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Title: Microbial Community Structure–Function Relationships in Yaquina Bay Estuary Reveal Spatially Distinct Carbon and Nitrogen Cycling Capacities

Abstract

Linking microbial community structure to ecological processes requires understanding of the functional roles among individual populations and the factors that influence their distributions. These structure–function relationships are particularly difficult to disentangle in estuaries, due to highly variable physico-chemical conditions. Yet, examining microbe-mediated turnover of resources in these “bioreactor” ecosystems is critical for understanding estuarine ecology. In this study, a combined metagenomics and metaproteomics approach was used to show that the unequal distribution of microbial populations across the Yaquina Bay estuary led to a habitat-specific taxonomic and functional structure and a clear spatial distribution in microbe-mediated capacities for cycling of carbon and nitrogen. For example, size-fractionation revealed that communities inhabiting suspended particulate material encoded more diverse types of metabolisms (e.g., fermentation and denitrification) than those with a planktonic lifestyle, suggesting that the metabolic reactions can differ between size fractions of the same parcel of an estuarine water column. Similarly, communities inhabiting oligotrophic conditions in the lower estuary were enriched in genes involved in central carbon metabolism (e.g., TCA cycle), while communities in the upper estuary were enriched in genes typical of copiotrophic populations (e.g., cell growth, cell division). Integrating gene and protein data revealed that abundant populations of Flavobacteriales and Rhodobacteralesmore » encoded similar genomic functions, yet differed significantly in protein expression, dedicating a large proportion of their respective proteomes to rapid growth and division versus metabolic versatility and resource acquisition. This suggested potentially distinct life-strategies between these two co-occurring lineages and was concomitant with differing patterns of positive evolutionary selection on their encoded genes. Microbial communities and their functions across Yaquina Bay appear to be structured by population-level habitat preferences, resulting in spatially distinct elemental cycling, while within each community, forces such as competitive exclusion and evolutionary selection influence species life-strategies and may help maintain microbial diversity.« less

Authors:
 [1];  [2];  [3];  [1];  [2];  [2];  [4];  [1]
  1. Oregon State Univ., Corvallis, OR (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  3. Univ. of Washington, Seattle, WA (United States)
  4. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1474503
Alternate Identifier(s):
OSTI ID: 1488816
Report Number(s):
LLNL-JRNL-741426
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
AC05-00OR22725; AC52-07NA27344
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 9; Journal Issue: n/a; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biological and medical sciences

Citation Formats

Kieft, Brandon, Li, Zhou, Bryson, Samuel, Crump, Byron C., Hettich, Robert, Pan, Chongle, Mayali, Xavier, and Mueller, Ryan S. Microbial Community Structure–Function Relationships in Yaquina Bay Estuary Reveal Spatially Distinct Carbon and Nitrogen Cycling Capacities. United States: N. p., 2018. Web. doi:10.3389/fmicb.2018.01282.
Kieft, Brandon, Li, Zhou, Bryson, Samuel, Crump, Byron C., Hettich, Robert, Pan, Chongle, Mayali, Xavier, & Mueller, Ryan S. Microbial Community Structure–Function Relationships in Yaquina Bay Estuary Reveal Spatially Distinct Carbon and Nitrogen Cycling Capacities. United States. doi:10.3389/fmicb.2018.01282.
Kieft, Brandon, Li, Zhou, Bryson, Samuel, Crump, Byron C., Hettich, Robert, Pan, Chongle, Mayali, Xavier, and Mueller, Ryan S. Thu . "Microbial Community Structure–Function Relationships in Yaquina Bay Estuary Reveal Spatially Distinct Carbon and Nitrogen Cycling Capacities". United States. doi:10.3389/fmicb.2018.01282. https://www.osti.gov/servlets/purl/1474503.
@article{osti_1474503,
title = {Microbial Community Structure–Function Relationships in Yaquina Bay Estuary Reveal Spatially Distinct Carbon and Nitrogen Cycling Capacities},
author = {Kieft, Brandon and Li, Zhou and Bryson, Samuel and Crump, Byron C. and Hettich, Robert and Pan, Chongle and Mayali, Xavier and Mueller, Ryan S.},
abstractNote = {Linking microbial community structure to ecological processes requires understanding of the functional roles among individual populations and the factors that influence their distributions. These structure–function relationships are particularly difficult to disentangle in estuaries, due to highly variable physico-chemical conditions. Yet, examining microbe-mediated turnover of resources in these “bioreactor” ecosystems is critical for understanding estuarine ecology. In this study, a combined metagenomics and metaproteomics approach was used to show that the unequal distribution of microbial populations across the Yaquina Bay estuary led to a habitat-specific taxonomic and functional structure and a clear spatial distribution in microbe-mediated capacities for cycling of carbon and nitrogen. For example, size-fractionation revealed that communities inhabiting suspended particulate material encoded more diverse types of metabolisms (e.g., fermentation and denitrification) than those with a planktonic lifestyle, suggesting that the metabolic reactions can differ between size fractions of the same parcel of an estuarine water column. Similarly, communities inhabiting oligotrophic conditions in the lower estuary were enriched in genes involved in central carbon metabolism (e.g., TCA cycle), while communities in the upper estuary were enriched in genes typical of copiotrophic populations (e.g., cell growth, cell division). Integrating gene and protein data revealed that abundant populations of Flavobacteriales and Rhodobacterales encoded similar genomic functions, yet differed significantly in protein expression, dedicating a large proportion of their respective proteomes to rapid growth and division versus metabolic versatility and resource acquisition. This suggested potentially distinct life-strategies between these two co-occurring lineages and was concomitant with differing patterns of positive evolutionary selection on their encoded genes. Microbial communities and their functions across Yaquina Bay appear to be structured by population-level habitat preferences, resulting in spatially distinct elemental cycling, while within each community, forces such as competitive exclusion and evolutionary selection influence species life-strategies and may help maintain microbial diversity.},
doi = {10.3389/fmicb.2018.01282},
journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = n/a,
volume = 9,
place = {United States},
year = {2018},
month = {6}
}

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Cited by: 3 works
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Figures / Tables:

Table 1. Table 1.: Genes in Rhodobacterales and Flavobacteriales lineages that are under putative positive selection. OG = orthologous group, where the 3-digit numbers represent clusters of orthologs predicted by ProteinOrtho. P-value = p-value from modeling. Q-value = Benjamin-Hochberg correction of p-values with FDR cut-off set at 0.05. In the COG cat.more » column, typefaces indicate the following classes: bold = Metabolism; italic = Cell Processing and Signaling; underlined = Information Storage and Processing; normal = Poorly characterized.« less

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