Microbial players and processes involved in phytoplankton bloom utilization in the water column of a fast-flowing, river-dominated estuary

Maria W. Smith, Lydie Herfort, Caroline S. Fortunato, Byron C. Crump, Holly Simon

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Fueled by seasonal phytoplankton blooms, the Columbia River estuary is a natural bioreactor for organic matter transformations. Prior metagenome analyses indicated high abundances of diverse Bacteroidetes taxa in estuarine samples containing phytoplankton. To examine the hypothesis that Bacteroidetes taxa have important roles in phytoplankton turnover, we further analyzed metagenomes from water collected along a salinity gradient at 0, 5, 15, 25, and 33 PSU during bloom events. Size fractions were obtained by using a 3-μm prefilter and 0.2-μm collection filter. Although this approach targeted bacteria by removing comparatively large eukaryotic cells, the metagenome from the ES-5 sample (5 PSU) nevertheless contained an abundance of diatom DNA. Biogeochemical measurements and prior studies indicated that this finding resulted from the leakage of cellular material due to freshwater diatom lysis at low salinity. Relative to the other metagenomes, the bacterial fraction of ES-5 was dramatically depleted of genes annotated as Bacteroidetes and lysogenic bacteriophages, but was overrepresented in DNA of protists and Myxococcales bacterivores. We suggest the following equally plausible scenarios for the microbial response to phytoplankton lysis: (1) Bacteroidetes depletion in the free-living fraction may at least in part be caused by their attachment to fluvial diatoms as the latter are lysed upon contact with low-salinity estuarine waters; (2) diatom particle colonization is likely followed by rapid bacterial growth and lytic phage infection, resulting in depletion of lysogenic bacteriophages and host bacteria; and (3) the subsequent availability of labile organic matter attracted both grazers and predators to feed in this estuarine biogeochemical "hotspot," which may have additionally depleted Bacteroidetes populations. These results represent the first detailed molecular analysis of the microbial response to phytoplankton lysis at the freshwater-brackish water interface in the fast-flowing Columbia River estuary.

Original languageEnglish (US)
JournalMicrobiologyOpen
DOIs
StateAccepted/In press - 2017

Fingerprint

Bacteroidetes
Phytoplankton
Estuaries
Metagenome
Diatoms
Rivers
Salinity
Water
Bacteriophages
Fresh Water
Myxococcales
Bacteria
DNA
Bioreactors
Eukaryotic Cells
Growth
Infection
Population
Genes

Keywords

  • Bacteroidetes
  • Metagenome analysis
  • Phytoplankton bloom degradation

ASJC Scopus subject areas

  • Microbiology

Cite this

Microbial players and processes involved in phytoplankton bloom utilization in the water column of a fast-flowing, river-dominated estuary. / Smith, Maria W.; Herfort, Lydie; Fortunato, Caroline S.; Crump, Byron C.; Simon, Holly.

In: MicrobiologyOpen, 2017.

Research output: Contribution to journalArticle

@article{6e772c768510473b9a745228954a06ae,
title = "Microbial players and processes involved in phytoplankton bloom utilization in the water column of a fast-flowing, river-dominated estuary",
abstract = "Fueled by seasonal phytoplankton blooms, the Columbia River estuary is a natural bioreactor for organic matter transformations. Prior metagenome analyses indicated high abundances of diverse Bacteroidetes taxa in estuarine samples containing phytoplankton. To examine the hypothesis that Bacteroidetes taxa have important roles in phytoplankton turnover, we further analyzed metagenomes from water collected along a salinity gradient at 0, 5, 15, 25, and 33 PSU during bloom events. Size fractions were obtained by using a 3-μm prefilter and 0.2-μm collection filter. Although this approach targeted bacteria by removing comparatively large eukaryotic cells, the metagenome from the ES-5 sample (5 PSU) nevertheless contained an abundance of diatom DNA. Biogeochemical measurements and prior studies indicated that this finding resulted from the leakage of cellular material due to freshwater diatom lysis at low salinity. Relative to the other metagenomes, the bacterial fraction of ES-5 was dramatically depleted of genes annotated as Bacteroidetes and lysogenic bacteriophages, but was overrepresented in DNA of protists and Myxococcales bacterivores. We suggest the following equally plausible scenarios for the microbial response to phytoplankton lysis: (1) Bacteroidetes depletion in the free-living fraction may at least in part be caused by their attachment to fluvial diatoms as the latter are lysed upon contact with low-salinity estuarine waters; (2) diatom particle colonization is likely followed by rapid bacterial growth and lytic phage infection, resulting in depletion of lysogenic bacteriophages and host bacteria; and (3) the subsequent availability of labile organic matter attracted both grazers and predators to feed in this estuarine biogeochemical {"}hotspot,{"} which may have additionally depleted Bacteroidetes populations. These results represent the first detailed molecular analysis of the microbial response to phytoplankton lysis at the freshwater-brackish water interface in the fast-flowing Columbia River estuary.",
keywords = "Bacteroidetes, Metagenome analysis, Phytoplankton bloom degradation",
author = "Smith, {Maria W.} and Lydie Herfort and Fortunato, {Caroline S.} and Crump, {Byron C.} and Holly Simon",
year = "2017",
doi = "10.1002/mbo3.467",
language = "English (US)",
journal = "MicrobiologyOpen",
issn = "2045-8827",
publisher = "John Wiley and Sons Inc.",

}

TY - JOUR

T1 - Microbial players and processes involved in phytoplankton bloom utilization in the water column of a fast-flowing, river-dominated estuary

AU - Smith, Maria W.

AU - Herfort, Lydie

AU - Fortunato, Caroline S.

AU - Crump, Byron C.

AU - Simon, Holly

PY - 2017

Y1 - 2017

N2 - Fueled by seasonal phytoplankton blooms, the Columbia River estuary is a natural bioreactor for organic matter transformations. Prior metagenome analyses indicated high abundances of diverse Bacteroidetes taxa in estuarine samples containing phytoplankton. To examine the hypothesis that Bacteroidetes taxa have important roles in phytoplankton turnover, we further analyzed metagenomes from water collected along a salinity gradient at 0, 5, 15, 25, and 33 PSU during bloom events. Size fractions were obtained by using a 3-μm prefilter and 0.2-μm collection filter. Although this approach targeted bacteria by removing comparatively large eukaryotic cells, the metagenome from the ES-5 sample (5 PSU) nevertheless contained an abundance of diatom DNA. Biogeochemical measurements and prior studies indicated that this finding resulted from the leakage of cellular material due to freshwater diatom lysis at low salinity. Relative to the other metagenomes, the bacterial fraction of ES-5 was dramatically depleted of genes annotated as Bacteroidetes and lysogenic bacteriophages, but was overrepresented in DNA of protists and Myxococcales bacterivores. We suggest the following equally plausible scenarios for the microbial response to phytoplankton lysis: (1) Bacteroidetes depletion in the free-living fraction may at least in part be caused by their attachment to fluvial diatoms as the latter are lysed upon contact with low-salinity estuarine waters; (2) diatom particle colonization is likely followed by rapid bacterial growth and lytic phage infection, resulting in depletion of lysogenic bacteriophages and host bacteria; and (3) the subsequent availability of labile organic matter attracted both grazers and predators to feed in this estuarine biogeochemical "hotspot," which may have additionally depleted Bacteroidetes populations. These results represent the first detailed molecular analysis of the microbial response to phytoplankton lysis at the freshwater-brackish water interface in the fast-flowing Columbia River estuary.

AB - Fueled by seasonal phytoplankton blooms, the Columbia River estuary is a natural bioreactor for organic matter transformations. Prior metagenome analyses indicated high abundances of diverse Bacteroidetes taxa in estuarine samples containing phytoplankton. To examine the hypothesis that Bacteroidetes taxa have important roles in phytoplankton turnover, we further analyzed metagenomes from water collected along a salinity gradient at 0, 5, 15, 25, and 33 PSU during bloom events. Size fractions were obtained by using a 3-μm prefilter and 0.2-μm collection filter. Although this approach targeted bacteria by removing comparatively large eukaryotic cells, the metagenome from the ES-5 sample (5 PSU) nevertheless contained an abundance of diatom DNA. Biogeochemical measurements and prior studies indicated that this finding resulted from the leakage of cellular material due to freshwater diatom lysis at low salinity. Relative to the other metagenomes, the bacterial fraction of ES-5 was dramatically depleted of genes annotated as Bacteroidetes and lysogenic bacteriophages, but was overrepresented in DNA of protists and Myxococcales bacterivores. We suggest the following equally plausible scenarios for the microbial response to phytoplankton lysis: (1) Bacteroidetes depletion in the free-living fraction may at least in part be caused by their attachment to fluvial diatoms as the latter are lysed upon contact with low-salinity estuarine waters; (2) diatom particle colonization is likely followed by rapid bacterial growth and lytic phage infection, resulting in depletion of lysogenic bacteriophages and host bacteria; and (3) the subsequent availability of labile organic matter attracted both grazers and predators to feed in this estuarine biogeochemical "hotspot," which may have additionally depleted Bacteroidetes populations. These results represent the first detailed molecular analysis of the microbial response to phytoplankton lysis at the freshwater-brackish water interface in the fast-flowing Columbia River estuary.

KW - Bacteroidetes

KW - Metagenome analysis

KW - Phytoplankton bloom degradation

UR - http://www.scopus.com/inward/record.url?scp=85016416901&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85016416901&partnerID=8YFLogxK

U2 - 10.1002/mbo3.467

DO - 10.1002/mbo3.467

M3 - Article

JO - MicrobiologyOpen

JF - MicrobiologyOpen

SN - 2045-8827

ER -