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Microbial adaptations and controlling mechanisms of surface-associated microhabitat heterogeneity in aquatic systems
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology.
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Habitat heterogeneity is a driving factor for speciation and ecosystem functioning and is well studied in macro-ecology. Yet our understanding of microbial adaptations, and governing processes is incomplete. The here presented thesis aims at giving us a better understanding of patterns in micro-heterogeneity, and microbial adaptations to such heterogeneity with particular focus on surface-dominated, aquatic habitats. The most prominent microbial adaptation to surface associated mode of life is biofilm formation. Biofilms rely heavily on type IV pili. These pili systems are well studied in Bacteria, but largely unknown in Archaea. Therefore, the first part of this thesis focuses on resolving genetic and structural feature of the type IV like aap-pilus of the thermo-acidophilic Sulfolobus acidocaldarius. We found the aap-pilus to be indispensible for biofilm formation, and to be unparalleled in variability of its quaternary structure and cross regulation with other filaments. The second part of this thesis investigates particle colonization in the water column, focusing on diatoms as a model system, allowing an in situ assessment of different stages of particle colonization, and potential particle-specificity of the associated bacterial community. Opposing reports from marine systems, we did not observe diatom-specificity in the associated bacterial community. Instead we found bacterial community subsets, one likely originating from sediment resuspension, and the other being controlled by biofilm-forming populations (e.g. Flexibacter), able to attach to newly formed particle surfaces and subsequently facilitate secondary colonization by other bacteria. Finally, the habitat heterogeneity in top-layers of lake sediments were investigated in experimental microcosms. Cell-specific oxygen consumption rates were determined, to assess microbial activity across different scales. Individual activity rates differed strongly across all investigated scales, likely due to spatially heterogeneous distribution of nutrients with differing quality. Vice versa, the influence of microbial activity on micro-habitat-heterogeneity was investigated. We correlated sediment redox-state with bacterial community composition and populations. Our results indicate that habitat heterogeneity is generally beneficial for microorganism, and greater heterogeneity results in greater bacterial diversity. However, this heterogeneity-diversity relationship is limited and microorganisms actively stabilize their immediate redox environment to a preferred, community-specific, stable state, if cell abundances exceed a minimum threshold.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2015. , 69 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1296
Keyword [en]
microbial habitat heterogeneity
National Category
Biological Sciences
Research subject
Biology with specialization in Limnology
Identifiers
URN: urn:nbn:se:uu:diva-263206ISBN: 978-91-554-9351-6 (print)OAI: oai:DiVA.org:uu-263206DiVA: diva2:857707
Public defence
2015-11-20, Ekman Salen, Norbyvägen 14, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2015-10-27 Created: 2015-09-28 Last updated: 2015-11-10
List of papers
1. Structure and function of the adhesive type IV pilus of Sulfolobus acidocaldarius
Open this publication in new window or tab >>Structure and function of the adhesive type IV pilus of Sulfolobus acidocaldarius
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2012 (English)In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 14, no 12, 3188-3202 p.Article in journal (Refereed) Published
Abstract [en]

Archaea display a variety of type IV pili on their surface and employ them in different physiological functions. In the crenarchaeon Sulfolobus acidocaldarius the most abundant surface structure is the aap pilus (archaeal adhesive pilus). The construction of in frame deletions of the aap genes revealed that all the five genes (aapA, aapX, aapE, aapF, aapB) are indispensible for assembly of the pilus and an impact on surface motility and biofilm formation was observed. Our analyses revealed that there exists a regulatory cross-talk between the expression of aap genes and archaella (formerly archaeal flagella) genes during different growth phases. The structure of the aap pilus is entirely different from the known bacterial type IV pili as well as other archaeal type IV pili. An aap pilus displayed 3 stranded helices where there is a rotation per subunit of ∼ 138° and a rise per subunit of ∼ 5.7 Å. The filaments have a diameter of ∼ 110 Å and the resolution was judged to be ∼ 9 Å. We concluded that small changes in sequence might be amplified by large changes in higher-order packing. Our finding of an extraordinary stability of aap pili possibly represents an adaptation to harsh environments that S. acidocaldarius encounters.

National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-192617 (URN)10.1111/j.1462-2920.2012.02898.x (DOI)
Available from: 2013-01-23 Created: 2013-01-23 Last updated: 2017-12-06Bibliographically approved
2. Bacterial communities shaping the redox environment in top-layer sediments of an oligotrophic high latitude lake
Open this publication in new window or tab >>Bacterial communities shaping the redox environment in top-layer sediments of an oligotrophic high latitude lake
(English)Manuscript (preprint) (Other academic)
Keyword
Electromicrobiology, Bacteria, Microsensors, Redox potential, Lake Sediments
National Category
Biological Sciences
Research subject
Biology with specialization in Limnology
Identifiers
urn:nbn:se:uu:diva-263205 (URN)
Available from: 2015-09-28 Created: 2015-09-28 Last updated: 2017-01-25Bibliographically approved
3. Population-linkages in freshwater bacterial communities associated with individual diatoms and particles
Open this publication in new window or tab >>Population-linkages in freshwater bacterial communities associated with individual diatoms and particles
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(English)Manuscript (preprint) (Other academic)
Keyword
Freshwater, Diatom, Bacteria community composition, Colonization, Network, Single particle analysis
National Category
Natural Sciences
Research subject
Biology with specialization in Limnology
Identifiers
urn:nbn:se:uu:diva-263204 (URN)
Available from: 2015-09-28 Created: 2015-09-28 Last updated: 2017-01-25Bibliographically approved
4. Microscale decoupling of sediment oxygen consumption and microbial biomass in an oligotrophic lake
Open this publication in new window or tab >>Microscale decoupling of sediment oxygen consumption and microbial biomass in an oligotrophic lake
2016 (English)In: Freshwater Biology, ISSN 0046-5070, E-ISSN 1365-2427, Vol. 61, no 9, 1477-1491 p.Article in journal (Refereed) Published
Abstract [en]

Sediments of aquatic ecosystems are hotspots for biological activity. Here, we address the question if, within surface sediments, oxygen consumption is linearly related to cell abundance. In addition, we identify habitat-specific factors influencing underlying microbial processes. Sediment microcosms were established from three sites within oligotrophic Lake angstrom nnsjon, Sweden, to use microsensors for measuring oxygen profiles and estimate spatially resolved oxygen consumption rates at the water-sediment interfaces. To evaluate differences between habitats, we measured sediment carbon content and C:N:P as a proxy for diagenetic state and organic matter bioavailability. Epifluorescence microscopy was used to assess the microscale distribution and size of surface-colonising microorganisms. There was no linear correlation between oxygen consumption rates and microbial cell abundances. Cell-specific respiration rates were highest in the profundal compared to the littoral- and inflow-sediment microcosms, whereas vertical variability in all these parameters was highest at the inflow, intermediate in the littoral and least variable in profundal sediments. Illumina sequencing of spatially resolved 16SrRNA genes was used to test for possible influence of bacterial diversity on spatially resolved oxygen consumption rates. Bacterial -diversity decreased over depth at each site, but was also lower in sediments from the most active profundal zones of the lake compared to the inflow. We suggest that bacteria in profundal sediments mainly use highly oxidised organic compounds, resulting in overall low growth yield despite high metabolic activity. In the lake inflow and the littoral, more reduced organic substrates of terrestrial origin are used at lower rates but with higher yield.

Keyword
Cell-specific respiration, Sediment microbiology, Macro- and Microenvironment heterogeneity, Environmental Microbiology
National Category
Microbiology Ecology
Research subject
Biology with specialization in Limnology
Identifiers
urn:nbn:se:uu:diva-261278 (URN)10.1111/fwb.12787 (DOI)000380902400010 ()
External cooperation:
Funder
Swedish Research CouncilSwedish Research Council Formas
Available from: 2015-09-28 Created: 2015-09-01 Last updated: 2017-12-01Bibliographically approved

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