Genomic Signatures for Sedimentary Microbial Utilization of Phytoplankton Detritus in a Fast-Flowing Estuary

In fast-flowing, river-dominated estuaries, “hotspots” of microbial biogeochemical cycling can be found within areas of extended water retention. Lateral bays located off of the North and South channels of the Columbia River estuary are proposed to be such hotspots. Previous metagenomic studies on w...

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Main Authors: Maria W. Smith, Lydie Herfort, Adam R. Rivers, Holly M. Simon
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02475/full
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author Maria W. Smith
Lydie Herfort
Lydie Herfort
Adam R. Rivers
Holly M. Simon
Holly M. Simon
author_facet Maria W. Smith
Lydie Herfort
Lydie Herfort
Adam R. Rivers
Holly M. Simon
Holly M. Simon
author_sort Maria W. Smith
collection DOAJ
description In fast-flowing, river-dominated estuaries, “hotspots” of microbial biogeochemical cycling can be found within areas of extended water retention. Lateral bays located off of the North and South channels of the Columbia River estuary are proposed to be such hotspots. Previous metagenomic studies on water samples indicated that these regions function both as sources and sinks of biogenic particles, with potential to impact organic matter fluxes in the estuary. To extend this work, we analyzed 11 sediment metagenomes from three disparate bays: the freshwater Cathlamet Bay, and the brackish Youngs Bay and more saline Baker Bay located nearer the mouth to the south and north of the main channel, respectively. Samples were collected from upper layers of sediments in August of 2011 and 2013 for DNA extraction and metagenome sequencing. All metagenomes were dominated by bacterial sequences, although diatom sequences as high as 26% of the total annotated sequences were observed in the higher salinity samples. Unsupervised 2D hierarchical clustering analysis resulted in the eleven metagenome samples clustered into four groups by microbial taxonomic composition, with Bacteroides, diatom, and phage levels driving most of the grouping. Results of functional gene clustering further indicated that diatom bloom degradation stage (early vs. late) was an important factor. While the Flavobacteriia and Cytophagia classes were well represented in metagenomes containing abundant diatoms, taxa from the Bacteroidia class, along with certain members of the Sphingobacteriia class, were particularly abundant in metagenomes representing later stages of diatom decomposition. In contrast, the sediment metagenomes with low relative abundance of diatom and Bacteroidetes sequences appeared to have a metabolic potential biased toward microbial growth under nutrient limitation. While differences in water salinity clearly also influenced the microbial community composition and metabolic potential, our results highlight a central role for allochthonous labile organic matter (i.e., diatom detritus), in shaping bacterial taxonomic and functional properties in the Columbia River estuary lateral bay sediments. These results suggest that in fast-flowing, river-dominated estuaries, sediment microbial communities in areas of extended water retention, such as the lateral bays, may contribute disproportionately to estuarine organic matter degradation and recycling.
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spelling doaj.art-413b0f6e152845ea992b95f162a31d2f2022-12-21T23:50:13ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-11-011010.3389/fmicb.2019.02475476678Genomic Signatures for Sedimentary Microbial Utilization of Phytoplankton Detritus in a Fast-Flowing EstuaryMaria W. Smith0Lydie Herfort1Lydie Herfort2Adam R. Rivers3Holly M. Simon4Holly M. Simon5Center for Coastal Margin Observation & Prediction, Oregon Health & Science University, Portland, OR, United StatesCenter for Coastal Margin Observation & Prediction, Oregon Health & Science University, Portland, OR, United StatesInstitute of Environmental Health, Oregon Health & Science University, Portland, OR, United StatesU.S. Department of Energy Joint Genome Institute, Walnut Creek, CA, United StatesCenter for Coastal Margin Observation & Prediction, Oregon Health & Science University, Portland, OR, United StatesInstitute of Environmental Health, Oregon Health & Science University, Portland, OR, United StatesIn fast-flowing, river-dominated estuaries, “hotspots” of microbial biogeochemical cycling can be found within areas of extended water retention. Lateral bays located off of the North and South channels of the Columbia River estuary are proposed to be such hotspots. Previous metagenomic studies on water samples indicated that these regions function both as sources and sinks of biogenic particles, with potential to impact organic matter fluxes in the estuary. To extend this work, we analyzed 11 sediment metagenomes from three disparate bays: the freshwater Cathlamet Bay, and the brackish Youngs Bay and more saline Baker Bay located nearer the mouth to the south and north of the main channel, respectively. Samples were collected from upper layers of sediments in August of 2011 and 2013 for DNA extraction and metagenome sequencing. All metagenomes were dominated by bacterial sequences, although diatom sequences as high as 26% of the total annotated sequences were observed in the higher salinity samples. Unsupervised 2D hierarchical clustering analysis resulted in the eleven metagenome samples clustered into four groups by microbial taxonomic composition, with Bacteroides, diatom, and phage levels driving most of the grouping. Results of functional gene clustering further indicated that diatom bloom degradation stage (early vs. late) was an important factor. While the Flavobacteriia and Cytophagia classes were well represented in metagenomes containing abundant diatoms, taxa from the Bacteroidia class, along with certain members of the Sphingobacteriia class, were particularly abundant in metagenomes representing later stages of diatom decomposition. In contrast, the sediment metagenomes with low relative abundance of diatom and Bacteroidetes sequences appeared to have a metabolic potential biased toward microbial growth under nutrient limitation. While differences in water salinity clearly also influenced the microbial community composition and metabolic potential, our results highlight a central role for allochthonous labile organic matter (i.e., diatom detritus), in shaping bacterial taxonomic and functional properties in the Columbia River estuary lateral bay sediments. These results suggest that in fast-flowing, river-dominated estuaries, sediment microbial communities in areas of extended water retention, such as the lateral bays, may contribute disproportionately to estuarine organic matter degradation and recycling.https://www.frontiersin.org/article/10.3389/fmicb.2019.02475/fullmetagenomicsmicrobial communityestuarine sedimentsphytoplanktonBacteroidetesbacteriophage
spellingShingle Maria W. Smith
Lydie Herfort
Lydie Herfort
Adam R. Rivers
Holly M. Simon
Holly M. Simon
Genomic Signatures for Sedimentary Microbial Utilization of Phytoplankton Detritus in a Fast-Flowing Estuary
Frontiers in Microbiology
metagenomics
microbial community
estuarine sediments
phytoplankton
Bacteroidetes
bacteriophage
title Genomic Signatures for Sedimentary Microbial Utilization of Phytoplankton Detritus in a Fast-Flowing Estuary
title_full Genomic Signatures for Sedimentary Microbial Utilization of Phytoplankton Detritus in a Fast-Flowing Estuary
title_fullStr Genomic Signatures for Sedimentary Microbial Utilization of Phytoplankton Detritus in a Fast-Flowing Estuary
title_full_unstemmed Genomic Signatures for Sedimentary Microbial Utilization of Phytoplankton Detritus in a Fast-Flowing Estuary
title_short Genomic Signatures for Sedimentary Microbial Utilization of Phytoplankton Detritus in a Fast-Flowing Estuary
title_sort genomic signatures for sedimentary microbial utilization of phytoplankton detritus in a fast flowing estuary
topic metagenomics
microbial community
estuarine sediments
phytoplankton
Bacteroidetes
bacteriophage
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02475/full
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