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Environmental filtering of bacteria in low productivity habitats
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology. Department of Environmental Microbiology, Helmholtz Centre for Environmental Research – UFZ, Microbial Ecosystem Services Group, Leipzig, Germany. (Department of Ecology and Genetics, Limnology Uppsala University, Uppsala, Sweden)
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Microbes fulfill important ecosystem functions by contributing as drivers of global nutrient cycles. Their distribution patterns are mainly controlled by environmental heterogeneities. So far, little is known about the mode of action of particular environmental drivers on the microbiota, particularly in low productivity habitats.

The aim of this thesis was to investigate the relationships between local environmental drivers and the microbial responses at the level of communities, individuals and realized function, using three structurally different model habitats sharing the feature of overall low productivity. Using a hypothesis-based approach and extensive 16S rRNA amplicon mapping of bacterioplankton colonizing the polar Southern Ocean, I identified how the seasonal formation of open-water polynyas and coupled phytoplankton production affected the diversity of surface bacterial communities and resulted in a cascading effect influencing the underlying dark polar water masses. Additional laboratory experiments, with cultures exposed to light, resulted in reduction in alpha diversity and promoted opportunistic populations with most bacterial populations thriving in the cultures typically reflected the dominants in situ.

Furthermore it was experimentally tested how induced cyclic water table fluctuations shaping environmental heterogeneity in a constructed wetland on temporal scale, by directly affecting redox conditions. Twelve months of water table fluctuations resulted in enhanced microbial biomass, however a shift in community composition did not lead to a significant increase in pollutant removal efficiency when compared to a static control wetland. I detected phyla that have previously been proposed as key players in anaerobic benzene break-down using a protocol that was developed for single cell activity screening using isotope-substrate uptake and microautoradiography combined with taxonomic identification based on fluorescent in situ hybridization targeting the 16S rRNA. Eventually, I provide an example of how anthropogenic pollution with polyaromatic hydrocarbons induced a strong environmental filtering on intrinsic microbial communities in lake sediments.

In conclusion, my studies reveal that microorganisms residing in low productivity habitats are greatly influenced by environmental heterogeneity across both spatial and temporal scales. However, such variation in community composition or overall abundance does not always translate to altered community function.

 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2014. , 44 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1157
Keyword [en]
bacteria, environmental filtering, diversity, ecosystem service, hydrocarbon utilization, Southern Ocean, sediment
National Category
Natural Sciences Biological Sciences
Research subject
Biology with specialization in Microbiology
Identifiers
URN: urn:nbn:se:uu:diva-229144ISBN: 978-91-554-8986-1 (print)OAI: oai:DiVA.org:uu-229144DiVA: diva2:735861
Public defence
2014-09-16, Fries salen, Evolutionsbiologiskt centrum, EBC, Norbyvägen 18, 752 36 Uppsala, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2014-08-26 Created: 2014-08-01 Last updated: 2014-09-08
List of papers
1. Spatial patterns of marine bacterioplankton along gradients of primary production in the Amundsen Sea Polynya, Southern Ocean
Open this publication in new window or tab >>Spatial patterns of marine bacterioplankton along gradients of primary production in the Amundsen Sea Polynya, Southern Ocean
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

During austral summers, the Southern Ocean's biota experience a sharp increase in primary production and a steepening of biotic and abiotic gradients, resulting from increased solar radiation and retreating ice.  In one of the largest ice-free patches - the Amundsen Sea Polynya - we aimed to identify connections between spatial diversity patterns of heterotrophic bacterioplankton and gradients of phytoplankton biomass. We gathered samples from throughout the depth profile at 15 sites during the austral summer of 2010/2011, collecting bacterioplankton and measuring several biotic and abiotic factors in the surrounding seawater.  We assessed bacterial community structure by targeting the 16S rRNA gene for pyrosequencing. Our overall goal was to identify patterns of spatial diversity in heterotrophic bacterioplankton and to generate and test mechanistic hypotheses for bacterioplankton community structure related to phytoplankton biomass, biotic and abiotic nutrients, and hydrological relationships due to depth and water mass.

We found that processes acting within the photic surface related to the level of phytoplankton biomass induce a strong filtering effect by decreasing bacterioplankton community richness while increasing bacterioplankton abundance as phytoplankton biomass increases. We also found that the bacterioplankton community in the photic surface represents a subset of that found in the underlying dark water masses, likely reformed annually as the polynya appears; bacterial communities in surface waters reflect the communities found beneath, though as phytoplankton biomass increases, the similarity of these communities between different sites within the polynya increases, likely due to the filtering effect. The high phytoplankton biomass in the photic surface represents an important pool of organic matter and inorganic nutrients, fueling the underlying dark water with nutrients in a cascading effect; we found that in contrast to the community response in shallower water, the bacterioplankton community at the bottom of the phytoplankton biomass increased in diversity as phytoplankton biomass in overlying waters increased, while deeper waters remained largely unaffected. We propose that this lack of, response in deeper water masses gives rise to the observed high group dispersal in bacterial community composition in all water masses and the relatively homogenous community in the bottom water mass.

Keyword
marine bacterioplankton, community dynamics, Southern Ocean
National Category
Biological Sciences
Research subject
Biology with specialization in Microbiology
Identifiers
urn:nbn:se:uu:diva-229137 (URN)
Funder
Swedish Research Council
Available from: 2014-08-01 Created: 2014-08-01 Last updated: 2015-05-07
2. The impact of light and water mass on bacterial population dynamics in the Amundsen Sea Polynya
Open this publication in new window or tab >>The impact of light and water mass on bacterial population dynamics in the Amundsen Sea Polynya
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Although the Antarctic Ocean is perpetually cold, mostly ice-covered and dark, it is a highly productive and diverse marine ecosystem. During austral summer, ice-free patches (polynyas) form, exposing marine organisms to sunlight, while mobilizing large amounts of nutrients from the melting ice. As a result, intense phytoplankton blooms form that sustain life across the entire Antarctic food web. This seasonality is likely to shape microbial communities, but the main environmental drivers controlling these communities and the biogeochemical processes they mediate are largely unknown.

In this study, the remote Amundsen Sea Polynya (ASP) was used as a model system to identify the influence of some of the most important environmental drivers of the Southern Ocean. We studied the dynamics in occurrence and activity of abundant members of the bacterioplankton community, directly in environmental samples as well as in microcosm experiments, by using next-generation sequencing of bar-coded 16S rRNA genes in combination with immunochemical detection of DNA-synthesis using bromodeoxyuridine as a tracer.

We found that the photic zone harbored a bacterioplankton community with a low species richness. Here, the dominant populations were related to taxa known to benefit from high organic carbon and nutrient loads (copiotrophs). In contrast, the dark water masses below the photic zone hosted bacterial communities of higher richness, and were dominated by oligotrophs. Results from enrichment studies suggested that indirect impacts of light via photosynthetic production and competition for dissolved nutrients provided in the water masses are the two main factors shaping bacterial communities of the ASP.

Keyword
marine bacterioplankton, population dynamics, Southern Ocean
National Category
Biological Sciences
Research subject
Biology with specialization in Microbiology
Identifiers
urn:nbn:se:uu:diva-229138 (URN)
Available from: 2014-08-01 Created: 2014-08-01 Last updated: 2014-09-08
3. The effect of water table fluctuation on microbial benzene utilization in a constructed wetland
Open this publication in new window or tab >>The effect of water table fluctuation on microbial benzene utilization in a constructed wetland
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Microbial degradation of benzene in anoxic habitats is so low that it’s hardly detectable. In this study benzene-utilizing taxa residing in a mostly anoxic wetland were identified and visualized by applying single-cell techniques and phylogenetic identification based on 16S rRNA amplicon sequencing. We also tested whether cyclic water table fluctuations had a positive effect on benzene removal rates.

We found that cyclic water table changes in a constructed wetland with horizontal water flow created fluctuations in redox conditions and resulted in an increase of microbial biomass. However, it did not enhance the removal of recalcitrant hydrocarbon contaminants, at least not within one year of operation. Benzene remained persistent, despite the increased microbial biomass. A slight decrease in ammonia and nitrate concentrations may hint towards an increase in microbial denitrification as a result of the artificially induced hydrodynamic changes.

Despite the low benzene uptake rates, we successfully visualized and identified anaerobic benzene-degrading microbes, by using 14C-benzene-Microautoradiography (MAR) and Catalyzed Reporter Deposition Fluorescence in situ Hybridization (CARD-FISH) with a probe set targeting proposed anaerobic benzene-utilizers. We found Deltaproteobacteria, Firmicutes, Archaea and Azoarcus (Betaproteobacteria) to actively take up benzene anaerobically

Our MAR-CARD-FISH protocol can be applied to visualize benzene- or other aromatic hydrocarbon-utilizing microbes in contaminated sediments and soils and can help to reveal physical associations of different taxa involved in the recalcitrant hydrocarbon break-down.

Keyword
constructed wetland, benzene, anoxic, bacteria, fluctuation
National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-229139 (URN)
Available from: 2014-08-01 Created: 2014-08-01 Last updated: 2014-09-08
4. Bacterial communities in a tar-contaminated lake sediment
Open this publication in new window or tab >>Bacterial communities in a tar-contaminated lake sediment
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Organic anthropogenic pollutants, such as polycyclic aromatic hydrocarbons (PAHs) are widespread in nature and even low concentrations can be harmful for many organisms. To assess if also microbiota residing in freshwater sediments respond to such contaminants a lake sediment adjacent to the former discharge of a factory that conducted tar distillation in the early 20th century in central Sweden were studied. We compared the bacterial community composition (BCC) at sites affected by high tar loads to BCC in a linked, but pristine sediment, and a downstream site that is likely influenced by regular diffusive loads of PAHs. PAH and VOC (Volatile Organic Carbon) concentrations were analyzed whereas sediment aliquots were used for molecular identification of the local BCC. Here we took the opportunity to compare the bacteria abundance-data retrieved from two distinct approaches; two OTU tables were generated based on either paired-end MiSeq Illumina 16S rRNA gene amplicon sequencing or direct HiSeq Illumina-based metagenome sequencing of sediment DNA extracts. Both methods revealed that the high PAH loads adjacent to the tar factory significantly alters the BCC compared to the less affected sites, even though they both partly result in contrasting outcome. The highly contaminated sediments hosted a bacterial community that was low in richness, featuring taxa known to colonize habitats with high PAH loads. For instance the relative abundance of Sphingomonadales and Burkhoderiales, both orders, within the phylum Proteobacteria, increased relative to the pristine site as well as Acidimicrobiales, one subclass of Actinobacteria. Interestingly the sediment downstream of the former factory outlet was colonized by bacteria which were very similar in community composition to the pristine site upstream of the factory outlet, implying a capacity of the natural sediment microbiota to cope with low levels of PAH contamination. 

National Category
Microbiology
Research subject
Biology with specialization in Microbiology
Identifiers
urn:nbn:se:uu:diva-229140 (URN)
Available from: 2014-08-01 Created: 2014-08-01 Last updated: 2014-09-08

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