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

Journal Article · · PLoS ONE

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.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC05-76RL01830; AC06-76RLO 1830
OSTI ID:
1595181
Alternate ID(s):
OSTI ID: 1597652
Report Number(s):
PNNL-SA-125632
Journal Information:
PLoS ONE, Vol. 15, Issue 1; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 7 works
Citation information provided by
Web of Science

References (66)

The Influence of Functional Diversity and Composition on Ecosystem Processes journal August 1997
Influence of land-use intensity on the spatial distribution of N-cycling microorganisms in grassland soils: Spatial distribution of N-cycling soil microorganisms journal April 2011
Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils journal November 2012
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform journal July 2002
Recently identified microbial guild mediates soil N2O sink capacity journal July 2014
Impacts of Biodiversity Loss on Ocean Ecosystem Services journal November 2006
Functional redundancy in ecology and conservation journal July 2002
Nitrogen Cycling Potential of a Grassland Litter Microbial Community journal July 2015
Complete nitrification by Nitrospira bacteria journal November 2015
Fundamentals of Microbial Community Resistance and Resilience journal January 2012
Global biogeography of microbial nitrogen-cycling traits in soil journal July 2016
Hydrologic Controls on Nitrogen Cycling Processes and Functional Gene Abundance in Sediments of a Groundwater Flow-Through Lake journal March 2016
Accelerated Profile HMM Searches journal October 2011
Do we need to understand microbial communities to predict ecosystem function? A comparison of statistical models of nitrogen cycling processes journal January 2014
Xander: employing a novel method for efficient gene-targeted metagenomic assembly journal August 2015
Division of labour in microorganisms: an evolutionary perspective journal September 2016
Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes? journal February 2016
Cell biology and molecular basis of denitrification. journal January 1997
Deterministic influences exceed dispersal effects on hydrologically-connected microbiomes: Deterministic assembly of hyporheic microbiomes journal March 2017
Ecosystem Consequences of Microbial Diversity and Community Structure book January 1995
Bacterial diversity promotes community stability and functional resilience after perturbation journal March 2005
Effects of Biodiversity on Ecosystem Functioning: a Consensus of Current Knowledge journal February 2005
Microbial diversity — exploration of natural ecosystems and microbiomes journal December 2015
Fine-Scale in Situ Measurement of Riverbed Nitrate Production and Consumption in an Armored Permeable Riverbed journal March 2014
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments journal March 2010
Resistance, resilience, and redundancy in microbial communities journal August 2008
VEGAN, a package of R functions for community ecology journal April 2003
Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis journal February 1999
Microbial diversity and function in soil: from genes to ecosystems journal June 2002
Biodiversity and Ecological Redundancy journal March 1992
Organismal and spatial partitioning of energy and macronutrient transformations within a hypersaline mat journal March 2017
Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale journal August 2010
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
Genomic insights that advance the species definition for prokaryotes journal February 2005
Sequential computation of elementary modes and minimal cut sets in genome-scale metabolic networks using alternate integer linear programming journal March 2017
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
Habitat Loss, Trophic Collapse, and the Decline of Ecosystem Services journal August 2006
Influences of organic carbon speciation on hyporheic corridor biogeochemistry and microbial ecology journal February 2018
Characteristics of aerobic and anaerobic ammonium-oxidizing bacteria in the hyporheic zone of a contaminated river journal June 2012
VEGAN, a package of R functions for community ecology journal January 2003
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins journal March 2021
Cell biology and molecular basis of denitrification journal December 1997
Effects of biodiversity on ecosystem functioning: a consensus of current knowledge text January 2005
Ecosystem Consequences of Microbial Diversity and Community Structure book January 1995
Characteristics of aerobic and anaerobic ammonium-oxidizing bacteria in the hyporheic zone of a contaminated river journal June 2012
Microbial diversity — exploration of natural ecosystems and microbiomes journal December 2015
Fine-Scale in Situ Measurement of Riverbed Nitrate Production and Consumption in an Armored Permeable Riverbed journal March 2014
Functional redundancy in ecology and conservation journal July 2002
Complete nitrification by Nitrospira bacteria journal November 2015
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
Full-length transcriptome analysis of multiple organs and identification of adaptive genes and pathways in Mikania micrantha journal February 2022
Biodiversity and Ecological Redundancy journal March 1992
Genomic insights that advance the species definition for prokaryotes journal February 2005
Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils journal November 2012
Global biogeography of microbial nitrogen-cycling traits in soil journal July 2016
Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis journal February 1999
Sequential computation of elementary modes and minimal cut sets in genome-scale metabolic networks using alternate integer linear programming journal March 2017
Organismal and spatial partitioning of energy and macronutrient transformations within a hypersaline mat journal March 2017
VEGAN, a package of R functions for community ecology journal April 2003
Linking Uncultivated Microbial Populations and Benthic Carbon Turnover by Using Quantitative Stable Isotope Probing journal July 2018
Cell biology and molecular basis of denitrification journal December 1997
Accelerated Profile HMM Searches journal October 2011
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments journal March 2010
Effects of Biodiversity on Ecosystem Functioning: a Consensus of Current Knowledge journal February 2005
Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes? journal February 2016
Coupling Spatiotemporal Community Assembly Processes to Changes in Microbial Metabolism journal December 2016