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Title: Distinct temporal diversity profiles for nitrogen cycling genes in a hyporheic microbiome

Abstract

Biodiversity is thought to prevent decline in community function in response to changing environmental conditions through replacement of organisms with similar functional capacity but different optimal growth characteristics. We examined how this concept translates to the within-gene level by exploring seasonal dynamics of within-gene diversity for genes involved in nitrogen cycling in hyporheic zone communities. Nitrification genes displayed low richness—defined as the number of unique within-gene phylotypes—across seasons. Conversely, denitrification genes varied in both richness and the degree to which phylotypes were recruited or lost. These results demonstrate that there is not a universal mechanism for maintaining community functional potential for nitrogen cycling activities, even across seasonal environmental shifts to which communities would be expected to be well adapted. As such, extreme environmental changes could have very different effects on the stability of the different nitrogen cycle activities. These outcomes suggest a need to modify existing conceptual models that link biodiversity to microbiome function to incorporate within-gene diversity. Specifically, we suggest an expanded conceptualization that 1) recognizes component steps (genes) with low diversity as potential bottlenecks influencing pathway-level function, and 2) includes variation in both the number of entities (e.g. species, phylotypes) that can contribute to a given process andmore » the turnover of those entities in response to shifting conditions. In conclusion, building these concepts into process-based ecosystem models represents an exciting opportunity to connect within-gene-scale ecological dynamics to ecosystem-scale services.« less

Authors:
ORCiD logo; ; ORCiD logo; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1595181
Alternate Identifier(s):
OSTI ID: 1597652
Report Number(s):
PNNL-SA-125632
Journal ID: ISSN 1932-6203; 10.1371/journal.pone.0228165
Grant/Contract Number:  
AC06-76RLO 1830; AC05-76RL01830
Resource Type:
Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Name: PLoS ONE Journal Volume: 15 Journal Issue: 1; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science (PLoS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; microbial ecology; hyporheic zone; nitrification; denitrification; metagenomics

Citation Formats

Nelson, William C., Graham, Emily B., Crump, Alex R., Fansler, Sarah J., Arntzen, Evan V., Kennedy, David W., Stegen, James C., and Liu, ed., Wenzhi. Distinct temporal diversity profiles for nitrogen cycling genes in a hyporheic microbiome. United States: N. p., 2020. Web. doi:10.1371/journal.pone.0228165.
Nelson, William C., Graham, Emily B., Crump, Alex R., Fansler, Sarah J., Arntzen, Evan V., Kennedy, David W., Stegen, James C., & Liu, ed., Wenzhi. Distinct temporal diversity profiles for nitrogen cycling genes in a hyporheic microbiome. United States. https://doi.org/10.1371/journal.pone.0228165
Nelson, William C., Graham, Emily B., Crump, Alex R., Fansler, Sarah J., Arntzen, Evan V., Kennedy, David W., Stegen, James C., and Liu, ed., Wenzhi. Mon . "Distinct temporal diversity profiles for nitrogen cycling genes in a hyporheic microbiome". United States. https://doi.org/10.1371/journal.pone.0228165.
@article{osti_1595181,
title = {Distinct temporal diversity profiles for nitrogen cycling genes in a hyporheic microbiome},
author = {Nelson, William C. and Graham, Emily B. and Crump, Alex R. and Fansler, Sarah J. and Arntzen, Evan V. and Kennedy, David W. and Stegen, James C. and Liu, ed., Wenzhi},
abstractNote = {Biodiversity is thought to prevent decline in community function in response to changing environmental conditions through replacement of organisms with similar functional capacity but different optimal growth characteristics. We examined how this concept translates to the within-gene level by exploring seasonal dynamics of within-gene diversity for genes involved in nitrogen cycling in hyporheic zone communities. Nitrification genes displayed low richness—defined as the number of unique within-gene phylotypes—across seasons. Conversely, denitrification genes varied in both richness and the degree to which phylotypes were recruited or lost. These results demonstrate that there is not a universal mechanism for maintaining community functional potential for nitrogen cycling activities, even across seasonal environmental shifts to which communities would be expected to be well adapted. As such, extreme environmental changes could have very different effects on the stability of the different nitrogen cycle activities. These outcomes suggest a need to modify existing conceptual models that link biodiversity to microbiome function to incorporate within-gene diversity. Specifically, we suggest an expanded conceptualization that 1) recognizes component steps (genes) with low diversity as potential bottlenecks influencing pathway-level function, and 2) includes variation in both the number of entities (e.g. species, phylotypes) that can contribute to a given process and the turnover of those entities in response to shifting conditions. In conclusion, building these concepts into process-based ecosystem models represents an exciting opportunity to connect within-gene-scale ecological dynamics to ecosystem-scale services.},
doi = {10.1371/journal.pone.0228165},
journal = {PLoS ONE},
number = 1,
volume = 15,
place = {United States},
year = {Mon Jan 27 00:00:00 EST 2020},
month = {Mon Jan 27 00:00:00 EST 2020}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1371/journal.pone.0228165

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Cited by: 7 works
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