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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. For this study, 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 by shifting metabolism towards carbohydrate-utilizing 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 or N content only (explaining 67% vs. 42% and 37% of variation respectively), and bulk C and N did not improve statistical models based on metabolome composition alone. These results point to organic nitrogen as a significant regulatorymore » 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.« less

Authors:
ORCiD logo [1];  [2];  [1];  [1];  [1];  [3];  [3];  [1];  [3];  [1]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  2. Univ. of Idaho, Moscow, ID (United States)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1457749
Alternate Identifier(s):
OSTI ID: 1548167
Report Number(s):
PNNL-SA-133671
Journal ID: ISSN 0048-9697; PII: S0048969718319089
Grant/Contract Number:  
AC0576RL01830; AC06-76RLO 1830
Resource Type:
Accepted Manuscript
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
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; FT-ICR-MS; Respiration; Coupled C-N cycling; Carbon cycle; Riparian; Hydrobiogeochemistry

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. https://doi.org/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. Sun . "Multi 'omics comparison reveals metabolome biochemistry, not microbiome composition or gene expression, corresponds to elevated biogeochemical function in the hyporheic zone". United States. https://doi.org/10.1016/J.SCITOTENV.2018.05.256. https://www.osti.gov/servlets/purl/1457749.
@article{osti_1457749,
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. For this study, 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 by shifting metabolism towards carbohydrate-utilizing 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 or N content only (explaining 67% vs. 42% and 37% of variation respectively), and bulk C and N 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},
number = C,
volume = 642,
place = {United States},
year = {Sun Jun 17 00:00:00 EDT 2018},
month = {Sun Jun 17 00:00:00 EDT 2018}
}

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Figures / Tables:

Fig. 1 Fig. 1: Multi 'omic differences in hotspots vs. low-activity sediments. (a–d) show the most abundant classifications only for visual simplicity, but P-values in the upper left-hand corner of each panel are derived from all data. All data are reported as percent abundance. P-values are derived from PERMANOVA with stratification bymore » depth. R2 values are provided for significant P-values. Red denotes hotspots, and blue denotes low-activity sediments. (a) shows abundant microorganisms (grouped at the class level), (b) shows abundant metagenomics annotations, (c) shows abundant metaproteomic identifications, and (d) shows metabolomics data grouped by compound class. Asterisks denote significant differences between hotspots and low-activity sediments, via mixed models with depth as a random effect (P < 0.05). (For interpretation of the references to colour in this figure legend, the reader is referred to the in web version of this article.)« less

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