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Microbial Ecosystem Functions Along the Steep Oxygen Gradient of the Landsort Deep, Baltic Sea
Södertörn University, School of Natural Sciences, Technology and Environmental Studies, Environmental Science.
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Through complex metabolic interactions aquatic microbial life is essential as a driver of ecosystem functions and hence a prerequisite for sustaining plant and animal life in the sea and on Earth. Despite its ecological importance, infor­mation on the complexity of microbial functions and how these are related to environmental conditions is limited. Due to climate change and eutrophication, marine areas facing oxygen depletion are increasing and predicted to continue to do so in the future. Vertically steep oxygen gradients are particularly pronoun­ced in the Baltic Sea. In this thesis, therefore, the ecosystem functions of micro­bial communities were investigated, using metagenomics, to understand how they were distributed along the steep oxygen gradient at the Landsort Deep, the deepest point of the Baltic Sea. Furthermore, microbial communities from the Lands­ort Deep transect were compared to microbial communities of other marine environments to establish whether the environment at this site resulted in a characteristic community. To reveal what microbial community functions and taxa were active in the anoxic sediment a metatranscriptomic approach was used. Results showed a marked effect of the coupled environmental parameters dissolved oxygen, salinity and temperature on distribution of taxa and par­ti­cularly community functions. Microbial communities showed functional capa­cities consistent with a copiotrophic life-style dependent on organic ma­terial sinking through the water column. The eutrophic condition with high organic load was further reflected in the metatranscriptome of the anoxic sedi­ment com­munity, which indicated active carbon mineralisation through ana­erobic hetero­trophic-autotrophic community synergism. New putative linkages between nitro­gen and- sulphur metabolisms were identified at anoxic depths. Further­more, viable Cyanobacteria in the anoxic sediment was evident from the tran­script analyses as another reflection of marine snow. High abundance and expres­­sion of integron integrases were identified as a charac­teristic feature of the Lands­ort Deep communities, and may provide these communities with a mech­an­ism for short-term-adaptation to environmental change. In summary, this thesis clearly documents what impact eutrophication and oxygen depletion have on microbial community functions. Furthermore, it specifically advances the mechanistic insight into microbial processes in anoxic deep-water sediment at both genomic and transcriptional level. Given the predicted progress of oxygen depletion in marine and brackish environments, this work advances information necessary to estimate effects on marine and in particular brackish ecosystem functions where anoxic conditions prevail.

Abstract [sv]

Mikroorganismer är essentiella för fungerande ekosystemfunktioner i akvatiska miljöer och därmed en förutsättning för övrigt växt- och djurliv på vår planet. Trots deras ekologiska nyckelroll är kunskapen om mikroorganismernas funk­tion och komplexitet samt hur dessa är relaterade till miljön begränsad. På grund av eutrofiering och klimatförändringar har marina områden som lider av syrebrist ökat och en ytterligare utbredning av marina och bräckta områden med syrebrist är predicerad i framtiden. Stora områden av Östersjön kännetecknas av vertikala syregradienter med syresatt ytvatten och anoxiskt bottenvatten. I denna avhandling undersöktes därför med metagenomik hur mikrobiella ekosystems funktioner var utbredda längs den vertikala syregradienten i Östersjöns djupaste del, Landsortsdjupet. Dessutom jämfördes de mikrobiella samhällena från Lands­­­ortsdjupet med mikrobiella samhällen från andra marina miljöer för att utröna om den karakteristiska miljön i Landsortsdjupet återspeglade de mikro­biella samhällen som lever där. För att undersöka vilka mikroorganismer samt vilka mikrobiella ekosystemfunktioner som var aktiva i det anoxiska sedimentet i Lands­ortsdjupet användes metatranskriptomik. Resultaten visade en stark kor­re­lation mellan miljöparametrarna syrehalt, salinitet och temperatur och för­del­ningen av mikrobiell taxa och i synnerhet mikrobiell funktion längs Lands­orts­djupets transekt. De mikrobiella samhällena uppvisade en funktionell kapa­citet förenlig med en livsstrategi beroende av organiskt material som sjunker genom vattenkolonnen som en konsekvens av eutrofiering. Eutrofa förhållanden med hög halt av organiskt material var även återspeglad i metatranskriptomet från det anoxiska sedimentet, som indikerade aktiv mineralisering av organiskt kol genom anaerob heterotrof-autotrof synergism. Nya möjliga kopplingar mellan kväve- och svavelmetabolism identifierades i det anoxiska vattnet. Vidare visade resultat från metatranskriptom-analys att livsdugliga cyanobakterier var abun­danta i det mörka och anoxiska sedimentet, vilket även detta kan vara en konse­kvens av sjunkande organiskt material. Hög abundans och hög transkribering av integrongener kunde identifieras som ett karakteristiskt kännetecken hos de mikro­biella samhällena i Landsortsdjupet vilket skulle kunna förse dem med en me­kanism för anpassning till miljöförändringar. Sammanfattningsvis dokumen­terar denna avhandling tydligt vilken påverkan eutrofiering och syrebrist har på mikrobiella funktioner. Dessutom för den specifikt kunskapen om mikrobiella processer i anoxiska djupvattensediment framåt på både genom- och transkrip­tions­nivå. Mot bakgrund av en predicerad ökning av syrebristen i marina mil­jöer, bidrar denna avhandling med information som är viktig för att kunna förutse vilka effekter anoxiska förhållanden kan komma att få på ekosystemfunktioner i marina miljöer och i brackvattenmiljöer i synnerhet.

Place, publisher, year, edition, pages
Huddinge: Södertörns högskola, 2016. , p. 63
Series
Södertörn Doctoral Dissertations, ISSN 1652-7399 ; 125
Keyword [en]
microbial ecology, ecosystem functions, microbial community, bacteria, archaea, metagenomics, metatranscriptomics, oxygen gradient, hypoxia, sediment, Baltic Sea
National Category
Environmental Sciences
Research subject
Environmental Studies; Baltic and East European studies
Identifiers
URN: urn:nbn:se:sh:diva-30910Local ID: 1169/42/2007:17ISBN: 978-91-87843-58-7 (print)ISBN: 978-91-87843-59-4 (electronic)OAI: oai:DiVA.org:sh-30910DiVA, id: diva2:974622
Public defence
2016-11-18, MA636, Alfred Nobels allé 7, Huddinge, 10:00 (English)
Opponent
Supervisors
Funder
The Foundation for Baltic and East European Studies, 1169/42/2007:17EU, FP7, Seventh Framework Programme, 222625
Available from: 2016-10-14 Created: 2016-09-27 Last updated: 2017-03-03Bibliographically approved
List of papers
1. A Metagenomics Transect into the Deepest Point of the Baltic Sea Reveals Clear Stratification of Microbial Functional Capacities
Open this publication in new window or tab >>A Metagenomics Transect into the Deepest Point of the Baltic Sea Reveals Clear Stratification of Microbial Functional Capacities
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2013 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 9, article id e74983Article in journal (Refereed) Published
Abstract [en]

The Baltic Sea is characterized by hyposaline surface waters, hypoxic and anoxic deep waters and sediments. These conditions, which in turn lead to a steep oxygen gradient, are particularly evident at Landsort Deep in the Baltic Proper. Given these substantial differences in environmental parameters at Landsort Deep, we performed a metagenomic census spanning surface to sediment to establish whether the microbial communities at this site are as stratified as the physical environment. We report strong stratification across a depth transect for both functional capacity and taxonomic affiliation, with functional capacity corresponding most closely to key environmental parameters of oxygen, salinity and temperature.

We report similarities in functional capacity between the hypoxic community and hadal zone communities, underscoring the substantial degree of eutrophication in the Baltic Proper. Reconstruction of the nitrogen cycle at Landsort deep shows potential for syntrophy between archaeal ammonium oxidizers and bacterial denitrification at anoxic depths, while anaerobic ammonium oxidation genes are absent, despite substantial ammonium levels below the chemocline. Our census also reveals enrichment in genetic prerequisites for a copiotrophic lifestyle and resistance mechanisms reflecting adaptation to prevalent eutrophic conditions and the accumulation of environmental pollutants resulting from ongoing anthropogenic pressures in the Baltic Sea.

Keyword
miljömikrobiologi, metagenomik, ekosystemfunktioner, eutrofiering, Östersjön, sediment
National Category
Ecology
Research subject
Environmental Studies; Baltic and East European studies
Identifiers
urn:nbn:se:sh:diva-20021 (URN)10.1371/journal.pone.0074983 (DOI)000326520200065 ()24086414 (PubMedID)2-s2.0-84884517639 (Scopus ID)1169/42/2007:17 (Local ID)1169/42/2007:17 (Archive number)1169/42/2007:17 (OAI)
Funder
The Foundation for Baltic and East European Studies, 1169/42/2007:17
Available from: 2013-10-24 Created: 2013-10-24 Last updated: 2017-12-06Bibliographically approved
2. A dark, anoxic mausoleum for DNA: perceived and actual community structure in the Landsort Deep sediment, the Baltic Sea
Open this publication in new window or tab >>A dark, anoxic mausoleum for DNA: perceived and actual community structure in the Landsort Deep sediment, the Baltic Sea
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2016 (English)In: PeerJ, ISSN 2167-8359, E-ISSN 2167-8359Article in journal (Other academic) Submitted
Abstract [en]

Numerous investigations of bacterial communities using sequence analysis of environmental DNA have revealed extensive diversity of microbial taxa in an array of different environmental habitats. Community analysis based solely on DNA, however, does not reveal whether the detected community members are actively contributing to community functioning, or whether they are dormant or remnants of dead cells. This dilemma is of particular concern when analyzing microbial community structure of sites with a high degree of deposited matter, such as marine sediments. For example, the Baltic Sea’s deepest point, the Landsort Deep, consists of anoxic sediments with a large deposition of allochthonous organic matter from the highly stratified 460 m water column above. Our previous metagenomics results indicated the presence of potential obligately aerobic and phototrophic microorganisms. To further elucidate which taxa may contribute to ecosystem function at this site, we here present three different datasets – rDNA amplicons, rDNA reads from a shotgun metagenome and expressed rRNA from a shotgun metatranscriptome. By comparing the three datasets and the ratios between rRNA and rDNA we seek to estimate the protein synthesis potential of the community members in order to provide an indication of what taxa may have cellular activity and metabolic potential. The variation in protein synthesis potential was large, both within and between taxa, in the sediment community. Many typically anaerobic taxa, e.g. from Deltaproteobacteria and Euryarchaeota, showed a high protein synthesis potential, while typical aerobes like Flavobacteria showed a low protein synthesis potential. More surprisingly, some common Baltic Sea surface water bacteria also displayed a high protein synthesis potential, suggesting they have an active role in the anoxic sediment ecosystem at 460 m depth. Both filamentous and unicellular Cyanobacteria exhibited very high protein synthesis potential, which implies a more complex role of these bacteria in carbon cycling in the Baltic Sea than previously suggested. Moreover, Mycobacteria, that were abundant in Landsort Deep sediment metagenome compared with other marine sediment metagenomes, showed protein synthesis potentials consistent with a functional role in the sediment community. Our results provide a new window of insight into the complexities of the microbial community of Landsort Deep with implications for the understanding of other anoxic accumulation sediments.

Keyword
Anoxic accumulation sediment, Tag sequencing, Protein synthesis potential, Dormancy, Microbial activity, rDNA, rRNA, Amplicon
National Category
Environmental Sciences
Research subject
Environmental Studies; Baltic and East European studies
Identifiers
urn:nbn:se:sh:diva-30915 (URN)
Note

Som manuskript i avhandling. As manuscript in dissertation.

Available from: 2016-10-07 Created: 2016-09-28 Last updated: 2017-11-30Bibliographically approved
3. Reconstructing ecosystem functions of the active microbial community of the Baltic Sea oxygen depleted sediments
Open this publication in new window or tab >>Reconstructing ecosystem functions of the active microbial community of the Baltic Sea oxygen depleted sediments
2016 (English)In: PeerJ, ISSN 2167-8359, E-ISSN 2167-8359, Vol. 4, article id e1593Article in journal (Refereed) Published
Abstract [en]

Baltic Sea deep water and sediments hold one of the largest anthropogenically induced hypoxic areas in the world. High nutrient input and low water exchange result in eutrophication and oxygen depletion below the halocline. As a consequence at Landsort Deep, the deepest point of the Baltic Sea, anoxia in the sediments has been a persistent condition over the past decades. Given that microbial communities are drivers of essential ecosystem functions we investigated the microbial community metabolisms and functions of oxygen depleted Landsort Deep sediments by metatranscriptomics. Results show substantial expression of genes involved in protein metabolism demonstrating that the Landsort Deep sediment microbial community is active. Identified expressed gene suites of metabolic pathways with importance for carbon transformation including fermentation, dissimilatory sulphate reduction and methanogenesis were identified. The presence of transcripts for these metabolic processes suggests a potential for heterotrophic-autotrophic community synergism and indicates active mineralisation of the organic matter deposited at the sediment as a consequence of the eutrophication process. Furthermore, cyanobacteria, probably deposited from the water column, are transcriptionally active in the anoxic sediment at this depth. Results also reveal high abundance of transcripts encoding integron integrases. These results provide insight into the activity of the microbial community of the anoxic sediment at the deepest point of the Baltic Sea and its possible role in ecosystem functioning.

National Category
Environmental Sciences Biological Sciences
Research subject
Environmental Studies; Baltic and East European studies
Identifiers
urn:nbn:se:sh:diva-29454 (URN)10.7717/peerj.1593 (DOI)000368413200005 ()26823996 (PubMedID)2-s2.0-84955558214 (Scopus ID)
Funder
The Foundation for Baltic and East European Studies, 1169/42/2007:17Stockholm County Council
Available from: 2016-02-05 Created: 2016-02-05 Last updated: 2017-11-30Bibliographically approved

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