Streambed microbial communities in the transition zone between groundwater and a first-order stream as impacted by bidirectional water exchange
Graphical Abstract
Graphical Abstract
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Introduction
Up to 85% of the total stream length in a river system consists of lower-order streams, typically classified as first- and second-order streams (Horton, 1945; Peterson et al., 2001; Scheidegger, 1965). Lower-order streams act as the fountainhead of fluvial networks and have a substantial imprint on stream water chemistry (Peterson et al., 2001). However, their reactivity and elimination potential towards incoming pollutants, in particular from diffuse agricultural sources, are not well understood. Especially, the partitioning of this reactivity between instream processing and the streambed remains sparsely addressed. Higher-order streams are typically connected to extensive hyporheic and parafluvial flow paths, which move stream water through streambed and riparian sediments to subsequently return to the stream (Boano et al., 2014; Gomez-Velez et al., 2015; Krause et al., 2011; McClain et al., 2003). Water passage through hyporheic zones can significantly stimulate biogeochemical turnover of pollutants and nutrient elimination because of elongated transit times (compared to instream transit times) and increased biogeochemical and physical heterogeneity. In contrast, lower-order agricultural streams are often strongly modified, straightened, and typically of low streambed morphological complexity, thus minimizing the potential for hyporheic exchange. Therefore, such streams have often been considered to act predominantly as drainage systems, largely receiving water from the surrounding landscape (Kaandorp et al., 2018; Needelman et al., 2007; Yu et al., 2018). This currently limits the perspective of how hydrology and biogeochemistry can interact to control oxidative and reductive pollutant transformation in lower-order agricultural streams.
Nitrate loading, mainly stemming from agricultural fertilizer inputs and also nitrification of ammonia arising from livestock manure, is a particular concern for stream and groundwater quality (Peterson et al., 2001; Starry et al., 2005). Capacities for the assimilative removal of nitrate in the stream itself mostly involve algal or macrophyte growth (Gooseff et al., 2004; Smith et al., 2006). More importantly, nitrate can also be removed by stream sediment microbial communities through heterotrophic denitrification and/or dissimilatory nitrate reduction to ammonium (DNRA) (Kuypers et al., 2018; Mulholland et al., 2008; Storey et al., 2004; Tiedje, 1988). Nitrate reduction can also occur autotrophically, coupled to the oxidation of iron and sulfur species, hydrogen, or methane (Kuypers et al., 2018). However, as all of these processes require microoxic or anoxic conditions, the local hydraulic pattern becomes a decisive parameter of control (Seitzinger et al., 2002; Zarnetske et al., 2011). It is now recognized that lower-order streams not only receive water, but steadily interact with the surrounding groundwater along successive and seasonally variable gaining (groundwater exfiltration) or losing (stream water infiltration) reaches (Covino and McGlynn, 2007; Mallard et al., 2014; Zhang et al., 2021). This sequential exchange and replacement of water along the flow of a lower-order stream has been termed 'hydrologic turnover', which can substantially influence the biogeochemistry of the stream (Mallard et al., 2014). Depending on the local availability of electron donors such as organic carbon, reduced iron, and/or sulfur species in the sediment, reactive hot-spots for denitrification may thus be generated in the streambed especially in losing reaches (Trauth et al., 2018). In an agriculturally impacted first-order stream in southern Germany, we recently identified substantial and seasonally variable bidirectional exchange fluxes between the stream and surrounding groundwater, contributing significantly to nitrate reduction in water entering the near-stream anoxic aquifer (Jimenez-Fernandez et al., 2022). However, the interplay of such hydrological and biogeochemical processes in shaping sedimentary bacterial communities and their activities in nitrogen cycling has not yet been addressed.
Previous studies addressing the microbiology of rivers and streams report that sediment microbial communities are typically distinct to those found in surface water and the surrounding groundwater, and suggest a depth-dependent stratification (Danczak et al., 2016; Graham et al., 2017; Lin et al., 2012; Saup et al., 2019). Longitudinally, successions in microbial community structure have been investigated from headwaters to large rivers and even estuaries, and are taken to be controlled by local stream characteristics, landscape type, and anthropogenic impact (Battin et al., 2008; Crump et al., 2004; Hullar et al., 2006; Liao et al., 2019; Stegen et al., 2016; Winter et al., 2007). It is also assumed that local sediment community assembly is dominated by deterministic selection, particularly for higher-order streams (Danczak et al., 2016; Graham et al., 2017). In contrast, mechanisms of dispersal-based stochastic assembly indicate zones impacted by direct hydrologic transport, such as hydrologic mixing and interstitial flow (Graham et al., 2017; Graham and Stegen, 2017).
To date, studies on structural patterns of microbial communities in the sediment of agricultural impacted lower-order streams (i.e. first- and second-order streams) remain scarce, especially in a dedicated hydrologic perspective. Here, we address this research gap by dissecting sedimentary bacterial communities in the above-mentioned agricultural first-order stream via qPCR and PacBio full-length 16S rRNA gene amplicon sequencing. Long-read amplicon sequencing was chosen to provide more reliable phylogenetic resolution on possible taxon distribution patterns associated with local hydrology characteristics. We posit that typical hydrological and geochemical parameters alone are necessary, but not sufficient for understanding nitrate reduction mechanisms in such systems, and explicitly address the interplay of hydrologic and microbial process controls (Harvey et al., 2013; Mulholland et al., 2008). We hypothesize that (1) sediment microbial communities along successive net gaining and losing sections of the first-order stream are distinct and impacted by local hydrology, (2) the impact of hydrology on sediment microbial communities should be apparent in distinct assembly patterns between communities over longitudinal stream sections and over streambed sediment depths, and (3) local hydrologic turnover caused by simultaneous bidirectional water exchange impacts the distribution and the abundance of nitrate-reducing populations.
Section snippets
Site description
The Schönbrunnen stream (48.32°N latitude and 8.57°E longitude) is a first-order stream located in a predominantly agricultural area. It is a tributary of the second-order Käsbach stream, within the Ammer catchment in the west of the city of Tübingen, Germany (Fig. 1). Both hydrology and hydrochemistry of the site (Table 1) have been described elsewhere (Jimenez-Fernandez et al., 2022). The studied section of the stream has a length of approximately 550 m, a mean discharge of approximately 1 L s
Hydrology and hydrochemistry of the Schönbrunnen stream
Nitrate concentrations in Schönbrunnen stream water and the alluvial aquifer were repeatedly measured over several years, and a representative set of water chemistry data corresponding to our sampling season is shown in Fig. 2B. Nitrate was generally highest in the northwestern, most upstream section of the Schönbrunnen, with concentrations > 50 mg L−1, consistent with the intensive agricultural activities in this area. This was also reflected in the highest nitrate concentrations (≥ 60 mg L−1)
Discussion
In this study, we comprehensively interrogate the microbial community structure in the streambed of the Schönbrunnen, an agriculturally impacted first-order stream. We differentiate microbes in sections of the streambed where seasonal bidirectional gaining and losing fluxes of water are occurring. We propose that the demonstrated longitudinal and vertical heterogeneity of the streambed microbial communities and the distribution of distinct functional capacities were impacted by this specific
Conclusions
In this study, we show that bidirectional water exchange between an agricultural first-order stream and the surrounding alluvial aquifer is important not only for stream water chemistry, but also for sediment microbial populations and their presumed activities in attenuating agricultural solute inputs. By disentangling the stream into net gaining and losing sections, we show that sediment microbial community assembly was mostly dominated by deterministic heterogeneous assembly processes, except
CRediT authorship contribution statement
Zhe Wang: Investigation, Writing – original draft, Formal analysis, Conceptualization, Visualization. Oscar Jimenez-Fernandez: Investigation, Methodology, Formal analysis, Writing – review & editing. Karsten Osenbrück: Investigation, Validation, Writing – review & editing. Marc Schwientek: Investigation, Validation, Writing – review & editing. Michael Schloter: Resources, Validation, Writing – review & editing. Jan H. Fleckenstein: Conceptualization, Validation, Writing – review & editing.
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
This study was supported by collaborative research project 1253 CAMPOS (Project 2: Sub-Catchments), funded by the German Research Foundation (DFG, Grant agreement SFB 1253/1). We thank Research Unit for Comparative Microbiome Analyses at the Helmholtz Zentrum München for providing laboratory and computing resources, especially Susanne Kublik and Dr. Silvia Gschwendtner for technical support on PacBio Sequel sequencing. We additionally thank Gabriele Barthel for assistance during field sampling,
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