Shifts in coastal sediment oxygenation cause pronounced changes in microbial community composition and associated metabolism

Elias Broman, Johanna Sjöstedt, Jarone Pinhassi, Mark Dopson

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Abstract

A key characteristic of eutrophication in coastal seas is the expansion of hypoxic bottom waters, often referred to as 'dead zones'. One proposed remediation strategy for coastal dead zones in the Baltic Sea is to mix the water column using pump stations, circulating oxygenated water to the sea bottom. Although microbial metabolism in the sediment surface is recognized as key in regulating bulk chemical fluxes, it remains unknown how the microbial community and its metabolic processes are influenced by shifts in oxygen availability. Here, coastal Baltic Sea sediments sampled from oxic and anoxic sites, plus an intermediate area subjected to episodic oxygenation, were experimentally exposed to oxygen shifts. Chemical, 16S rRNA gene, metagenomic, and metatranscriptomic analyses were conducted to investigate changes in chemistry fluxes, microbial community structure, and metabolic functions in the sediment surface. Compared to anoxic controls, oxygenation of anoxic sediment resulted in a proliferation of bacterial populations in the facultative anaerobic genus Sulfurovum that are capable of oxidizing toxic sulfide. Furthermore, the oxygenated sediment had higher amounts of RNA transcripts annotated as sqr, fccB, and dsrA involved in sulfide oxidation. In addition, the importance of cryptic sulfur cycling was highlighted by the oxidative genes listed above as well as dsvA, ttrB, dmsA, and ddhAB that encode reductive processes being identified in anoxic and intermediate sediments turned oxic. In particular, the intermediate site sediments responded differently upon oxygenation compared to the anoxic and oxic site sediments. This included a microbial community composition with more habitat generalists, lower amounts of RNA transcripts attributed to methane oxidation, and a reduced rate of organic matter degradation. These novel data emphasize that genetic expression analyses has the power to identify key molecular mechanisms that regulate microbial community responses upon oxygenation of dead zones. Moreover, these results highlight that microbial responses, and therefore ultimately remediation efforts, depend largely on the oxygenation history of sites. Furthermore, it was shown that re-oxygenation efforts to remediate dead zones could ultimately be facilitated by in situ microbial molecular mechanisms involved in removal of toxic H2S and the potent greenhouse gas methane.
Original languageEnglish
JournalMicrobiome
Volume5
Issue number1
Pages (from-to)96
Number of pages1
ISSN2049-2618
DOIs
Publication statusPublished - 2017

Keywords

  • 16S rRNA
  • Anoxic
  • Metagenomics
  • Metatranscriptomics
  • Oxic
  • Sediment

Cite this

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title = "Shifts in coastal sediment oxygenation cause pronounced changes in microbial community composition and associated metabolism",
abstract = "A key characteristic of eutrophication in coastal seas is the expansion of hypoxic bottom waters, often referred to as 'dead zones'. One proposed remediation strategy for coastal dead zones in the Baltic Sea is to mix the water column using pump stations, circulating oxygenated water to the sea bottom. Although microbial metabolism in the sediment surface is recognized as key in regulating bulk chemical fluxes, it remains unknown how the microbial community and its metabolic processes are influenced by shifts in oxygen availability. Here, coastal Baltic Sea sediments sampled from oxic and anoxic sites, plus an intermediate area subjected to episodic oxygenation, were experimentally exposed to oxygen shifts. Chemical, 16S rRNA gene, metagenomic, and metatranscriptomic analyses were conducted to investigate changes in chemistry fluxes, microbial community structure, and metabolic functions in the sediment surface. Compared to anoxic controls, oxygenation of anoxic sediment resulted in a proliferation of bacterial populations in the facultative anaerobic genus Sulfurovum that are capable of oxidizing toxic sulfide. Furthermore, the oxygenated sediment had higher amounts of RNA transcripts annotated as sqr, fccB, and dsrA involved in sulfide oxidation. In addition, the importance of cryptic sulfur cycling was highlighted by the oxidative genes listed above as well as dsvA, ttrB, dmsA, and ddhAB that encode reductive processes being identified in anoxic and intermediate sediments turned oxic. In particular, the intermediate site sediments responded differently upon oxygenation compared to the anoxic and oxic site sediments. This included a microbial community composition with more habitat generalists, lower amounts of RNA transcripts attributed to methane oxidation, and a reduced rate of organic matter degradation. These novel data emphasize that genetic expression analyses has the power to identify key molecular mechanisms that regulate microbial community responses upon oxygenation of dead zones. Moreover, these results highlight that microbial responses, and therefore ultimately remediation efforts, depend largely on the oxygenation history of sites. Furthermore, it was shown that re-oxygenation efforts to remediate dead zones could ultimately be facilitated by in situ microbial molecular mechanisms involved in removal of toxic H2S and the potent greenhouse gas methane.",
keywords = "16S rRNA, Anoxic, Metagenomics, Metatranscriptomics, Oxic, Sediment",
author = "Elias Broman and Johanna Sj{\"o}stedt and Jarone Pinhassi and Mark Dopson",
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language = "English",
volume = "5",
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Shifts in coastal sediment oxygenation cause pronounced changes in microbial community composition and associated metabolism. / Broman, Elias; Sjöstedt, Johanna; Pinhassi, Jarone; Dopson, Mark.

In: Microbiome, Vol. 5, No. 1, 2017, p. 96.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Shifts in coastal sediment oxygenation cause pronounced changes in microbial community composition and associated metabolism

AU - Broman, Elias

AU - Sjöstedt, Johanna

AU - Pinhassi, Jarone

AU - Dopson, Mark

PY - 2017

Y1 - 2017

N2 - A key characteristic of eutrophication in coastal seas is the expansion of hypoxic bottom waters, often referred to as 'dead zones'. One proposed remediation strategy for coastal dead zones in the Baltic Sea is to mix the water column using pump stations, circulating oxygenated water to the sea bottom. Although microbial metabolism in the sediment surface is recognized as key in regulating bulk chemical fluxes, it remains unknown how the microbial community and its metabolic processes are influenced by shifts in oxygen availability. Here, coastal Baltic Sea sediments sampled from oxic and anoxic sites, plus an intermediate area subjected to episodic oxygenation, were experimentally exposed to oxygen shifts. Chemical, 16S rRNA gene, metagenomic, and metatranscriptomic analyses were conducted to investigate changes in chemistry fluxes, microbial community structure, and metabolic functions in the sediment surface. Compared to anoxic controls, oxygenation of anoxic sediment resulted in a proliferation of bacterial populations in the facultative anaerobic genus Sulfurovum that are capable of oxidizing toxic sulfide. Furthermore, the oxygenated sediment had higher amounts of RNA transcripts annotated as sqr, fccB, and dsrA involved in sulfide oxidation. In addition, the importance of cryptic sulfur cycling was highlighted by the oxidative genes listed above as well as dsvA, ttrB, dmsA, and ddhAB that encode reductive processes being identified in anoxic and intermediate sediments turned oxic. In particular, the intermediate site sediments responded differently upon oxygenation compared to the anoxic and oxic site sediments. This included a microbial community composition with more habitat generalists, lower amounts of RNA transcripts attributed to methane oxidation, and a reduced rate of organic matter degradation. These novel data emphasize that genetic expression analyses has the power to identify key molecular mechanisms that regulate microbial community responses upon oxygenation of dead zones. Moreover, these results highlight that microbial responses, and therefore ultimately remediation efforts, depend largely on the oxygenation history of sites. Furthermore, it was shown that re-oxygenation efforts to remediate dead zones could ultimately be facilitated by in situ microbial molecular mechanisms involved in removal of toxic H2S and the potent greenhouse gas methane.

AB - A key characteristic of eutrophication in coastal seas is the expansion of hypoxic bottom waters, often referred to as 'dead zones'. One proposed remediation strategy for coastal dead zones in the Baltic Sea is to mix the water column using pump stations, circulating oxygenated water to the sea bottom. Although microbial metabolism in the sediment surface is recognized as key in regulating bulk chemical fluxes, it remains unknown how the microbial community and its metabolic processes are influenced by shifts in oxygen availability. Here, coastal Baltic Sea sediments sampled from oxic and anoxic sites, plus an intermediate area subjected to episodic oxygenation, were experimentally exposed to oxygen shifts. Chemical, 16S rRNA gene, metagenomic, and metatranscriptomic analyses were conducted to investigate changes in chemistry fluxes, microbial community structure, and metabolic functions in the sediment surface. Compared to anoxic controls, oxygenation of anoxic sediment resulted in a proliferation of bacterial populations in the facultative anaerobic genus Sulfurovum that are capable of oxidizing toxic sulfide. Furthermore, the oxygenated sediment had higher amounts of RNA transcripts annotated as sqr, fccB, and dsrA involved in sulfide oxidation. In addition, the importance of cryptic sulfur cycling was highlighted by the oxidative genes listed above as well as dsvA, ttrB, dmsA, and ddhAB that encode reductive processes being identified in anoxic and intermediate sediments turned oxic. In particular, the intermediate site sediments responded differently upon oxygenation compared to the anoxic and oxic site sediments. This included a microbial community composition with more habitat generalists, lower amounts of RNA transcripts attributed to methane oxidation, and a reduced rate of organic matter degradation. These novel data emphasize that genetic expression analyses has the power to identify key molecular mechanisms that regulate microbial community responses upon oxygenation of dead zones. Moreover, these results highlight that microbial responses, and therefore ultimately remediation efforts, depend largely on the oxygenation history of sites. Furthermore, it was shown that re-oxygenation efforts to remediate dead zones could ultimately be facilitated by in situ microbial molecular mechanisms involved in removal of toxic H2S and the potent greenhouse gas methane.

KW - 16S rRNA

KW - Anoxic

KW - Metagenomics

KW - Metatranscriptomics

KW - Oxic

KW - Sediment

U2 - 10.1186/s40168-017-0311-5

DO - 10.1186/s40168-017-0311-5

M3 - Journal article

C2 - 28793929

VL - 5

SP - 96

JO - Microbiome

JF - Microbiome

SN - 2049-2618

IS - 1

ER -