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Drivers of Population Dynamics in Bacterioplankton: Spotlight on Alphaproteobacteria and its dominant SAR11 Lineage
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]

Bacteria are mediators of biogeochemical cycles and are in this way vital for maintaining life on earth. Their distribution, abundance and functioning are driven by environmental heterogeneity and dynamic change in abiotic and biotic factors. Both, freshwater lakes and oceans play central roles in the global carbon cycle and bacteria in these systems perform many services for the ecosystems, such as the transfer of organic carbon from primary producers to higher trophic levels. With estimated relative abundances up to 50% of the total bacterioplankton, the Alphaproteobacteria lineage SAR11 is the most abundant group of aquatic bacteria. It is globally distributed and can be partitioned into multiple sub-clades, one of which is exclusive to freshwaters. Until recently, the distribution, abundance and ecological role of this freshwater SAR11 named LD12 was unknown. The aim of the thesis was to study the drivers and mechanisms that influence the dynamics of aquatic bacterial communities in general and the SAR11 and LD12 groups in particular. The thesis consists of environmental surveys of a mesotrophic Lake Erken and the western Southern Ocean, an experiment and a data-mining exercise to reveal the phylogenetic structure of the SAR11 lineage on various temporal and spatial scales. The analysis of a long-term bacterioplankton community survey in lake Erken provided insights about the dynamics of the entire bacterial community and the LD12 population over an annual cycle. The results demonstrate that LD12 can be an equally abundant member of freshwater communities as marine SAR11 in oceans. LD12 featured strong seasonality and was positively coupled to environmental conditions indicative for an oligotrophic lifestyle. LD12 as well as other dominant lake bacterioplankton also maintained stable populations throughout spatial and temporal varying environments, but at high phylogenetic resolution, habitat preferences were revealed, particularly in response to oxygen concentrations. The later was not the case in LD12 as a single ribotype dominated. This is in stark contrast to the habitat partitioning with light availability, depth and water masses observed for marine SAR11 subclades in the Southern Ocean. The global data-mining corroborated that LD12 as a group was much less diverse than SAR11 furthermore, suggesting that the marine-freshwater barrier acted as a population bottleneck. My work shows that bacterial populations can respond in very different ways to environmental drivers, highlight the importance of highly resolved temporal and spatial scales as well as the need for high phylogenetic resolutions to target ecologically coherent populations.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2015. , 54 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1230
Keyword [en]
bacterial community dynamics, Alphaproteobacteria, SAR11, LD12, Southern Ocean, lakes
National Category
Ecology
Research subject
Biology with specialization in Limnology
Identifiers
URN: urn:nbn:se:uu:diva-245072ISBN: 978-91-554-9172-7 (print)OAI: oai:DiVA.org:uu-245072DiVA: diva2:790359
Public defence
2015-04-10, Fries-salen, Evolutionsbiologiskt Centrum (EBC), Norbyvägen 14, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2015-03-19 Created: 2015-02-24 Last updated: 2015-04-17
List of papers
1. Infrequent Transitions between Saline and Fresh Waters in One of the Most Abundant Microbial Lineages (SAR11)
Open this publication in new window or tab >>Infrequent Transitions between Saline and Fresh Waters in One of the Most Abundant Microbial Lineages (SAR11)
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2010 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 27, no 2, 347-357 p.Article in journal (Refereed) Published
Abstract [en]

The aquatic bacterial group SAR11 is one of the most abundant organisms on Earth, with an estimated global population size of 2.4 x 10(28) cells in the oceans. Members of SAR11 have also been detected in brackish and fresh waters, but the evolutionary relationships between the species present in the different environments have been ambiguous. In particular, it was not clear how frequently this lineage has crossed the saline-freshwater boundary during its evolutionary diversification. Due to the huge population size of SAR11 and the potential of microbes for long-distance dispersal, we hypothesized that environmental transitions could have occurred repeatedly during the evolutionary diversification of this group. Here, we have constructed extensive 16S rDNA-based molecular phylogenies and undertaken metagenomic data analyses to assess the frequency of saline-freshwater transitions in SAR11 and to investigate the evolutionary implications of this process. Our analyses indicated that very few saline-freshwater transitions occurred during the evolutionary diversification of SAR11, generating genetically distinct saline and freshwater lineages that do not appear to exchange genes extensively via horizontal gene transfer. In contrast to lineages from saline environments, extant freshwater taxa from diverse, and sometimes distant, geographic locations were very closely related. This points to a rapid diversification and dispersal in fresh waters or to slower evolutionary rates in fresh water SAR11 when compared with marine counterparts. In addition, the colonization of both saline and fresh waters appears to have occurred early in the evolution of SAR11. We conclude that the different biogeochemical conditions that prevail in saline and fresh waters have likely prevented the environmental transitions in SAR11, promoting the evolution of clearly distinct lineages in each environment.

Keyword
environmental transitions, prokaryotes, saline, freshwater, SAR11, 16S rDNA
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-137815 (URN)10.1093/molbev/msp239 (DOI)000273704400013 ()
Available from: 2010-12-17 Created: 2010-12-16 Last updated: 2017-12-11Bibliographically approved
2. Abundance and diveristy of Alphaproteobacteria in the Southern Ocean: the dark side of SAR11
Open this publication in new window or tab >>Abundance and diveristy of Alphaproteobacteria in the Southern Ocean: the dark side of SAR11
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Alphaproteobacteria represented by lineages such as SAR11 and Roseobacter are ubiquitous and often dominant in marine bacterioplankton communities. The Southern Ocean is no exception even if annual extremes in light regime and autochthonous inputs of organic substrates present an environment that are in many ways very different from other oceanic regions. Using population mapping and community analysis of bacterioplankton during the highly dynamic summer season within the Ross and Amundsen Seas, in combination with experimental incubations under contrasting light regimes, we studied the impact of solar radiation and other environmental factors on individual lineages and populations within class Alphaproteobacteria. Quantitative population tracking by fluorescence in-situ hybridization was combined with pyrosequencing-derived 16S rRNA gene inventories to resolve the community beyond class and abundant lineages. Both experiments and depth-resolved distribution patterns confirm SAR11 as a major component of the bacterial community regardless of water mass and depth. However, the experiments revealed that SAR11 as a lineage was less competitive under solar-exposed conditions whereas the opposite response was observed for Roseobacter. Resolving the SAR11 linage into subclades, clear partitioning of groups between the different water masses and light regimes was observed. Also the diversity within the SAR11 lineage varied with significantly higher richness in the deeper, permanently dark water masses. Using this abundant marine bacterial lineage as a model, we could demonstrate clear separation of closely related bacterial populations between water masses and along environmental gradients of light exposure, oxygen availability, phytoplankton and nutrients. It is evident that such ecologically coherent populations can only be tracked at high phylogenetic resolution and that ecological and evolutionary mechanisms underpinning the observed phylogeographic patterns differ between water masses in the Southern Ocean. 

Keyword
Southern Ocean, Alphaproteobacteria, SAR11, Roseobacter, community composition, solar radiation
National Category
Ecology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-245066 (URN)
Available from: 2015-02-24 Created: 2015-02-24 Last updated: 2015-04-17
3. Seasonality and environmental control of freshwater SAR11 (LD12) in a temperate lake (Lake Erken, Sweden)
Open this publication in new window or tab >>Seasonality and environmental control of freshwater SAR11 (LD12) in a temperate lake (Lake Erken, Sweden)
2013 (English)In: Aquatic Microbial Ecology, ISSN 0948-3055, E-ISSN 1616-1564, Vol. 70, no 1, 33-44 p.Article in journal (Refereed) Published
Abstract [en]

THE SAR11 clade is ubiquitous and abundant in planktonic environments. In freshwater lakes, the clade is represented by tribe LD12 which is phylogenetically distinct from the marine SAR11. We studied the ecology of LD12 in a temperate dimictic lake (Lake Erken, Sweden), by analyzing its seasonal dynamics with quantitative PCR, CARD-FISH and 454 pyrosequencing of the 16S rRNA gene. Results showed that LD12 can be as numerous in freshwater bacterioplankton as their marine SAR11 siblings. They exhibited strong seasonality and made up from 1.8 to 40% of the total bacterial 16S rRNA pool (mean 14%) with pronounced peaks in summer and late fall. Except in spring, LD12 was the dominant Alphaproteobacteria, contributing on average 72% of the 16S rRNA within this class. The LD12 population was dominated by a single persistent ribotype, suggesting low local divergence, at least at the phylogenetic resolution accessed with rRNA genes. The relative abundance of LD12 was positively correlated to nutrient concentrations (phosphate, ammonia, nitrate, and silica) and water transparency whereas the relative abundance was lower during periods characterized by high phytoplankton biomass. Based on these observations we propose that LD12 are poor competitors during periods of high phytoplankton productivity and associated release of labile organic compounds, but thrive when availability of inorganic nutrients is high. Similar to the marine SAR11 sibling group, local LD12 populations appear to respond in contrasting ways to nutrient availability in different lakes, pointing to either ecological divergence within the tribe or variations in the interplay between environmental driver variables.

Keyword
LD12, Freshwater SAR11, Alphaproteobacteria, Seasonal dynamics, Quantitative PCR, 454 Pyrosequencing, CARD-FISH, 16S rRNA
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-207118 (URN)10.3354/ame01637 (DOI)000322999500003 ()
Available from: 2013-09-10 Created: 2013-09-09 Last updated: 2017-12-06Bibliographically approved
4. Alteration of lake bacterioplankton diversity and community composition during lake stratification and gradual oxygen depletion
Open this publication in new window or tab >>Alteration of lake bacterioplankton diversity and community composition during lake stratification and gradual oxygen depletion
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Hypolimnetic waters of many stratifying lakes experience gradual oxygen depletion and seasonal hypoxia as organic matter is degraded with oxygen as terminal electron acceptor. Such changes are known to have dramatic effects on larger organisms, but also resident microbiota are likely to be affected by altered availability of oxygen, nutrients and other chemical constituents. We explored how such seasonal shifts in water mass characteristics influenced the resident bacterioplankton in a mesotrophic temperate lake by tracing the temporal dynamics of bacterial communities and populations at different phylogenetic resolution across the entire period of summer stratification. Compared to the epilimnion, bacterial richness was significantly higher in the hypolimnion where varying hypoxia was also reflected in higher beta diversity. Many abundant groups of freshwater bacteria, such as Actinobacteria acI, Polynucleobacter and freshwater SAR11 (LD12), were abundant in both the epi- and hypolimnion, with distinct temporal and vertical population shifts observed at the 97% population identity level. The mechanisms that lead to closely related populations partitioning into ecotypes are not well understood, but are probably due to fine-tuned physiological adaptions towards oxygen and nutrient concentrations in the lake. The existence of ecotypes partitioned by oxygen availability and the seasonal succession in hypolimnetic bacteria driven by gradual oxygen depletion and associated changes in water chemistry merits further studies on their implications for biogeochemical cycles.

Keyword
hypolimnion, Bacteria, Community Composition, Diversity, Hypoxia, Dynamics, Indicator, Habitat
National Category
Ecology
Research subject
Biology with specialization in Evolutionary Genetics; Biology with specialization in Limnology
Identifiers
urn:nbn:se:uu:diva-245068 (URN)
Available from: 2015-02-24 Created: 2015-02-24 Last updated: 2015-04-17
5. Coherent dynamics and association networks among lake bacterioplankton taxa
Open this publication in new window or tab >>Coherent dynamics and association networks among lake bacterioplankton taxa
2012 (English)In: The ISME Journal: multidisciplinary journal of microbial ecology, ISSN 1751-7362, Vol. 6, no 2, 330-342 p.Article in journal (Refereed) Published
Abstract [en]

Bacteria have important roles in freshwater food webs and in the cycling of elements in the ecosystem. Yet specific ecological features of individual phylogenetic groups and interactions among these are largely unknown. We used 454 pyrosequencing of 16S rRNA genes to study associations of different bacterioplankton groups to environmental characteristics and their co-occurrence patterns over an annual cycle in a dimictic lake. Clear seasonal succession of the bacterioplankton community was observed. After binning of sequences into previously described and highly resolved phylogenetic groups (tribes), their temporal dynamics revealed extensive synchrony and associations with seasonal events such as ice coverage, ice-off, mixing and phytoplankton blooms. Coupling between closely and distantly related tribes was resolved by time-dependent rank correlations, suggesting ecological coherence that was often dependent on taxonomic relatedness. Association networks with the abundant freshwater Actinobacteria and Proteobacteria in focus revealed complex interdependencies within bacterioplankton communities and contrasting linkages to environmental conditions. Accordingly, unique ecological features can be inferred for each tribe and reveal the natural history of abundant cultured and uncultured freshwater bacteria.

Keyword
freshwater, 454 pyrosequencing, 16S rRNA, phylogenetic tribes, bacteria
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-171679 (URN)10.1038/ismej.2011.113 (DOI)000300984200011 ()
Available from: 2012-03-26 Created: 2012-03-25 Last updated: 2016-04-22Bibliographically approved

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