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Bacterial Degradation and Use of Chitin in Aquatic Habitats
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology.
2010 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Chitin belongs to the most abundant biopolymers on earth where it has an important role as a structural element in crustaceans, insects, fungi and some phytoplankton. Missing evidence for long-term accumulation of chitin in nature implies fast turnover and as chitin is composed of aminosugar subunits it holds central roles in both carbon and nitrogen cycles. The aim of this thesis was to contribute to a better understanding of organic matter cycling by learning more about the diversity, function and ecology of bacteria that degrade chitin. A metagenome-enabled study of the spatial distribution of chitinolytic bacteria in aquatic ecosystems identified salinity as the major environmental factor for shaping their community composition. To address the role of alternative environmental variables controlling chitinolytic communities, a temporally resolved study was completed in a dimictic freshwater lake. Pronounced seasonal change in the indigenous chitinolytic community was observed and parallel measured environmental parameters pointed to the availability and crystalline form of chitin as significant controlling factors.  The different ecological niches occupied by microbes that utilize chitin for growth were studied in an experimental study. Single-cell quantification of chitinolytic cells and cells incorporating chitin hydrolysis products suggested that commensal use of chitin hydrolysis products without simultaneous chitinase activity could be an important ecological strategy in freshwater bacterioplankton communities. Members of the ubiquitous and often quantitatively dominant group of freshwater Actinobacteria Ac1 were identified as particularly active in this “cheater” lifestyle. Further experiments based on artificially created gradients in bacterial diversity demonstrated the importance of specific bacterial populations and community composition rather than overall community richness in controlling more specific functions such as chitin and cellulose degradation. To conclude, results of this thesis provide insight into the biogeography, niche-separation and species interactions of the functional community of chitin degraders and the influence of general bacterial diversity to the respective system functioning.

 

 

 

 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis , 2010. , p. 48
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 770
Keywords [en]
Chitin, organic matter degradation, microbial ecology, functional guild
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:uu:diva-131128ISBN: 978-91-554-7902-2 (print)OAI: oai:DiVA.org:uu-131128DiVA, id: diva2:353008
Public defence
2010-11-05, Ekmansalen, Evolutionsbiologisk Centrum, Norbyv. 18 D, Uppsala, 10:00 (English)
Opponent
Supervisors
Note
Felaktigt tryckt som Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 700Available from: 2010-10-15 Created: 2010-09-23 Last updated: 2011-03-21Bibliographically approved
List of papers
1. Mechanisms and ecology of bacterial chitin degradation
Open this publication in new window or tab >>Mechanisms and ecology of bacterial chitin degradation
(English)Manuscript (preprint) (Other academic)
Identifiers
urn:nbn:se:uu:diva-131084 (URN)
Available from: 2010-09-22 Created: 2010-09-22 Last updated: 2011-03-21
2.
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3. Pronounced seasonal dynamics of freshwater chitinase genes and chitin processing
Open this publication in new window or tab >>Pronounced seasonal dynamics of freshwater chitinase genes and chitin processing
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2012 (English)In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 14, no 9, p. 2467-2479Article in journal (Refereed) Published
Abstract [en]

Seasonal variation in activity of enzymes involved in polymer degradation, including chitinases, has been observed previously in freshwater environments. However, it is not known whether the seasonal dynamics are due to shifts in the activity of bacteria already present, or shifts in community structure towards emergence or disappearance of chitinolytic organisms. We traced seasonal shifts in the chitinase gene assemblage in a temperate lake and linked these communities to variation in chitinase activity. Chitinase genes from 20 samples collected over a full yearly cycle were characterized by pyrosequencing. Pronounced temporal shifts in composition of the chitinase gene pool (beta diversity) occurred along with distinct shifts in richness (alpha diversity) as well as chitin processing. Changes in the chitinase gene pool correlated mainly with temperature, abundance of crustacean zooplankton and phytoplankton blooms. Also changes in the physical structure of the lake, e.g. stratification and mixing were associated with changes in the chitinolytic community, while differences were minor between surface and suboxic hypolimnetic water. The lake characteristics influencing the chitinolytic community are all linked to changes in organic particles and we suggest that seasonal changes in particle quality and availability foster microbial communities adapted to efficiently degrade them.

Keywords
chitinase genes, lake, temporal dynamics, seasonality, pyrosequencing
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-131091 (URN)10.1111/j.1462-2920.2012.02764.x (DOI)000308300600018 ()
Available from: 2010-09-22 Created: 2010-09-22 Last updated: 2017-12-12Bibliographically approved
4. Uncoupling of chitinase activity and uptake of hydrolyses products in freshwater bacterioplankton
Open this publication in new window or tab >>Uncoupling of chitinase activity and uptake of hydrolyses products in freshwater bacterioplankton
2011 (English)In: Limnology and Oceanography, ISSN 0024-3590, E-ISSN 1939-5590, Vol. 56, no 4, p. 1179-1188Article in journal (Refereed) Published
Abstract [en]

We investigated to what extent chitinolytic bacteria subsidize bacterial populations that do not produce chitinolytic enzymes but still use the products of chitin hydrolysis. Applying single-cell techniques to untreated and chitin-enriched lake water, we show that the number of planktonic cells taking up chitin hydrolysis products by far exceeds the number of cells expressing chitinases. Flavobacteria, Actinobacteria, and specifically members of the abundant and ubiquitous freshwater Ac1 cluster of the Actinobacteria, increased in abundance and were enriched in response to the chitin amendment. Flavobacteria were frequently observed in dense clusters on chitin particles, suggesting that they are actively involved in the hydrolysis and solubilization of chitin. In contrast, Actinobacteria were exclusively planktonic. We propose that planktonic Actinobacteria contain commensals specialized in the uptake of small hydrolysis products without expressing or possibly even possessing the machinery for chitin hydrolysis. More research is needed to assess the importance of such "cheater'' substrate acquisition strategies in the turnover and degradation of polymeric organic matter in aquatic ecosystems.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-131094 (URN)10.4319/lo.2011.56.4.1179 (DOI)000294603400001 ()
Available from: 2010-09-22 Created: 2010-09-22 Last updated: 2017-12-12Bibliographically approved
5. Function-specific response to depletion of microbial diversity
Open this publication in new window or tab >>Function-specific response to depletion of microbial diversity
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2011 (English)In: The ISME Journal, ISSN 1751-7362, Vol. 5, no 2, p. 351-361Article in journal (Refereed) Published
Abstract [en]

Recent meta-analyses suggest that ecosystem functioning increases with biodiversity, but contradictory results have been presented for some microbial functions. Moreover, observations of only one function underestimate the functional role of diversity because of species-specific trade-offs in the ability to carry out different functions. We examined multiple functions in batch cultures of natural freshwater bacterial communities with different richness, achieved by a dilution-to-extinction approach. Community composition was assessed by molecular fingerprinting of 16S rRNA and chitinase genes, representing the total community and a trait characteristic for a functional group, respectively. Richness was positively related to abundance and biomass, negatively correlated to cell volumes and unrelated to maximum intrinsic growth rate. The response of chitin and cellulose degradation rates depended on the presence of a single phylotype. We suggest that species identity and community composition rather than richness matters for specific microbial processes.

Keywords
cellulose, chitin, functional diversity, species traits, T-RFLP
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-131083 (URN)10.1038/ismej.2010.119 (DOI)000290020000018 ()20686511 (PubMedID)
Available from: 2010-09-22 Created: 2010-09-22 Last updated: 2017-11-30Bibliographically approved

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