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Groundwater-surface water mixing shifts ecological assembly processes and stimulates organic carbon turnover.

Stegen JC, Fredrickson JK, Wilkins MJ, Konopka AE, Nelson WC, Arntzen EV, Chrisler WB, Chu RK, Danczak RE, Fansler SJ, Kennedy DW, Resch CT, Tfaily M - Nat Commun (2016)

Bottom Line: Environmental transitions often result in resource mixtures that overcome limitations to microbial metabolism, resulting in biogeochemical hotspots and moments.Riverine systems, where groundwater mixes with surface water (the hyporheic zone), are spatially complex and temporally dynamic, making development of predictive models challenging.Our results indicate that groundwater-surface water mixing in the hyporheic zone stimulates heterotrophic respiration, alters organic carbon composition, causes ecological processes to shift from stochastic to deterministic and is associated with elevated abundances of microbial taxa that may degrade a broad suite of organic compounds.

View Article: PubMed Central - PubMed

Affiliation: Pacific Northwest National Laboratory, 902 Battelle Boulevard, P.O. Box 999, Richland, Washington 99352, USA.

ABSTRACT
Environmental transitions often result in resource mixtures that overcome limitations to microbial metabolism, resulting in biogeochemical hotspots and moments. Riverine systems, where groundwater mixes with surface water (the hyporheic zone), are spatially complex and temporally dynamic, making development of predictive models challenging. Spatial and temporal variations in hyporheic zone microbial communities are a key, but understudied, component of riverine biogeochemical function. Here, to investigate the coupling among groundwater-surface water mixing, microbial communities and biogeochemistry, we apply ecological theory, aqueous biogeochemistry, DNA sequencing and ultra-high-resolution organic carbon profiling to field samples collected across times and locations representing a broad range of mixing conditions. Our results indicate that groundwater-surface water mixing in the hyporheic zone stimulates heterotrophic respiration, alters organic carbon composition, causes ecological processes to shift from stochastic to deterministic and is associated with elevated abundances of microbial taxa that may degrade a broad suite of organic compounds.

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Conceptual depiction of hypothesized dynamics in the hyporheic zone driven by changes in river stage.(a) At high stage, the hyporheic zone is inundated with river water (dark blue arrow). Unattached microbial communities in the river and hyporheic zone are governed by stochastic ecological processes whereby a broad range of microbial taxa are present (visualized as different cell shapes); purple and brown cells represent river-derived and groundwater-derived microbial taxa, respectively. Well-connected pore channels and active microbial communities limit the accumulation of labile organic carbon (visualized as saccharide molecules) in pore channels. (b) At low river stage, the hyporheic zone is dominated by groundwater discharge (green arrow) and unattached microbial communities are governed by stochastic ecological processes. Large interconnected pores drain—but smaller pores do not—following the decline in river stage. Extracellular enzymes (black and red) continue to degrade POC into labile organic carbon; however, owing to unsaturated conditions, highly tortuous paths with long diffusion times delay the transport of labile carbon to microbial cells. The result is accumulation of labile carbon within microsites and along tortuous paths. (c) A rise in river stage causes groundwater–surface water mixing that leads to deterministic ecological processes that select for microbial taxa with particular ecological traits (indicated by a single cell shape in the hyporheic zone). The re-saturation of sediments disperses accumulated labile carbon into large pores, thereby decreasing transport times to microbial cells and, in turn, stimulating heterotrophic respiration.
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f8: Conceptual depiction of hypothesized dynamics in the hyporheic zone driven by changes in river stage.(a) At high stage, the hyporheic zone is inundated with river water (dark blue arrow). Unattached microbial communities in the river and hyporheic zone are governed by stochastic ecological processes whereby a broad range of microbial taxa are present (visualized as different cell shapes); purple and brown cells represent river-derived and groundwater-derived microbial taxa, respectively. Well-connected pore channels and active microbial communities limit the accumulation of labile organic carbon (visualized as saccharide molecules) in pore channels. (b) At low river stage, the hyporheic zone is dominated by groundwater discharge (green arrow) and unattached microbial communities are governed by stochastic ecological processes. Large interconnected pores drain—but smaller pores do not—following the decline in river stage. Extracellular enzymes (black and red) continue to degrade POC into labile organic carbon; however, owing to unsaturated conditions, highly tortuous paths with long diffusion times delay the transport of labile carbon to microbial cells. The result is accumulation of labile carbon within microsites and along tortuous paths. (c) A rise in river stage causes groundwater–surface water mixing that leads to deterministic ecological processes that select for microbial taxa with particular ecological traits (indicated by a single cell shape in the hyporheic zone). The re-saturation of sediments disperses accumulated labile carbon into large pores, thereby decreasing transport times to microbial cells and, in turn, stimulating heterotrophic respiration.

Mentions: We have revealed a collection of field-scale patterns that are consistent with a strong impact of surface water intrusion on hyporheic zone microbiomes and biogeochemical function. There are numerous mechanisms underlying these coupled dynamics that will require additional investigation. To guide future efforts and connect our study to a broader range of systems, we collate the patterns observed here into a conceptual model (Fig. 8). It is important to note that the conceptual model developed below is speculative and represents a collection of hypotheses that emerge from our results; it is intended to be a point of departure for future work. The conceptual model is most relevant to systems that transition between saturated and unsaturated conditions, such as sections of rivers that are influenced by dam operations and/or tides. We frame the conceptual model around a key question: what is the source (or sources) of labile organic carbon that is transported by surface water and why is it not consumed before entering the hyporheic zone?


Groundwater-surface water mixing shifts ecological assembly processes and stimulates organic carbon turnover.

Stegen JC, Fredrickson JK, Wilkins MJ, Konopka AE, Nelson WC, Arntzen EV, Chrisler WB, Chu RK, Danczak RE, Fansler SJ, Kennedy DW, Resch CT, Tfaily M - Nat Commun (2016)

Conceptual depiction of hypothesized dynamics in the hyporheic zone driven by changes in river stage.(a) At high stage, the hyporheic zone is inundated with river water (dark blue arrow). Unattached microbial communities in the river and hyporheic zone are governed by stochastic ecological processes whereby a broad range of microbial taxa are present (visualized as different cell shapes); purple and brown cells represent river-derived and groundwater-derived microbial taxa, respectively. Well-connected pore channels and active microbial communities limit the accumulation of labile organic carbon (visualized as saccharide molecules) in pore channels. (b) At low river stage, the hyporheic zone is dominated by groundwater discharge (green arrow) and unattached microbial communities are governed by stochastic ecological processes. Large interconnected pores drain—but smaller pores do not—following the decline in river stage. Extracellular enzymes (black and red) continue to degrade POC into labile organic carbon; however, owing to unsaturated conditions, highly tortuous paths with long diffusion times delay the transport of labile carbon to microbial cells. The result is accumulation of labile carbon within microsites and along tortuous paths. (c) A rise in river stage causes groundwater–surface water mixing that leads to deterministic ecological processes that select for microbial taxa with particular ecological traits (indicated by a single cell shape in the hyporheic zone). The re-saturation of sediments disperses accumulated labile carbon into large pores, thereby decreasing transport times to microbial cells and, in turn, stimulating heterotrophic respiration.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4829693&req=5

f8: Conceptual depiction of hypothesized dynamics in the hyporheic zone driven by changes in river stage.(a) At high stage, the hyporheic zone is inundated with river water (dark blue arrow). Unattached microbial communities in the river and hyporheic zone are governed by stochastic ecological processes whereby a broad range of microbial taxa are present (visualized as different cell shapes); purple and brown cells represent river-derived and groundwater-derived microbial taxa, respectively. Well-connected pore channels and active microbial communities limit the accumulation of labile organic carbon (visualized as saccharide molecules) in pore channels. (b) At low river stage, the hyporheic zone is dominated by groundwater discharge (green arrow) and unattached microbial communities are governed by stochastic ecological processes. Large interconnected pores drain—but smaller pores do not—following the decline in river stage. Extracellular enzymes (black and red) continue to degrade POC into labile organic carbon; however, owing to unsaturated conditions, highly tortuous paths with long diffusion times delay the transport of labile carbon to microbial cells. The result is accumulation of labile carbon within microsites and along tortuous paths. (c) A rise in river stage causes groundwater–surface water mixing that leads to deterministic ecological processes that select for microbial taxa with particular ecological traits (indicated by a single cell shape in the hyporheic zone). The re-saturation of sediments disperses accumulated labile carbon into large pores, thereby decreasing transport times to microbial cells and, in turn, stimulating heterotrophic respiration.
Mentions: We have revealed a collection of field-scale patterns that are consistent with a strong impact of surface water intrusion on hyporheic zone microbiomes and biogeochemical function. There are numerous mechanisms underlying these coupled dynamics that will require additional investigation. To guide future efforts and connect our study to a broader range of systems, we collate the patterns observed here into a conceptual model (Fig. 8). It is important to note that the conceptual model developed below is speculative and represents a collection of hypotheses that emerge from our results; it is intended to be a point of departure for future work. The conceptual model is most relevant to systems that transition between saturated and unsaturated conditions, such as sections of rivers that are influenced by dam operations and/or tides. We frame the conceptual model around a key question: what is the source (or sources) of labile organic carbon that is transported by surface water and why is it not consumed before entering the hyporheic zone?

Bottom Line: Environmental transitions often result in resource mixtures that overcome limitations to microbial metabolism, resulting in biogeochemical hotspots and moments.Riverine systems, where groundwater mixes with surface water (the hyporheic zone), are spatially complex and temporally dynamic, making development of predictive models challenging.Our results indicate that groundwater-surface water mixing in the hyporheic zone stimulates heterotrophic respiration, alters organic carbon composition, causes ecological processes to shift from stochastic to deterministic and is associated with elevated abundances of microbial taxa that may degrade a broad suite of organic compounds.

View Article: PubMed Central - PubMed

Affiliation: Pacific Northwest National Laboratory, 902 Battelle Boulevard, P.O. Box 999, Richland, Washington 99352, USA.

ABSTRACT
Environmental transitions often result in resource mixtures that overcome limitations to microbial metabolism, resulting in biogeochemical hotspots and moments. Riverine systems, where groundwater mixes with surface water (the hyporheic zone), are spatially complex and temporally dynamic, making development of predictive models challenging. Spatial and temporal variations in hyporheic zone microbial communities are a key, but understudied, component of riverine biogeochemical function. Here, to investigate the coupling among groundwater-surface water mixing, microbial communities and biogeochemistry, we apply ecological theory, aqueous biogeochemistry, DNA sequencing and ultra-high-resolution organic carbon profiling to field samples collected across times and locations representing a broad range of mixing conditions. Our results indicate that groundwater-surface water mixing in the hyporheic zone stimulates heterotrophic respiration, alters organic carbon composition, causes ecological processes to shift from stochastic to deterministic and is associated with elevated abundances of microbial taxa that may degrade a broad suite of organic compounds.

Show MeSH
Related in: MedlinePlus