Streamwater Microbial Communities as Hydrologic Observation: Insights Gained from Investigation of a Novel Dataset

Interactions and feedbacks among climate change effects and continued human impacts will exacerbate impacts to water resources in complex ways. An urgent imperative of the hydrologic community is to understand the response of hydrologic systems to these perturbations, thus contributing to long-term sustainability of water resources in an uncertain future. Critical to anticipating and mitigating changes to water resources is a thorough characterization of hydrologic processes across a variety of systems and spatiotemporal scales. However, major gaps in our understanding persist, particularly regarding the movement of water through the catchment and streamflow generation, despite decades of research supported by large amounts of highly complex hydrological observation data. We suggest that a new type of information-rich data, which can be easily collected and analyzed, might be the key to new insights that propel the field toward a deeper, more fundamental understanding of hydrologic processes. Genetic material (i.e., DNA) is a naturally-occurring, high-dimensional digitally-encoded dataset, and DNA analysis has become much cheaper and more widely available in recent years. Microbial communities, characterized taxonomically by sequencing the 16S rRNA gene in DNA, are highly diverse and respond dynamically to environmental conditions. Here, we investigate the streamwater microbial community as a novel hydrologic dataset. We collected DNA samples over three years, from 2017-2020, from more than 60 streams across the Willamette, Deschutes, and John Day watersheds, three large and characteristically divergent watersheds in Oregon, USA. We found that differences in microbial community composition among streams, particularly in headwater streams, was statistically related to differences in geomorphic and climatic characteristics of the drainage catchment. We furthermore found through an information-theoretic approach, that specific summer community constituents (i.e., microbial taxa) were related to stream discharge metrics at multiple temporal and flow scales. We also observed that streamwater microbial diversity exhibited a rich and dynamic response to event hydrograph dynamics on the Marys River in the Willamette Valley of Oregon. In that analysis, we furthermore classified microbial taxa (and broader phylogenetic groups) according to whether they are mobilized or diluted with streamflow, potentially contributing new insights regarding the sources of streamflow, as well as a new way of characterizing taxa in microbial ecology studies. Results of this research support further investigation of the hydrologic information encoded within microbial communities, as well as ways in which the field might best extract and apply this new information to further our understanding of hydrologic systems and contribute fresh insight to unsolved questions in hydrology

The streamwater microbiome encodes hydrologic data across scales

Many fundamental questions in hydrology remain unanswered due to the limited information that can be extracted from existing data sources. Microbial communities constitute a novel type of environmental data, as they are comprised of many thousands of taxonomically and functionally diverse groups known to respond to both biotic and abiotic environmental factors. As such, these microscale communities reflect a range of macroscale conditions and characteristics, some of which also drive hydrologic regimes. Here, we assess the extent to which streamwater microbial communities (as characterized by 16S gene amplicon sequence abundance) encode information about catchment hydrology across scales. We analyzed 64 summer streamwater DNA samples collected from subcatchments within the Willamette, Deschutes, and John Day river basins in Oregon, USA, which range 0.03–29,000 km2 in area and 343–2334 mm/year of precipitation. We applied information theory to quantify the breadth and depth of information about common hydrologic metrics encoded within microbial taxa. Of the 256 microbial taxa that spanned all three watersheds, we found 9.6 % (24.5/256) of taxa, on average, shared information with a given hydrologic metric, with a median 15.6 % (range = 12.4–49.2 %) reduction in uncertainty of that metric based on knowledge of the microbial biogeography. All of the hydrologic metrics we assessed, including daily discharge at different time lags, mean monthly discharge, and seasonal high and low flow durations were encoded within the microbial community. Summer microbial taxa shared the most information with winter mean flows. Our study demonstrates quantifiable relationships between streamwater microbial taxa and hydrologic metrics at different scales, likely resulting from the integration of multiple overlapping drivers of each. Streamwater microbial communities are rich sources of information that may contribute fresh insight to unresolved hydrologic questions

River Microbiome Composition Reflects Macroscale Climatic and Geomorphic Differences in Headwater Streams

Maintaining the quality and quantity of water resources in light of complex changes in climate, human land use, and ecosystem composition requires detailed understanding of ecohydrologic function within catchments, yet monitoring relevant upstream characteristics can be challenging. In this study, we investigate how variability in riverine microbial communities can be used to monitor the climate, geomorphology, land-cover, and human development of watersheds. We collected streamwater DNA fragments and used 16S rRNA sequencing to profile microbiomes from headwaters to outlets of the Willamette and Deschutes basins, two large watersheds prototypical of the U.S. Pacific Northwest region. In the temperate, north-south oriented Willamette basin, microbial community composition correlated most strongly with geomorphic characteristics (mean Mantel test statistic r = 0.19). Percentage of forest and shrublands (r = 0.34) and latitude (r = 0.41) were among the strongest correlates with microbial community composition. In the arid Deschutes basin, however, climatic characteristics were the most strongly correlated to microbial community composition (e.g., r = 0.11). In headwater sub-catchments of both watersheds, microbial community assemblages correlated with catchment-scale climate, geomorphology, and land-cover (r = 0.46, 0.38, and 0.28, respectively), but these relationships were weaker downstream. Development-related characteristics were not correlated with microbial community composition in either watershed or in small or large sub-catchments. Our results build on previous work relating streamwater microbiomes to hydrologic regime and demonstrate that microbial DNA in headwater streams additionally reflects the structural configuration of landscapes as well as other natural and anthropogenic processes upstream. Our results offer an encouraging indication that streamwater microbiomes not only carry information about microbial ecology, but also can be useful tools for monitoring multiple upstream watershed characteristics

Shifts in Streamwater Microbial Diversity Track Storm Hydrograph Dynamics

A thorough understanding of watershed response to precipitation events is critical as our climate shifts to produce increasingly extreme precipitation and thus hydrologic events. Hydrogeochemical tools, such as stable isotope analysis, are a common approach for tracking precipitation and identifying the source of surface water in catchments, however they sometimes lack the dimensionality necessary to capture the multitude of complex processes involved in streamflow generation and water storage. In contrast, aquatic microbial communities in streams comprise thousands of taxa, originating from a variety of sources, including groundwater, sediment, stable upstream communities, and the upslope terrestrial environment. In this study, we explore the dynamics of the streamwater microbial community response to a precipitation event on the Marys River in Oregon, USA, where tracing streamwater sources with stable isotopes is confounded by the underlying geology. We collected daily DNA samples from the Marys River before, during, and after a large, isolated precipitation event. Stable water isotopes (δ18O and δ2H) were also analyzed. Though isotopes signatures exhibited relatively little variation, prior work in the catchment suggests that distinct pre-event, early-event, and late-event water sources are visible. DNA samples were translated into the relative abundance of different distinct taxa (~1000 in total) using 16S amplicon sequencing. Cluster analysis of the microbial composition similarly reveals coherent pre-event, early-event, and late-event microbial communities. Shifts in microbial diversity reflect changes in discharge over the course of the storm, and abundance-discharge relationships (analogous to a concentration-discharge geochemical analysis) reveal that some taxa are mobilized and others diluted over the course of the event. This study provides an approach for integrating information from DNA suspended in the water column into an investigation of a hydrologic response that incorporates tools from both hydrology and microbiology and demonstrates that microbial DNA is useful not only as an indicator of biodiversity but also as an innovative hydrologic tracer

Microbial Communities Reveal Sources of Streamflow in Response to Early-Season Storm Event

Persistent gaps in our understanding of watershed processes, including streamflow generation, attest to the limitations of current hydrologic tools and the urgent need to explore new approaches. Common hydrogeochemical tracing tools, such as stable isotope analysis, offer incomplete information, in part because the many complex processes involved in streamflow generation and water storage are integrated into a one- or two-dimensional datapoint. In contrast, aquatic microbial communities in streams are composed of thousands of unique taxa, originating from a variety of sources, including groundwater, sediment, stable upstream communities, and the upslope terrestrial environment. In this study, we explore the dynamics of the streamwater microbial community response to a precipitation event on the Marys River in Oregon, USA. We collected daily samples for DNA and stable water isotopes (δ18O and δ2H) from the Marys River before, during, and after a large, isolated precipitation event. Although variation in isotope ratios suggested distinct pre-event, early-event, and late-event water sources, microbial communities were much more sensitive and responded more dynamically to the stream event response. Microbial diversity metrics closely tracked streamflow volume, and cluster analysis of microbial community composition revealed coherent pre-event, early-event, and late-event communities. Furthermore, abundance of distinct taxonomies of microbes were diluted with increasing streamflow volume, including groups commonly associated with freshwater. In contrast, groups mobilized with increasing streamflow included taxa that are associated with terrestrial environments, suggesting a growing contribution of water from the hillslope. Thus, whereas traditional geochemical tracers are useful for inferring the age of water in the stream channel, microbial communities provide additional information on the sources and pathways of water to the stream channel as a result of the vast diversity of microbes and their biogeochemical interactions with the environment. This study illustrates an approach for integrating information from DNA suspended in the water column into an investigation of a hydrologic response that incorporates tools from both hydrology and microbiology and contributes to growing evidence that microbial DNA is useful not only as an indicator of biodiversity but also as an innovative hydrologic tracer