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Title: Colonization Habitat Controls Biomass, Composition, and Metabolic Activity of Attached Microbial Communities in the Columbia River Hyporheic Corridor

Abstract

Hydrologic exchange plays a critical role in biogeochemical cycling within the hyporheic zone (the interface between river water and groundwater) of riverine ecosystems. Such exchange may set limits on the rates of microbial metabolism and impose deterministic selection on microbial communities that adapt to dynamically changing dissolved organic carbon (DOC) sources. This study examined the response of attached microbial communities (in situcolonized sand packs) from groundwater, hyporheic, and riverbed habitats within the Columbia River hyporheic corridor to “cross-feeding” with either groundwater, river water, or DOC-free artificial fluids. Our working hypothesis was that deterministic selection duringin situcolonization would dictate the response to cross-feeding, with communities displaying maximal biomass and respiration when supplied with their native fluid source. In contrast to expectations, the major observation was that the riverbed colonized sand had much higher biomass and respiratory activity, as well as a distinct community structure, compared with those of the hyporheic and groundwater colonized sands. 16S rRNA gene amplicon sequencing revealed a much higher proportion of certain heterotrophic taxa as well as significant numbers of eukaryotic algal chloroplasts in the riverbed colonized sand. Significant quantities of DOC were released from riverbed sediment and colonized sand, and separate experiments showed that the releasedmore » DOC stimulated respiration in the groundwater and piezometer colonized sand. These results suggest that the accumulation and degradation of labile particulate organic carbon (POC) within the riverbed are likely to release DOC, which may enter the hyporheic corridor during hydrologic exchange, thereby stimulating microbial activity and imposing deterministic selective pressure on the microbial community composition. IMPORTANCEThe influence of river water-groundwater mixing on hyporheic zone microbial community structure and function is an important but poorly understood component of riverine biogeochemistry. This study employed an experimental approach to gain insight into how such mixing might be expected to influence the biomass, respiration, and composition of hyporheic zone microbial communities. Colonized sands from three different habitats (groundwater, river water, and hyporheic) were “cross-fed” with either groundwater, river water, or DOC-free artificial fluids. We expected that the colonization history would dictate the response to cross-feeding, with communities displaying maximal biomass and respiration when supplied with their native fluid source. By contrast, the major observation was that the riverbed communities had much higher biomass and respiration, as well as a distinct community structure compared with those of the hyporheic and groundwater colonized sands. These results highlight the importance of riverbed microbial metabolism in organic carbon processing in hyporheic corridors.« less

Authors:
; ; ; ; ORCiD logo; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1415091
Report Number(s):
PNNL-SA-129379
Journal ID: ISSN 0099-2240; 49160; KP1702030
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Applied and Environmental Microbiology; Journal Volume: 83; Journal Issue: 16
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; Environmental Molecular Sciences Laboratory

Citation Formats

Stern, Noah, Ginder-Vogel, Matthew, Stegen, James C., Arntzen, Evan, Kennedy, David W., Larget, Bret R., Roden, Eric E., and Kostka, Joel E. Colonization Habitat Controls Biomass, Composition, and Metabolic Activity of Attached Microbial Communities in the Columbia River Hyporheic Corridor. United States: N. p., 2017. Web. doi:10.1128/AEM.00260-17.
Stern, Noah, Ginder-Vogel, Matthew, Stegen, James C., Arntzen, Evan, Kennedy, David W., Larget, Bret R., Roden, Eric E., & Kostka, Joel E. Colonization Habitat Controls Biomass, Composition, and Metabolic Activity of Attached Microbial Communities in the Columbia River Hyporheic Corridor. United States. doi:10.1128/AEM.00260-17.
Stern, Noah, Ginder-Vogel, Matthew, Stegen, James C., Arntzen, Evan, Kennedy, David W., Larget, Bret R., Roden, Eric E., and Kostka, Joel E. Fri . "Colonization Habitat Controls Biomass, Composition, and Metabolic Activity of Attached Microbial Communities in the Columbia River Hyporheic Corridor". United States. doi:10.1128/AEM.00260-17.
@article{osti_1415091,
title = {Colonization Habitat Controls Biomass, Composition, and Metabolic Activity of Attached Microbial Communities in the Columbia River Hyporheic Corridor},
author = {Stern, Noah and Ginder-Vogel, Matthew and Stegen, James C. and Arntzen, Evan and Kennedy, David W. and Larget, Bret R. and Roden, Eric E. and Kostka, Joel E.},
abstractNote = {Hydrologic exchange plays a critical role in biogeochemical cycling within the hyporheic zone (the interface between river water and groundwater) of riverine ecosystems. Such exchange may set limits on the rates of microbial metabolism and impose deterministic selection on microbial communities that adapt to dynamically changing dissolved organic carbon (DOC) sources. This study examined the response of attached microbial communities (in situcolonized sand packs) from groundwater, hyporheic, and riverbed habitats within the Columbia River hyporheic corridor to “cross-feeding” with either groundwater, river water, or DOC-free artificial fluids. Our working hypothesis was that deterministic selection duringin situcolonization would dictate the response to cross-feeding, with communities displaying maximal biomass and respiration when supplied with their native fluid source. In contrast to expectations, the major observation was that the riverbed colonized sand had much higher biomass and respiratory activity, as well as a distinct community structure, compared with those of the hyporheic and groundwater colonized sands. 16S rRNA gene amplicon sequencing revealed a much higher proportion of certain heterotrophic taxa as well as significant numbers of eukaryotic algal chloroplasts in the riverbed colonized sand. Significant quantities of DOC were released from riverbed sediment and colonized sand, and separate experiments showed that the released DOC stimulated respiration in the groundwater and piezometer colonized sand. These results suggest that the accumulation and degradation of labile particulate organic carbon (POC) within the riverbed are likely to release DOC, which may enter the hyporheic corridor during hydrologic exchange, thereby stimulating microbial activity and imposing deterministic selective pressure on the microbial community composition. IMPORTANCEThe influence of river water-groundwater mixing on hyporheic zone microbial community structure and function is an important but poorly understood component of riverine biogeochemistry. This study employed an experimental approach to gain insight into how such mixing might be expected to influence the biomass, respiration, and composition of hyporheic zone microbial communities. Colonized sands from three different habitats (groundwater, river water, and hyporheic) were “cross-fed” with either groundwater, river water, or DOC-free artificial fluids. We expected that the colonization history would dictate the response to cross-feeding, with communities displaying maximal biomass and respiration when supplied with their native fluid source. By contrast, the major observation was that the riverbed communities had much higher biomass and respiration, as well as a distinct community structure compared with those of the hyporheic and groundwater colonized sands. These results highlight the importance of riverbed microbial metabolism in organic carbon processing in hyporheic corridors.},
doi = {10.1128/AEM.00260-17},
journal = {Applied and Environmental Microbiology},
number = 16,
volume = 83,
place = {United States},
year = {Fri Jun 09 00:00:00 EDT 2017},
month = {Fri Jun 09 00:00:00 EDT 2017}
}
  • The hyporheic corridor (HC) is a critical component of riverine ecosystems that encompasses the river-11 groundwater continuum. The mixing of groundwater (GW) with river water (RW) in the HC can 12 stimulate biogeochemical activity, and here we (i) propose a novel thermodynamic mechanism 13 underlying this phenomenon, and (ii) reveal broader impacts on dissolved organic carbon (DOC) 14 biogeochemistry and microbial ecology. We show that thermodynamically-favorable DOC 15 accumulates in GW despite decreases in DOC concentration along subsurface flow paths, and that RW 16 contains less thermodynamically-favorable DOC, but at higher concentrations. This indicates that DOC 17 in GW ismore » protected from microbial oxidation by low total energy contained within the DOC pool, while 18 RW DOC is protected by lower thermodynamic favorability of carbon species. We propose that GW-19 RW mixing overcomes these protection mechanisms and stimulates respiration. Mixing models 20 coupled with time-lapse electrical resistance tomography revealed that stimulated respiration leads 21 to tipping points in spatiotemporal dynamics of DOC across the HC. Further, shifts in DOC speciation 22 and biochemical pathways were associated with shifts in microbiome composition, highlighting 23 feedbacks among hydrology, DOC biochemistry, and microbial ecology. These results reveal that 24 previously unrecognized thermodynamic-based mechanisms regulated by GW-RW mixing can strongly 25 influence biogeochemical and microbial dynamics in riverine ecosystems.« less
  • Potential increases in rhizodeposition under elevated CO{sub 2} has been hypothesized to stimulate microbial activity and, therefore, alter plant nitrogen availability. We investigated nitrogen relations of a nutrient poor calcareous grassland. Plant communities with 5, 12 or 31 of the species locally present were established in field plots and exposed to ambient (356{mu}l l{sup -1}) or elevated (600{mu}l l{sup -1}) atmospheric CO{sub 2} using open-top chambers. After 5 months of CO{sub 2} exposure, soil microbial biomass, microbial activity, plant above- and belowground biomass and nitrogen contents were measured. No significant effect of elevated CO{sub 2} or plant species number onmore » soil microbial biomass or activity was observed. Elevated CO{sub 2} led to significant increases in aboveground plant biomass in the 31 spp. community only. Under elevated CO{sub 2}, net ecosystem CO{sub 2} gas exchange and fine root biomass increased in all communities. Whole plot plant nitrogen uptake did not change, but significant increases in C:N ratios of N rich forbs were found. We conclude that, although rhizodeposition appears to have increased under elevated CO{sub 2}, neither microbial biomass nor activity changed significantly. Finally, the increased amount of fine roots observed under elevated CO{sub 2} led to intensified root exploration of soil, but did not result in increased total plant nitrogen uptake.« less
  • Aquifer microbes in the 300 Area of the Hanford Site in southeastern Washington State, USA are periodically exposed to U(VI) concentrations that can range up to 10 μM in small sediment fractures. Assays of 35 H-leucine incorporation indicated that both sediment-associated and planktonic microbes were metabolically active, and that organic C was growth-limiting in the sediments. Although bacteria suspended in native groundwater retained high activity when exposed to 100 μM U(VI), they were inhibited by U(VI) < 1 μM in synthetic groundwater that lacked added bicarbonate. Chemical speciation modeling suggested that positively-charged species and particularly (UO2)3(OH)5+ rose in concentration asmore » more U(VI) was added to synthetic groundwater, but that carbonate complexes dominated U(VI) speciation in natural groundwater. U toxicity was relieved when increasing amounts of bicarbonate were added to synthetic groundwater containing 4.5 μM U(VI). Pertechnetate, an oxyanion that is another contaminant of concern at the Hanford Site, was not toxic to groundwater microbes at concentrations up to 125 μM.« less
  • Fall chinook salmon (Oncorhynchus tshawytscha) spawned predominantly in areas of the Hanford Reach of the Columbia River where hyporheic water discharged into the river channel. This upwelling water had a dissolved solids content (i.e., specific conductance) indicative of river water and was presumed to have entered highly permeable riverbed substrate at locations upstream of the spawning areas. Hyporheic discharge zones composed of undiluted ground water or areas with little or no upwelling were not used by spawning salmon. Rates of upwelling into spawning areas averaged 1,200 L?m-2?day-1 (95% C.I.= 784 to 1,665 L?m-2?day-1) as compared to approximately 500 L?m-2?day-1 (95%more » C.I.= 303 to 1,159 L?m-2?day-1) in non-spawning areas. Dissolved oxygen content of the hyporheic discharge near salmon spawning areas was about 9 mg?L-1 (+ 0.4 mg?L-1) whereas in non-spawning areas dissolved oxygen values were 7 mg?L-1 (+ 0.9 mg?L-1) or lower. In both cases dissolved oxygen of the river water was higher (11.3+ 0.3 mg?L-1). Physical and chemical gradients between the hyporheic zone and the river may provide cues for adult salmon to locate suitable spawning areas. This information will help fisheries managers to describe the suitability of salmon spawning habitat in large rivers.« less