities were highly correlated with Austral season and the most abundant functional groups reflected a likely response to common agricultural pollutants found the Waiotahe catchment and in many rural rivers across Aotearoa (e.g., nitrogen pollution and livestock waste/effluents). The drivers commonly associated with bacterial survival (e.g., conductivity and temperature) were less important than dispersal and lotic pressures, particularly at lower taxonomic levels. Cultured E. coli concentrations from sediment and/or the water column were poorly indicators of Campylobacter, Enterobacter, and Enterococcus relative abundances. Additionally, neither Enterobacter nor Enterococcus relative abundances were correlated with E. coli/E. cloacae group concentrations or Campylobacter relative abundances.
These findings have important implications for water quality monitoring and recreational human health risk assessments in Aotearoa. Currently, microbiological water testing is limited to bathing season (i.e., late spring to early autumn) and to culturing either Enterococcus in saline/brackish water or E. coli in freshwater. Effective water quality monitoring must include both water and benthic substrates to accurately portray the entire riverscape. Genetic loci associated with zoonotic human pathogens are present in some of Aotearoa’s waterways and they are likely a result of catchment land use, livestock farming, and effluent contamination. Additionally, genetic loci can be detected with collection methods similar to those employed for current water quality monitoring using Escherichia coli and some molecular methods are more specific (i.e., not proxies).
Metagenomic methods allowed for the discernment of microbial communities and core biomes from genetic information extracted from environmental samples. Microbial communities were affected by many different in-stream conditions; however, dispersal and the pressures associated with lotic systems proved to be more important than adjacent land use, precipitation levels, or season. In contrast, archaeal communities were better explained by season.
It is clear that water monitoring in Aotearoa needs an overhaul and to incorporate new technology in a thoughtful and ecologically informed manner. A review of the current methods and new technologies should be undertaken by a multi-disciplinary group of experts in the fields of microbiology, epidemiology, and freshwater and microbial ecology. Community buy in and the inclusion of Māori values and indigenous rights should be at the forefront of any proposed changes to freshwater restoration and conservation.
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Water, Microbiology, Microbial ecology, Pathogenic microorganisms, New Zealand, Microbial genomics, Zoonoses, biogeochemical cycling, eDNA, estuaries, freshwater, genomics, microbial communities, rivers, waterborne disease, water quality