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Title: Multi 'omics comparison reveals metabolome biochemistry, not microbiome composition or gene expression, corresponds to elevated biogeochemical function in the hyporheic zone

Abstract

Biogeochemical hotspots are pervasive at terrestrial-aquatic interfaces, particularly within groundwater-surface water mixing zones (hyporheic zones), and they are critical to understanding spatiotemporal variation in biogeochemical cycling. Here, we use multi ‘omic comparisons of hotspots to low-activity sediments to gain mechanistic insight into hyporheic zone organic matter processing. We hypothesized that microbiome structure and function, as described by metagenomics and metaproteomics, would distinguish hotspots from low-activity sediments through a shift towards carbohydrate-utilizing metabolic pathways and elucidate discrete mechanisms governing organic matter processing in each location. We also expected these differences to be reflected in the metabolome, whereby hotspot carbon (C) pools and metabolite transformations therein would be enriched in sugar-associated compounds. In contrast to expectations, we found pronounced phenotypic plasticity in the hyporheic zone microbiome that was denoted by similar microbiome structure, functional potential, and expression across sediments with dissimilar metabolic rates. Instead, diverse nitrogenous metabolites and biochemical transformations characterized hotspots. Metabolomes also corresponded more strongly to aerobic metabolism than bulk C content only (explaining 67% vs. 42% of variation), and bulk C did not improve statistical models based on metabolome composition alone. These results point to organic nitrogen as a significant regulatory factor influencing hyporheic zone organic matter processing. Basedmore » on our findings, we propose incorporating knowledge of metabolic pathways associated with different chemical fractions of C pools into ecosystem models will enhance prediction accuracy.« less

Authors:
ORCiD logo; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1503534
Report Number(s):
PNNL-SA-133671
Journal ID: ISSN 0048-9697
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Science of the Total Environment
Additional Journal Information:
Journal Volume: 642; Journal Issue: C; Journal ID: ISSN 0048-9697
Publisher:
Elsevier
Country of Publication:
United States
Language:
English

Citation Formats

Graham, Emily B., Crump, Alex R., Kennedy, David W., Arntzen, Evan, Fansler, Sarah, Purvine, Samuel O., Nicora, Carrie D., Nelson, William, Tfaily, Malak M., and Stegen, James C. Multi 'omics comparison reveals metabolome biochemistry, not microbiome composition or gene expression, corresponds to elevated biogeochemical function in the hyporheic zone. United States: N. p., 2018. Web. doi:10.1016/j.scitotenv.2018.05.256.
Graham, Emily B., Crump, Alex R., Kennedy, David W., Arntzen, Evan, Fansler, Sarah, Purvine, Samuel O., Nicora, Carrie D., Nelson, William, Tfaily, Malak M., & Stegen, James C. Multi 'omics comparison reveals metabolome biochemistry, not microbiome composition or gene expression, corresponds to elevated biogeochemical function in the hyporheic zone. United States. doi:10.1016/j.scitotenv.2018.05.256.
Graham, Emily B., Crump, Alex R., Kennedy, David W., Arntzen, Evan, Fansler, Sarah, Purvine, Samuel O., Nicora, Carrie D., Nelson, William, Tfaily, Malak M., and Stegen, James C. Thu . "Multi 'omics comparison reveals metabolome biochemistry, not microbiome composition or gene expression, corresponds to elevated biogeochemical function in the hyporheic zone". United States. doi:10.1016/j.scitotenv.2018.05.256.
@article{osti_1503534,
title = {Multi 'omics comparison reveals metabolome biochemistry, not microbiome composition or gene expression, corresponds to elevated biogeochemical function in the hyporheic zone},
author = {Graham, Emily B. and Crump, Alex R. and Kennedy, David W. and Arntzen, Evan and Fansler, Sarah and Purvine, Samuel O. and Nicora, Carrie D. and Nelson, William and Tfaily, Malak M. and Stegen, James C.},
abstractNote = {Biogeochemical hotspots are pervasive at terrestrial-aquatic interfaces, particularly within groundwater-surface water mixing zones (hyporheic zones), and they are critical to understanding spatiotemporal variation in biogeochemical cycling. Here, we use multi ‘omic comparisons of hotspots to low-activity sediments to gain mechanistic insight into hyporheic zone organic matter processing. We hypothesized that microbiome structure and function, as described by metagenomics and metaproteomics, would distinguish hotspots from low-activity sediments through a shift towards carbohydrate-utilizing metabolic pathways and elucidate discrete mechanisms governing organic matter processing in each location. We also expected these differences to be reflected in the metabolome, whereby hotspot carbon (C) pools and metabolite transformations therein would be enriched in sugar-associated compounds. In contrast to expectations, we found pronounced phenotypic plasticity in the hyporheic zone microbiome that was denoted by similar microbiome structure, functional potential, and expression across sediments with dissimilar metabolic rates. Instead, diverse nitrogenous metabolites and biochemical transformations characterized hotspots. Metabolomes also corresponded more strongly to aerobic metabolism than bulk C content only (explaining 67% vs. 42% of variation), and bulk C did not improve statistical models based on metabolome composition alone. These results point to organic nitrogen as a significant regulatory factor influencing hyporheic zone organic matter processing. Based on our findings, we propose incorporating knowledge of metabolic pathways associated with different chemical fractions of C pools into ecosystem models will enhance prediction accuracy.},
doi = {10.1016/j.scitotenv.2018.05.256},
journal = {Science of the Total Environment},
issn = {0048-9697},
number = C,
volume = 642,
place = {United States},
year = {2018},
month = {11}
}