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Ecology and evolution of coastal Baltic Sea 'dead zone' sediments
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)ORCID iD: 0000-0001-9005-5168
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Since industrialization and the release of agricultural fertilizers began, coastal and open waters of the Baltic Sea have been loaded with nutrients. This has increased the growth of algal blooms and because a portion of the algal organic matter sinks to the sea floor, hypoxia has increased. In conjunction to this, natural stratification of the water column makes the bottom zones especially prone to oxygen depletion due to microbes using oxygen and organic matter to grow. Hypoxia (<2 mg/L O2) and anoxia (no oxygen) are deadly for many organisms and only specialists (typically some microorganisms) are able to survive. Due to the harsh conditions these bottom zones are commonly referred to as 'dead zones'. The focus of this thesis was to look closer at the microbial community changes upon degradation of algal organic matter and the effect of oxygenating coastal Baltic Sea 'dead zone' sediments on chemistry fluxes, phyto- and zooplankton, the microbial community structure, and microbial metabolic responses. Results from field sampling and incubation experiments showed that degradation of algal biomass in nutrient rich oxic sediment was partly related to the growth of archaea; that oxygenation of anoxic sediments decreased stored organic matter plus triggered hatching of zooplankton eggs increasing the benthic-pelagic coupling; and resting diatoms buried in hypoxic/anoxic sediment were alive and triggered to germinate by light rather than oxygen. Changes in the microbial community structures to oxygen shifts were dependent on the historical exposure to oxygen and that microbial generalists adapted to episodic oxygenation were favored during oxygen shifts. Facultative anaerobic sulfur/sulfide oxidizing bacterial genera were favored upon oxygenation of hypoxic/anoxic sediment plus sulfur cycling and nitrogen fixation genes were abundant. Finally, it was discovered that oxygenation regulates metabolic processes involved in the sulfur and methane cycles, especially by metabolic processes that results in a decrease of toxic hydrogen sulfide as well as the potent greenhouse gas methane. This thesis has explored how 'dead zones' change and develop during oxygen shifts and that re-oxygenation of ‘dead zones’ could bring favorable conditions in the sediment surface for reestablishment of new micro- and macroorganism communities.

Abstract [sv]

Arealerna av 'döda bottnar' i Östersjön har ökat som en följd av industrialiseringen och användandet av gödningsmedel. Föroreningen av Östersjöns kust och öppna vatten med näringsämnen leder till en ökad tillväxt av algblomningar. En del av dessa alger sjunker till havsbotten och orsakar att så kallad hypoxia utvecklas. Den naturliga stratifieringen av vattenkolummen avgränsar yt- och bottenvattnet vilket leder till att bottenzonen är speciellt utsatt för syrebrist. Detta eftersom mikroorganismer i bottensedimentet använder syre och organiskt material för att leva. Hypoxia (<2 mg/L O2) och anoxia (inget syre) är dödligt för de flesta organismer och endast specialiserade organismer (vanligtvis vissa mikroorganismer) kan överleva. Det är av denna anledning dessa bottenzoner ofta kallas för 'döda bottnar'. Målet med denna avhandling var att undersöka förändringar i de mikrobiologiska samhällena vid nedbrytning av organiskt algmaterial, och undersöka vilken effekt syresättning har på ekologin i döda bottensediment i Östersjöns kust. I mer detalj studerades kemiska flöden, växt- och djurplankton, samt mikrobiologiska samhällen och deras metaboliska processer. Resultaten från fältprovtagningar och inkubationer i laboratoriet visade att nedbrytning av algmaterial i syrerikt sediment till viss del gynnade arkéer; syretillsättning av anoxiska sediment minskade det lagrade organiska materialet och ledde till ökad kläckning av djurplanktonägg; vilande kiselalger begravda i hypoxisk/anoxisk sediment var levande och vaknade vid tillförsel av ljus snarare än syre. Förändringar i mikrobiologiska samhällen vid syreförändringar var beroende av historisk exponering av syre i sedimentytan. Det observerades också att mikroorganismer anpassade till episodiska förändringar i syre gynnades. Fakultativt anaerobiska svavel/sulfidoxiderande bakteriesläkten gynnades efter syresättning av hypoxisk/anoxiskt sediment och gener involverade i omvandling av svavelämnen och kvävefixering var vanliga. Slutligen visade resultaten att syresättning reglerar metaboliska processer involverade i kretsloppen för svavel och metan. Speciellt genom processer som leder till en minskning av den gifta gasen svavelväte och växthusgasen metan. Denna avhandling har undersökt hur döda bottensediment förändras och utvecklas vid skiftande syreförhållanden och visar att syresättning av 'döda bottnar' kan skapa gynnsamma förhållanden i sedimentytan för återetablering av mikro- och makroorganismsamhällen. 

Place, publisher, year, edition, pages
Växjö: Linnaeus University Press, 2018.
Series
Linnaeus University Dissertations ; 302
Keywords [en]
Baltic Sea, sediment, oxygen, metatranscriptomics, metagenomics, 16S rRNA gene, RNA-seq, dead zone, re-oxygenation
National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
URN: urn:nbn:se:lnu:diva-69710ISBN: 9789188761002 (print)ISBN: 9789188761019 (electronic)OAI: oai:DiVA.org:lnu-69710DiVA, id: diva2:1172838
Public defence
2018-02-02, Fullriggaren, Landgången 4, Kalmar, 13:30 (English)
Opponent
Supervisors
Available from: 2018-01-12 Created: 2018-01-11 Last updated: 2024-02-19Bibliographically approved
List of papers
1. Shifts in coastal sediment oxygenation cause pronounced changes in microbial community composition and associated metabolism
Open this publication in new window or tab >>Shifts in coastal sediment oxygenation cause pronounced changes in microbial community composition and associated metabolism
2017 (English)In: Microbiome, E-ISSN 2049-2618, Vol. 5, article id 96Article in journal (Refereed) Published
Abstract [en]

Background

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.

Results

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.

Conclusions

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.

Place, publisher, year, edition, pages
BioMed Central, 2017
National Category
Ecology
Research subject
Ecology, Aquatic Ecology; Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-67205 (URN)10.1186/s40168-017-0311-5 (DOI)000407724600002 ()28793929 (PubMedID)2-s2.0-85030759622 (Scopus ID)
Projects
EcoChange
Available from: 2017-08-09 Created: 2017-08-09 Last updated: 2022-07-14Bibliographically approved
2. Oxygenation of anoxic sediments triggers hatching of zooplankton eggs
Open this publication in new window or tab >>Oxygenation of anoxic sediments triggers hatching of zooplankton eggs
2015 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 282, no 1817, article id 20152025Article in journal (Refereed) Published
Abstract [en]

Many coastal marine systems have extensive areas with anoxic sediments and it is not well known how these conditions affect the benthic-pelagic coupling. Zooplankton lay their eggs in the pelagic zone, and some sink and lie dormant in the sediment, before hatched zooplankton return to the water column. In this study, we investigated how oxygenation of long-term anoxic sediments affects the hatching frequency of dormant zooplankton eggs. Anoxic sediments from the brackish Baltic Sea were sampled and incubated for 26 days with constant aeration whereby, the sediment surface and the overlying water were turned oxic. Newly hatched rotifers and copepod nauplii (juveniles) were observed after 5 and 8 days, respectively. Approximately 1.5 × 105 nauplii per m-2 emerged from sediment turned oxic compared to 0.02 × 105 m-2 from controls maintained anoxic. This study demonstrated that re-oxygenation of anoxic sediments activated a large pool of buried zooplankton eggs, strengthening the benthic-pelagic coupling of the system. Modelling of the studied anoxic zone suggested that a substantial part of the pelagic copepod population can derive from hatching of dormant eggs. We suggest that this process should be included in future studies to understand population dynamics and carbon flows in marine pelagic systems.

National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-46523 (URN)10.1098/rspb.2015.2025 (DOI)000363485700018 ()26468249 (PubMedID)2-s2.0-84945237739 (Scopus ID)
Projects
EcoChange
Funder
Ecosystem dynamics in the Baltic Sea in a changing climate perspective - ECOCHANGE
Available from: 2015-09-28 Created: 2015-09-28 Last updated: 2023-08-31Bibliographically approved
3. Eutrophication induced early stage hypoxic ‘dead zone’ sediment releases nitrate and stimulates growth of archaea
Open this publication in new window or tab >>Eutrophication induced early stage hypoxic ‘dead zone’ sediment releases nitrate and stimulates growth of archaea
Show others...
(English)Manuscript (preprint) (Other academic)
Abstract [en]

In the Baltic Sea, two annual algal blooms occur in spring and summer. The bloom intensity is determined by nutrient concentrations in the water column, while the period depends on weather conditions. During the course of the bloom, dead cells sink to the sediment where their degradation consumes oxygen to create hypoxic zones (< 2 mg/L dissolved oxygen, referred to as ‘dead zones’). These zones prevent the establishment of benthic communities and result in fish mortality. The aim of the study was to determine how the sediment chemistry and microbial community composition changed due to phytoplankton biomass degradation by adding cyanobacterial or diatom biomass to sediment cores from an all-year round oxic coastal Baltic Sea bay. After biomass addition, some typical anaerobic microbial processes were observed such as a decrease in NO2-+NO3- in the sediment surface (0-1 cm) and iron in the underlying layer (1-2 cm). In addition, an increase in NO2-+NO3- was observed in the water phase in all incubations (including controls without addition of phytoplankton biomass). The combination of NO2-+NO3- diffusion from the sediment plus nitrification of the available NH4+ could not account for this increase. Potential nitrogen sources that could at least partially explain this discrepancy included microbial nitrogen fixation and cycling of nitrogen compounds from deeper layers of the sediment. Based on 16S rRNA gene sequences, the addition of diatom biomass caused minor changes in the relative abundance of microbial community members while cyanobacterial biomass caused a large increase in ferrous iron-oxidizing archaea. Considering that OTUs sharing lineages with acidophilic microorganisms were present, it was suggested that specific niches developed in sediment microenvironments. These findings highlight the importance of nitrogen cycling in oxic sediments and early microbial community changes in the sediment surface due to sinking phytoplankton before major hypoxia events occur. The release of nitrate into the water could potentially enhance algal blooms and facilitate the development of ‘dead zones’.

National Category
Ecology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-69708 (URN)
Available from: 2018-01-11 Created: 2018-01-11 Last updated: 2018-02-26Bibliographically approved
4. Oxygenation of Hypoxic Coastal Baltic Sea Sediments Impacts on Chemistry, Microbial Community Composition, and Metabolism
Open this publication in new window or tab >>Oxygenation of Hypoxic Coastal Baltic Sea Sediments Impacts on Chemistry, Microbial Community Composition, and Metabolism
2017 (English)In: Frontiers in Microbiology, E-ISSN 1664-302X, Vol. 8, article id 2453Article in journal (Refereed) Published
Abstract [en]

The Baltic Sea has undergone severe eutrophication during the last century, resulting in increased algal blooms and the development of hypoxic bottom waters. In this study, we sampled oxygen deficient sediment cores from a Baltic Sea coastal bay and exposed the bottom water including the sediment surface to oxygen shifts via artificial addition of air during laboratory incubation. Surface sediment (top 1 cm) from the replicate cores were sliced in the field as well as throughout the laboratory incubations and chemical parameters were analyzed along with high throughput sequencing of community DNA and RNA. After oxygenation, dissolved iron decreased in the water overlying the sediment while inorganic sulfur compounds (thiosulfate and tetrathionate) increased when the water was kept anoxic. Oxygenation of the sediment also maintained RNA transcripts attributed to sulfide and sulfur oxidation as well as nitrogen fixation in the sediment surface. Based on 16S rRNA gene and metatranscriptomic analyses it was found that oxygenation of the sediment surface caused a bloom of the Epsilonproteobacteria genus Arcobacter. In addition, the formation of a thick white film was observed that was likely filamentous zero-valent sulfur produced by the Arcobacter spp. Based on these results, sulfur cycling and nitrogen fixation that were evident in the field samples were ongoing during re-oxygenation of the sediment. These processes potentially added organic nitrogen to the system and facilitated the re-establishment of micro- and macroorganism communities in the benthic zone.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2017
National Category
Ecology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-69514 (URN)10.3389/fmicb.2017.02453 (DOI)000417698300001 ()2-s2.0-85037733019 (Scopus ID)
Available from: 2017-12-30 Created: 2017-12-30 Last updated: 2024-01-17Bibliographically approved
5. Diatoms dominate the eukaryotic metatranscriptome during spring in coastal 'dead zone' sediments
Open this publication in new window or tab >>Diatoms dominate the eukaryotic metatranscriptome during spring in coastal 'dead zone' sediments
2017 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 284, no 1864, article id 20171617Article in journal (Refereed) Published
Abstract [en]

An important characteristic of marine sediments is the oxygen concentration that affects many central metabolic processes. There has been a widespread increase in hypoxia in coastal systems (referred to as 'dead zones') mainly caused by eutrophication. Hence, it is central to understand the metabolism and ecology of eukaryotic life in sediments during changing oxygen conditions. Therefore, we sampled coastal 'dead zone' Baltic Sea sediment during autumn and spring, and analysed the eukaryotic metatranscriptome from field samples and after incubation in the dark under oxic or anoxic conditions. Bacillariophyta (diatoms) dominated the eukaryotic metatranscriptome in spring and were also abundant during autumn. A large fraction of the diatom RNA reads was associated with the photosystems suggesting a constitutive expression in darkness. Microscope observation showed intact diatom cells and these would, if hatched, represent a significant part of the pelagic phytoplankton biomass. Oxygenation did not significantly change the relative proportion of diatoms nor resulted in any major shifts in metabolic 'signatures'. By contrast, diatoms rapidly responded when exposed to light suggesting that light is limiting diatom development in hypoxic sediments. Hence, it is suggested that diatoms in hypoxic sediments are on 'standby' to exploit the environment if they reach suitable habitats.

Place, publisher, year, edition, pages
The Royal Society Publishing, 2017
Keywords
diatoms, sediment, oxygen, anoxia, metatranscriptomics
National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-68552 (URN)10.1098/rspb.2017.1617 (DOI)000412553400005 ()2-s2.0-85030782117 (Scopus ID)
Projects
EcoChange
Funder
Ecosystem dynamics in the Baltic Sea in a changing climate perspective - ECOCHANGE
Available from: 2017-11-01 Created: 2017-11-01 Last updated: 2023-08-31Bibliographically approved

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