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Life strategies for substrate assimilation by freshwater bacterioplankton
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology.
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The availability of substrates is one of the most important environmental constraints on the diversity and functioning of microorganisms. Substrate quantity and quality as well as the metabolic features of heterotrophic microorganisms determine the efficiency, speed and type of transformation that can occur in nature. As such their interplay with the environment regulates how much carbon and energy is incorporated by bacteria and subsequently reaches higher trophic levels. In lakes the bulk substrate that is available for bacteria is composed of a complex mixture of compounds, varying in lability and distribution in the environment. This thesis addresses the coupling of organic substrates, their metabolic use and the composition and ecology of the microbial community. Controlled laboratory experiments with mixed bacterial communities in either batch cultures or chemostats were designed to shed further light on bacterial use of labile and quantitatively significant carbon compounds.

I show that different amino acid substrates only exert a minor influence on bacterioplankton community composition and growth. Hence the ability to use a wide range of such abundantly produced protein monomers seems to be widespread among freshwater bacteria. In contrast, when acetate was provided as the only carbon substrate, in either pulsed or continuous amendments, this very different substrate input mode had a strong effect on bacterial community composition. Biomass yield, for example, was twice as high when acetate was given in the form of pulses rather than provided continuously.

In another set of experiments, I show that the oxidation of the globally significant greenhouse gas methane is a process that can potentially take place at the water-ice interface of seasonally ice-covered lakes and was not constrained by temperature as suggested in previous studies. This work also suggests that methane oxidation in ice-covered lakes can be constrained by competition for nutrients between specialized methanotrophs and heterotrophic bacteria.

Combined these studies suggest that some labile substrates cause minor selection on bacterial community structure and functioning. This probably reflects the competitive advantage of using a broad range of low molecular weight substrates. However, as in the case of methanotrophs there is specialization for a specific low molecular weight substrate such as methane. In which case, competition with other community members i.e. for nutrients can constrain methane oxidation. In both cases it might however not depend just on the availability of substrate, but also on how substrates are distributed in time and space.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2016. , 39 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1342
Keyword [en]
lake, methane, bacteria, substrate, methanotrophs, pulse, chemostat
National Category
Natural Sciences
Identifiers
URN: urn:nbn:se:uu:diva-275181ISBN: 978-91-554-9470-4 (print)OAI: oai:DiVA.org:uu-275181DiVA: diva2:899153
Public defence
2016-03-18, Friessalen, EBC, Norbyvägen 14, Uppsala, 09:00 (English)
Opponent
Supervisors
Available from: 2016-02-26 Created: 2016-02-01 Last updated: 2016-03-09
List of papers
1. Are freshwater bacterioplankton indifferent to variable types of amino acid substrates?
Open this publication in new window or tab >>Are freshwater bacterioplankton indifferent to variable types of amino acid substrates?
2016 (English)In: FEMS Microbiology Ecology, ISSN 0168-6496, E-ISSN 1574-6941, Vol. 92, no 2, UNSP fiw005Article in journal (Refereed) Published
Abstract [en]

A wide range of carbon compounds sustain bacterial activity and growth in freshwater ecosystems and the amount and quality of these substrates influence bacterial diversity and metabolic function. Biologically labile low-molecular-weight compounds, such as dissolved free amino acids, are particularly important substrates and can fuel as much as 20% of the total heterotrophic production. In this study, we show that extensive laboratory incubations with variable amino acids as substrates caused only minimal differences in bacterial growth rate, growth yield, quantitative amino acid usage, community composition and diversity. This was in marked contrast to incubations under dark or light regimes, where significant responses were observed in bacterial community composition and with higher diversity in the dark incubations. While a few individual taxa still responded to amendment with specific amino acids, our results suggest that compositional shifts in the specific supply of amino acids and possibly also other labile organic substrates have a minor impact on heterotrophic bacterioplankton communities, at least in nutrient rich lakes and compared to other prevailing environmental factors.

Keyword
freshwater bacteria; amino acid substrates; light regime; community composition; substrate specialization
National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-275179 (URN)10.1093/femsec/fiw005 (DOI)000371249600019 ()
Funder
Swedish Research CouncilSwedish Research Council Formas
Available from: 2016-02-01 Created: 2016-02-01 Last updated: 2017-11-30Bibliographically approved
2. Influence of pulsed and continuous substrate inputs on freshwater bacterial community composition and functioning in bioreactors
Open this publication in new window or tab >>Influence of pulsed and continuous substrate inputs on freshwater bacterial community composition and functioning in bioreactors
Show others...
2017 (English)Manuscript (preprint) (Other academic)
Abstract [en]

Aquatic environments are typically not homogenous, but characterized by changing substrate concentration gradients and nutrient patches. This heterogeneity in substrate availability creates a multitude of niches allowing bacteria with different substrate utilization strategies to hypothetically coexist even when competing for the same substrate. To study the impact of heterogeneous distribution of organic substrates on bacterioplankton, bioreactors with freshwater bacterial communities were fed artificial freshwater medium with acetate supplied either continuously or in pulses. After a month-long incubation, bacterial biomass and community-level substrate uptake rates were twice as high in the pulsed treatment compared to the continuously fed reactors even if the same total amount of acetate was supplied to both treatments. The composition of the bacterial communities emerging in the two treatments differed significantly with specific taxa overrepresented in the respective treatments. The higher estimated growth yield in cultures that received pulsed substrate inputs, imply that such conditions enable bacteria to use resources more efficiently for biomass production. This finding agrees with established concepts of basal maintenance energy requirements and high energetic costs to assimilate substrates at low concentration. Our results further imply that degradation of organic matter is influenced by temporal and spatial heterogeneity in substrate availability. 

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-275178 (URN)10.1111/1462-2920.13979 (DOI)
Available from: 2016-02-01 Created: 2016-02-01 Last updated: 2017-12-04
3. Methane oxidation at the water-ice interface of an ice-covered lake
Open this publication in new window or tab >>Methane oxidation at the water-ice interface of an ice-covered lake
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2016 (English)In: Limnology and Oceanography, ISSN 0024-3590, E-ISSN 1939-5590, Vol. 61, no S1, S78-S90 p.Article in journal (Refereed) Published
Abstract [en]

Lakes are important components of the global methane (CH4) cycle. In seasonally ice-covered lakes, CH4 transported by ebullition (bubbling) from anoxic sediments gets trapped at the water-ice interface. If not oxidized by methane-oxidizing bacteria (MOB), this can potentially lead to high episodic CH4 emissions at ice-melt. To understand the fate of CH4 trapped below ice, we measured depth-distributions of CH4 concentrations in the water column near bubbles trapped below ice in Lake Erken. We also performed a 21 d incubation experiment at low temperature (2.3 ± 0.2°C) to investigate the potential for CH4 oxidation. During most sampling occasions, we found steep CH4 concentration gradients just below the ice with a 13-fold decrease from the surface to a depth of 20 cm. In vitro incubations revealed that CH4oxidation can occur at low temperatures typical for the water-ice interface. CH4 oxidation was observed as a significant decrease in CH4 concentration, a significant increase in stable isotope 13C signature, and an increase in MOB during the incubation. Thus, CH4 accumulating in the top 20 cm of the water column, fed by diffusion from CH4 in trapped bubbles, may fuel significant CH4 oxidation. Since northern latitude lakes can be ice-covered for many months of the year and significant amounts of CH4 accumulate below the ice, the extent of CH4oxidation under these low temperature-conditions is important for understanding the potential CH4 emissions to the atmosphere during ice-melt.

National Category
Oceanography, Hydrology, Water Resources
Identifiers
urn:nbn:se:uu:diva-274392 (URN)10.1002/lno.10288 (DOI)000388560900007 ()
Funder
Swedish Research CouncilSwedish Research Council Formas
Available from: 2016-01-21 Created: 2016-01-21 Last updated: 2017-11-30Bibliographically approved
4. Constraints on methane oxidation in ice-covered boreal lakes
Open this publication in new window or tab >>Constraints on methane oxidation in ice-covered boreal lakes
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2016 (English)In: Journal of Geophysical Research - Biogeosciences, ISSN 2169-8953, E-ISSN 2169-8961, Vol. 121, no 7, 1924-1933 p.Article in journal (Refereed) Published
Abstract [en]

Boreal lakes can be ice covered for a substantial portion of the year at which time methane (CH4) can accumulate below ice. The amount of CH4 emitted at ice melt is partially determined by the interplay between CH4 production and CH4 oxidation, performed by methane-oxidizing bacteria (MOB). Yet the balance between oxidation and emission and the potential for CH4 oxidation in various lakes during winter is largely unknown. To address this, we performed incubations at 2 degrees C to screen for wintertime CH4 oxidation potential in seven lakes. Results showed that CH4 oxidation was restricted to three lakes, where the phosphate concentrations were highest. Molecular analyses revealed that MOB were initially detected in all lakes, although an increase in type I MOB only occurred in the three lake water incubations where oxidation could be observed. Accordingly, the increase in CO2 was on average 5 times higher in these three lake water incubations. For one lake where no oxidation was measured, we tested if temperature and CH4 availability could trigger CH4 oxidation. However, regardless of incubation temperatures and CH4 concentrations, ranging from 2 to 20 degrees C and 1-500M, respectively, no oxidation was observed. Our study indicates that some lakes with active wintertime CH4 oxidation may have low emissions during ice melt, while other and particularly nutrient poor lakes may accumulate large amounts of CH4 below ice that, in the absence of CH4 oxidation, will be emitted following ice melt. This variability in CH4 oxidation rates between lakes needs to be accounted for in large-scale CH4 emission estimates.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-274393 (URN)10.1002/2016JG003382 (DOI)000382581900015 ()
Funder
Swedish Research CouncilSwedish Research Council FormasCarl Tryggers foundation
Note

De två första författarna delar förstaförfattarskapet.

Available from: 2016-01-21 Created: 2016-01-21 Last updated: 2017-11-30Bibliographically approved

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