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Structure and function of microbial communities in acid sulfate soil and the terrestrial deep biosphere
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Centre for Ecology and Evolution in Microbial Model Systems (EEMiS))
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

This thesis describes the use of different DNA sequencing technologies to investigate the structure and function of microbial communities in two extreme environments, boreal acid sulfate soil and the terrestrial deep biosphere.

The first of the two investigated environments was soils containing un-oxidized metal sulfides that are termed ‘potential acid sulfate soil’ (PASS) materials. If these materials are exposed to atmospheric oxygen by either natural phenomena (e.g., land uplift) or human activities (e.g., drainage) then the metal sulfides become oxidized and the PASS becomes acidic and is defined as an ‘acid sulfate soil’ (ASS). The resulting acid and metal release from metal sulfide oxidation can lead to severe environmental damage. Although acidophilic microorganisms capable of catalyzing acid and metal release have been identified from many sulfide mineral containing environments, the microbial community of boreal PASSs/ASSs remains unclear. This study investigated the physicochemical and microbial characteristics of PASSs and ASSs from the Risöfladan experimental field in Vasa, Finland. Sanger sequencing of 16S rRNA gene sequences of microorganisms present in the PASSs and ASSs were mostly assigned to acidophilic species and environmental clones previously identified from acid- and metal-contaminated environments. Enrichment cultures inoculated from the ASS demonstrated that the acidophilic microorganisms were responsible for catalyzing acid and metal release from PASSs/ASSs. Lastly, the study investigated how to mitigate metal sulfide oxidation and the concomitant formation of sulfuric acid by treating ASSs in situ with CaCO3 or Ca(OH)2 suspensions. The DNA sequencing still identified acidophilic microorganisms after the chemical treatments. However, the increased pH during and after treatment suggested that the activity of the acidophiles might be inhibited. This study was the first to identify the microbial community present in boreal PASSs/ASSs and suggested that treatment with basic compounds may inhibit microbial catalysis of metal sulfide dissolution.

The second studied environment was the deep, dark terrestrial subsurface that is suggested to be both extremely stable and highly oligotrophic. Despite the scarcity of carbon and energy sources, the deep biosphere is estimated to constitute up to 20% of the total biomass on earth and thus, represents the largest microbial ecosystem. However, due to the difficulties of accessing this environment and our inability to cultivate the indigenous microbial populations, details of the diversity and metabolism of these communities remain largely unexplored. This study was carried out at Äspö Hard Rock Laboratory, Sweden and utilized second-generation sequencing to identify the taxonomic composition and genetic potential of planktonic and biofilm populations. Community DNA sequencing of planktonic cells from three water types at varied age and depth (‘modern marine’, ‘undefined mixed’, and ‘old saline’) showed the existence of ultra-small cells capable of passing through a 0.22 μm filter that were phylogenetically distinct communities from the >0.22 μm fraction. The reduced cell size and/or genome size suggested a potential adaptation to the oligotrophic environment in the terrestrial deep biosphere. The identified planktonic communities were dominated by Proteobacteria, Candidate divisions, unclassified archaea, and unclassified bacteria. Functional analysis of the assembled genomes showed that the planktonic population from the shallow modern marine water demonstrated a predominantly anaerobic and heterotrophic lifestyle. In contrast, the deeper, old saline water was more closely aligned with the hypothesis of a hydrogen-driven deep biosphere. Metagenomic analysis of subsurface biofilms from ‘modern marine’ and ‘old saline’ water types suggested only a subset of populations were involved in initial biofilm formation. The identified biofilm populations from both water types were distinct from the planktonic community and were suggested to be dominated by hydrogen fed, chemolithoautotrophic and diazotrophic populations.

Place, publisher, year, edition, pages
Växjö: Linnaeus University Press, 2016. , 146 p.
Series
Linnaeus University Dissertations, 255/2016
Keyword [en]
molecular phylogeny, acid sulfate soils, metal, acidophiles, deep biosphere, oligotrophy, biofilm formation, metagenome, binning, metabolism
National Category
Ecology
Research subject
Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-52538Libris ID: 19478031ISBN: 978-91-88357-22-9 (print)OAI: oai:DiVA.org:lnu-52538DiVA: diva2:929156
Public defence
2016-06-17, Hörsalen Fullriggaren, Landgången 4, Kalmar, 09:30 (English)
Opponent
Supervisors
Available from: 2016-05-20 Created: 2016-05-17 Last updated: 2016-11-22Bibliographically approved
List of papers
1. Microbial community potentially responsible for acid and metal release from an Ostrobothnian acid sulfate soil
Open this publication in new window or tab >>Microbial community potentially responsible for acid and metal release from an Ostrobothnian acid sulfate soil
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2013 (English)In: FEMS Microbiology Ecology, ISSN 0168-6496, E-ISSN 1574-6941, Vol. 84, no 3, 555-563 p.Article in journal (Refereed) Published
Abstract [en]

Soils containing an approximately equal mixture of metastable iron sulfides and pyrite occur in the boreal Ostrobothnian coastal region of Finland, termed 'potential acid sulfate soil materials'. If the iron sulfides are exposed to air, oxidation reactions result in acid and metal release to the environment that can cause severe damage. Despite that acidophilic microorganisms catalyze acid and metal release from sulfide minerals, the microbiology of acid sulfate soil (ASS) materials has been neglected. The molecular phylogeny of a depth profile through the plough and oxidized ASS layers identified several known acidophilic microorganisms and environmental clones previously identified from acid- and metal-contaminated environments. In addition, several of the 16S rRNA gene sequences were more similar to sequences previously identified from cold environments. Leaching of the metastable iron sulfides and pyrite with an ASS microbial enrichment culture incubated at low pH accelerated metal release, suggesting microorganisms capable of catalyzing metal sulfide oxidation were present. The 16S rRNA gene analysis showed the presence of species similar to Acidocella sp. and other clones identified from acid mine environments. These data support that acid and metal release from ASSs was catalyzed by indigenous microorganisms adapted to low pH.

National Category
Microbiology
Research subject
Natural Science, Microbiology
Identifiers
urn:nbn:se:lnu:diva-26021 (URN)10.1111/1574-6941.12084 (DOI)000318932300010 ()23369102 (PubMedID)2-s2.0-84877704320 (Scopus ID)
Available from: 2013-06-03 Created: 2013-06-03 Last updated: 2017-12-06Bibliographically approved
2. Impact of mitigation strategies on acid sulfate soil chemistry and microbial community
Open this publication in new window or tab >>Impact of mitigation strategies on acid sulfate soil chemistry and microbial community
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2015 (English)In: Science of the Total Environment, ISSN 0048-9697, E-ISSN 1879-1026, Vol. 526, 215-221 p.Article in journal (Refereed) Published
Abstract [en]

Potential acid sulfate soils contain reduced iron sulfides that if oxidized, can cause significant environmental damage by releasing large amounts of acid and metals. This study examines metal and acid release as well as the microbial community capable of catalyzing metal sulfide oxidation after treating acid sulfate soil with calcium carbonate (CaCO3) or calcium hydroxide (Ca(OH)2). Leaching tests of acid sulfate soil samples were carried out in the laboratory. The pH of the leachate during the initial flushing with water lay between 3.8 and 4.4 suggesting that the jarosite/schwertmannite equilibrium controls the solution chemistry. However, the pH increased to circa 6 after treatment with CaCO3 suspension and circa 12 after introducing Ca(OH)2 solution. 16S rRNA gene sequences amplified from community DNA extracted from the untreated and both CaCO3and Ca(OH)2 treated acid sulfate soils were most similar to bacteria (69.1% to 85.7%) and archaea (95.4% to 100%) previously identified from acid and metal contaminated environments. These species included a Thiomonas cuprina-like and an Acidocella-like bacteria as well as a Ferroplasma acidiphilum-like archeon. Although the CaCO3 and Ca(OH)2 treatments did not decrease the proportion of microorganisms capable of accelerating acid and metal release, the chemical effects of the treatments suggested their reduced activity.

Keyword
Acid sulfate soil, Acid, Metal, Molecular phylogeny, Acidophile
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-50208 (URN)10.1016/j.scitotenv.2015.04.049 (DOI)000356224100021 ()25933291 (PubMedID)2-s2.0-84928744474 (Scopus ID)
Available from: 2016-03-04 Created: 2016-03-04 Last updated: 2017-11-30Bibliographically approved
3. Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations
Open this publication in new window or tab >>Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations
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2016 (English)In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 10, no 5, 1192-1203 p.Article in journal (Refereed) Published
Abstract [en]

Microorganisms in the terrestrial deep biosphere host up to 20% of the earth's biomass and are suggested to be sustained by the gases hydrogen and carbon dioxide. A metagenome analysis of three deep subsurface water types of contrasting age (from <20 to several thousand years) and depth (171 to 448 m) revealed phylogenetically distinct microbial community subsets that either passed or were retained by a 0.22 μm filter. Such cells of <0.22 μm would have been overlooked in previous studies relying on membrane capture. Metagenomes from the three water types were used for reconstruction of 69 distinct microbial genomes, each with >86% coverage. The populations were dominated by Proteobacteria, Candidate divisions, unclassified archaea and unclassified bacteria. The estimated genome sizes of the <0.22 μm populations were generally smaller than their phylogenetically closest relatives, suggesting that small dimensions along with a reduced genome size may be adaptations to oligotrophy. Shallow 'modern marine' water showed community members with a predominantly heterotrophic lifestyle. In contrast, the deeper, 'old saline' water adhered more closely to the current paradigm of a hydrogen-driven deep biosphere. The data were finally used to create a combined metabolic model of the deep terrestrial biosphere microbial community.

National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-49416 (URN)10.1038/ismej.2015.185 (DOI)000374377200016 ()26484735 (PubMedID)2-s2.0-84944910110 (Scopus ID)
Available from: 2016-01-29 Created: 2016-01-29 Last updated: 2017-11-30Bibliographically approved
4. Hydrogen fed chemolithoautotrophic and diazotrophic populations initiate biofilm formation in oligotrophic, deep terrestrial subsurface waters
Open this publication in new window or tab >>Hydrogen fed chemolithoautotrophic and diazotrophic populations initiate biofilm formation in oligotrophic, deep terrestrial subsurface waters
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(English)Manuscript (preprint) (Other academic)
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-52537 (URN)
External cooperation:
Available from: 2016-05-17 Created: 2016-05-17 Last updated: 2016-11-30Bibliographically approved

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