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The aquatic microbial food web and occurence of predation-resistant and potentially pathogenic bacteria, such as Francisella tularensis
Umeå University, Faculty of Science and Technology, Ecology and Environmental Science.
2008 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

All natural aquatic systems harbour a vast variety of microorganisms. In the aquatic microbial food web, the larger microorganisms (i.e. protozoa) feed on the smaller microorganisms (i.e. bacteria and phytoplankton). An increase in nutrient availability results in changes of the microbial food web structure, like altered community composition and blooms of toxic phytoplankton. In this thesis work I hypothesised that nutrient-rich aquatic environments, with strong protozoan predation, favour the occurrence of predation-resistant bacteria like F. tularensis, and that the microbial food web may provide a reservoir for the bacterium between outbreaks.

By using a size-structured ecosystem food web model it was shown that the protozoan predation pressure on bacteria, defined as protozoan predation per bacterial biomass, increases with increasing nutrient availability in aquatic systems (estimated chlorophyll a 0.2 to 112 μg L-1). This dynamics was caused by increasing growth-rate of a relatively constant number of bacterial cells, maintaining the growth of an increasing number of protozoan cells. The results were supported by meta-analysis of field studies. Thus my results suggest that protozoa control the bacterial community by predation in nutrient-rich environments. In a field study in a natural productivity gradient (chlorophyll a 1.4 to 31 μg L-1) it was shown that intense selection pressure from protozoan predators, favours predation-resistant forms of bacteria. Thus, the abundance of predation-resistant bacteria increases with increasing nutrient availability in lakes.

Furthermore, I could demonstrate that the bacterium Francisella tularensis, the causative agent of tularemia, was present in eutrophic aquatic systems in an emerging tularemia area. Isolated strains of the bacterium were found to be resistant to protozoan predation. In a microcosm study, using natural lake water, high nutrient availability in combination with high abundance of a small colourless flagellate predator favoured the occurrence of F. tularensis holarctica. In laboratory experiments F. tularensis strains were able to form biofilm at temperatures between 30-37°C, but not below 30°C.

In conclusion, I have shown that the protozoan predation pressure on bacteria increases with increasing nutrient availability in aquatic systems. Predation-resistant forms of bacteria, such as F. tularensis are favoured in nutrient-rich environments. The complexity of the microbial food web and nutrient-richness of the water, influence the transmission of the pathogenic F. tularensis holarctica. However, over long periods of time, the bacterium survives in lake water but may lose its virulence. The temperature-regulated biofilm formation by F. tularensis may play a role in colonization of vectors or for colonization of hosts, rather than for survival in aquatic environments.

Place, publisher, year, edition, pages
Umeå: Ekologi, miljö och geovetenskap , 2008. , 49 p.
Keyword [en]
bacteria, protozoa, ecology, predation, nutrient-availability, microbial food web, model, predation-resistance, Francisella, reservoir, biofilm formation
National Category
Ecology
Identifiers
URN: urn:nbn:se:umu:diva-1620ISBN: 978-91-7264-529-5 (print)OAI: oai:DiVA.org:umu-1620DiVA: diva2:141580
Public defence
2008-05-22, Lilla hörsalen, KBC - huset, Umeå Universitet, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2008-04-24 Created: 2008-04-24 Last updated: 2009-08-12Bibliographically approved
List of papers
1. Predation pressure on bacteria increases along aquatic productivity gradients
Open this publication in new window or tab >>Predation pressure on bacteria increases along aquatic productivity gradients
2008 (English)In: Aquatic Microbial Ecology, ISSN 0948-3055, E-ISSN 1616-1564, Vol. 52, 45-55 p.Article in journal (Refereed) Published
Abstract [en]

To elucidate how predation pressure on bacteria is affected by increasing productivity in aquatic systems, we ran model simulations of a microbial food web. In addition, we conducted a meta-analysis of data from studies in seas and lakes. The model was run as a flow-through system simulating conditions ranging from oligotrophic to hypertrophic. The organisms included in the model were heterotrophic bacteria, phytoplankton, 3 size classes of protozoa and metazooplankton. Predation pressure was defined as flagellate and ciliate grazing per bacterial biomass. The food-web model simulations showed increasing predation pressure on bacteria with increasing productivity (estimated chlorophyll a concentration 0.2 to 112 µg l–1). This was explained by an increase in bacterial production and the ratio of protozoan to bacterial biomass with increasing productivity. The results of the model simulation were supported by the meta-analysis, which showed increasing protozoan predation pressure on bacteria with increasing productivity in aquatic systems (chlorophyll a concentration 0.1 to 250 µg l–1). The ratio of protozoan to bacterial biomass also increased with productivity in the meta-analysis of field data. Our results suggest that protozoa control the bacterial community by predation in high-productivity environments.

Keyword
Bacteria, Protozoa, Predation, Microbial food web, Productivity, Regulation, Model, Omnivory
Identifiers
urn:nbn:se:umu:diva-11434 (URN)10.3354/ame01200 (DOI)
Available from: 2009-01-08 Created: 2009-01-08 Last updated: 2017-10-24Bibliographically approved
2. Role of productivity and protozoan abundance for the occurrence of predation-resistant bacteria in aquatic systems.
Open this publication in new window or tab >>Role of productivity and protozoan abundance for the occurrence of predation-resistant bacteria in aquatic systems.
2008 (English)In: Microbial Ecology, ISSN 0095-3628, Vol. 56, no 1, 18-28 p.Article in journal (Refereed) Published
Abstract [en]

Top–down control of lower trophic levels, e.g., bacteria, has been suggested to increase along aquatic productivity gradients. The response by the bacterial community may be to become more predation resistant in highly productive environments. To test this hypothesis, samples were taken from 20 aquatic systems along a productivity gradient (dissolved organic carbon from 7 to 71 mg/L), during late summer. The results showed that the biomass of bacteria, phytoplankton, and ciliates increased along the gradient (r 2 = 0.532, 0.426, and 0.758, P < 0.01, respectively). However, the organisms did not increase equally, and the ratio of protozoan to bacterial biomass showed a 100-fold increase along the gradient. Ciliates dominated the protozoan biomass in the more nutrient-rich waters. The edibility of colony-forming bacteria was tested using a ciliate predator, Tetrahymena pyriformis. Bacterial edibility was found to decrease with increases in nutrient richness and ciliate biomass in the aquatic systems (r 2 = 0.358, P < 0.01; r 2 = 0.242, P < 0.05, respectively). Quantile regression analysis indicated that the selection pressures on edible bacteria were increasing along the productivity gradient. Thus, inedible forms of bacteria were selected for in the transition from oligotrophic to eutrophic conditions. Isolated bacteria were distributed among the α-, β-, and γ- Proteobacteria and the Actinobacteria and Firmicutes taxa. We conclude that bacterial predation resistance increases in nutrient-rich waters with high protozoan predation.

Keyword
Animals, Bacteria/*classification/genetics/*growth & development/isolation & purification, Ciliophora/growth & development/physiology, DNA; Bacterial/analysis/isolation & purification, Ecosystem, Electrophoresis/methods, Fresh Water/chemistry/microbiology/parasitology, Genetic Variation, Molecular Sequence Data, Phylogeny, Predatory Behavior/*physiology, Protozoa/growth & development/*physiology, RNA; Ribosomal; 16S/genetics, Sequence Analysis; DNA, Sweden
Identifiers
urn:nbn:se:umu:diva-11437 (URN)10.1007/s00248-007-9320-4 (DOI)17874304 (PubMedID)
Available from: 2009-01-08 Created: 2009-01-08 Last updated: 2017-10-24Bibliographically approved
3. Influence of nutrient status and microbial food web structure on the fate of Francisella tularensis in lake water
Open this publication in new window or tab >>Influence of nutrient status and microbial food web structure on the fate of Francisella tularensis in lake water
Show others...
(English)In: Article in journal (Refereed) Submitted
Identifiers
urn:nbn:se:umu:diva-3110 (URN)
Available from: 2008-04-24 Created: 2008-04-24 Last updated: 2017-10-24Bibliographically approved
4. Characterization of biofilm formation by Francisella tularensis
Open this publication in new window or tab >>Characterization of biofilm formation by Francisella tularensis
Show others...
Article in journal (Refereed) Submitted
Identifiers
urn:nbn:se:umu:diva-3111 (URN)
Available from: 2008-04-24 Created: 2008-04-24Bibliographically approved

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