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Environmental factors selecting for predation resistant and potentially pathogenic bacteria in aquatic environments
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.ORCID iD: 0000-0001-5601-9358
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The long history of co-existence of bacteria and their protozoan predators in aquatic environments has led to evolution of protozoa resistant bacteria (PRB). Many of these bacteria are also pathogenic to humans. However, the ecological drivers determining the occurrence of different types of PRB in aquatic environments, and the eco-evolutionary link between bacterial adaptation and the resulting implications for mammalian hosts are poorly known. This thesis examines the impact of nutrients and predation on PRB, as well as the ecological and evolutionary connection between their life in aquatic environments and mammalian hosts. In the first study seven bacterial isolates from the Baltic Sea were investigated for their plasticity of adaptation to predation. The response to predation showed large variation where some bacteria rapidly developed a degree of grazing resistance when exposed to predators. The rapid adaptation observed may result in bacterial communities being resilient or resistant to predation, and thus rapid adaptation may be a structuring force in the food web. With the aim to elucidate the link between occurrence of PRB and environmental conditions, a field study and a laboratory experiment were performed. In both studies three PRB genera were found: Mycobacterium, Pseudomonas and Rickettsia. PRB were found both in oligotrophic and eutrophic waters, indicating that waters of all nutrient states can harbor pathogenic bacteria. However, the ecological strategy of the PRB varied depending on environmental nutrient level and disturbance. Using an advanced bioinformatic analysis, it was shown that ecotypes within the same PRB genus can be linked to specific environmental conditions or the presence of specific protozoa, cyanobacteria or phytoplankton taxa. These environmental conditions or specific plankton taxa could potentially act as indicators for occurrence of PRB. Finally, using four mutants (with specific protein deletions) of the pathogenic and predation resistant Francisella tularensis ssp. holarctica, I found evidence of an eco-evolutionary connection between the bacterium´s life in aquatic and mammalian hosts (aquatic amoeba Acanthamoeba castellanii and a murine macrophage).  To a large extent F. t. holarctica use similar mechanisms to persist predation by protozoa and to resist degradation by mammal macrophages. To summarize I found a link between predation resistant bacteria in aquatic environments and bacteria that are pathogenic to mammals. Further, I showed that different environmental conditions rapidly selects for PRB with either intracellular or extracellular lifestyles. This thesis provides insights regarding environmental conditions and biomarkers that can be used for assessment of aquatic environments at risk for spreading pathogenic bacteria.  

Place, publisher, year, edition, pages
Umeå: Umeå Universitet , 2017. , 28 p.
Keyword [en]
Eutrophication, productivity, predation pressure, predation-resistant bacteria, pathogens, Francisella tularensis, adaptation, biomarker, oligotyping
National Category
Ecology
Identifiers
URN: urn:nbn:se:umu:diva-133338ISBN: 978-91-7601-684-8 (print)OAI: oai:DiVA.org:umu-133338DiVA: diva2:1087115
Public defence
2017-04-28, Lilla Hörsalen, KB3A9, Chemical Biological Center (KBC), Umeå Universitet, Umeå, 12:30 (English)
Opponent
Supervisors
Funder
Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning, 217-2008-1443Swedish Research Council, 60276201Ecosystem dynamics in the Baltic Sea in a changing climate perspective - ECOCHANGE
Note

Medfinansiärer var även: Swedish Ministry of Defence (A4040, A4042, A404215, A404217), Swedish Minestry of Foreign Affairs (A4952), Swedish Civil Contingencies Agency (B4055)

Available from: 2017-04-07 Created: 2017-04-05 Last updated: 2017-05-10Bibliographically approved
List of papers
1. Rapid adaptation of predation resistance in bacteria isolated from a seawater microcosm
Open this publication in new window or tab >>Rapid adaptation of predation resistance in bacteria isolated from a seawater microcosm
2016 (English)In: Aquatic Microbial Ecology, ISSN 0948-3055, E-ISSN 1616-1564, Vol. 78, no 2, 81-92 p.Article in journal (Refereed) Published
Abstract [en]

Bacterial defense against protozoan grazing has been shown to occur in many different bacteria. Predation resistance traits may however be plastic, making bacterial com munities resilient or resistant to predation perturbations. We studied the adaptation of pre dation resistance traits in bacteria isolated from a microcosm experiment. In the initial microcosm ex periment the predation pressure on bacteria varied markedly, while changes in the bacterial community composition could not be verified. Seven bacteria were isolated from the microcosm (Micrococcus sp., Rhodobacter sp., Paracoccus sp., Shewanella sp., Rhizobium sp. and 2 un identified species) and these were repeatedly exposed to high predation by the ciliate Tetrahymena pyriformis. High variations in edibility and rate of adaptation of predation resistance traits were observed among the strains. The initial mortality rate of the different bacterial taxa and the change over time varied by a factor of 7 and 24, respectively. Rhodobacter sp. was already predation resistant at the start of the experiment and did not change much over time, while Micrococcus sp., Paracoccus sp. and Shewanella sp. initially were relatively edible and later developed predation resistance. In conclusion, we show that rapid adaptation of predation resistance traits is common among bacteria in an aquatic microbial community, and that a single test of a bacterium’s edibility will in many cases not be enough to fully understand its ecological role, as it will not reveal the potential adaptive response. The results suggest the potential of rapid changes of predation resistance as a mechanism for bacterial communities to be resilient to variations in predation disturbances.

Keyword
Bacterial isolates, Predation pressure, Predation resistance, Inedible, Adaptation, Tetrahymena
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-131263 (URN)10.3354/ame01802 (DOI)000394504400002 ()
Available from: 2017-02-10 Created: 2017-02-10 Last updated: 2017-04-06Bibliographically approved
2. Oligotyping reveals divergent responses of predation resistant bacteria to aquatic productivity and plankton composition
Open this publication in new window or tab >>Oligotyping reveals divergent responses of predation resistant bacteria to aquatic productivity and plankton composition
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Predation-resistance has been suggested to be a key for persistence of pathogenic bacteria in aquatic environments. Little is known about driving factors for different types of protozoa resistant bacteria (PRB). We studied if presence of PRB is linked to specific plankton taxa, the aquatic nutrient state, or predation pressure on bacteria. Nineteen freshwater systems were sampled and analyzed for PRB, plankton composition and physicochemical variables. Three PRB genera were identified; Pseudomonas, Mycobacterium and Rickettsia. Use of minimum entropy decomposition algorithm and phylogenetic analysis showed that different nodes (representing OTUs of high taxonomic resolution) matched to environmental isolates of the three genera. Links between the PRB genera and specific plankton taxa were found, but showed different relationships depending on if 18S rRNA OTU or microscopy data were used in the analysis. Mycobacterium spp. was negatively correlated to aquatic nutrient state, while Pseudomonas showed the opposite pattern. Rickettsia spp. was positively related to predation pressure on bacteria. Both Mycobacterium and Rickettsia were more abundant in systems with high eukaryotic diversity, while Pseudomonas occurred abundantly in waters with low prokaryotic diversity. The different drivers may be explained by varying ecological strategies, where Mycobacterium and Rickettsia are slow growing and have an intracellular life style, while Pseudomonas is fast growing and opportunistic. Here we give an insight to the possibilities of newly advanced methods such as sequencing and oligotyping to link potential pathogens with biomarkers. This as a tool to assist predictions of the occurrence and persistence of environmental pathogens.

Keyword
Protozoa resistant bacteria (PRB), trophic state, oligotyping, predation pressure, biomarker
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-133333 (URN)
Funder
Ecosystem dynamics in the Baltic Sea in a changing climate perspective - ECOCHANGESwedish Research Council for Environment, Agricultural Sciences and Spatial Planning, 17-2008-1443
Note

Medfinansiärer var även: Swedish Ministry of Foreign Affairs, project A4952, the Swedish Civil Contingencies Agency, project B4055 and the Swedish Ministry of Defence, project A4040 and A4042.

Available from: 2017-04-05 Created: 2017-04-05 Last updated: 2017-04-06
3. Aquatic ecosystems at risk for occurrence of pathogenic bacteria
Open this publication in new window or tab >>Aquatic ecosystems at risk for occurrence of pathogenic bacteria
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Pathogenic bacteria occur naturally in aquatic systems. Co-existence of bacteria and protozoa has led to development of predation resistance strategies, which is suggested to serve as a driver for evolution of pathogenic bacteria. However, the ecological mechanisms for selection for different types of predation resistant and pathogenic bacteria are poorly known. To disentangle effects from nutrient availability and protozoan predation pressure on the occurrence of varying predation resistant bacterial genera, an enrichment-dilution experiment was performed where an aquatic bacterial community was exposed to protozoa. Operational taxonomical units, specific for three predation resistant bacterial genera were identified; Pseudomonas, Rickettsia and Mycobacterium. These genera are also known to harbor species that are potentially pathogenic to mammals. Rickettsia and Mycobacterium were promoted where protozoa were abundant and the predation pressure high, while Pseudomonas dominated the bacterial community at the highest nutrient level where the predation pressure on bacteria were low. Our study thus indicates that waters of all nutrient states can harbor pathogenic bacteria, but that bacteria with different ecological strategies occur depending on nutrient level and perturbation. The generative model approach presented here provide a possibility to integrate environmental data in prediction models of pathogens in complex environments.

Keyword
Protozoa resistant bacteria, predation pressure, aquatic bacterial pathogens, risk assessment, microcosm experiment
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-133336 (URN)
Funder
Ecosystem dynamics in the Baltic Sea in a changing climate perspective - ECOCHANGESwedish Research Council for Environment, Agricultural Sciences and Spatial Planning, 217-2008-1443Swedish Research Council, 60276201
Note

Medfinansiär var även: The Swedish Ministry of Defence [A404217]

Available from: 2017-04-05 Created: 2017-04-05 Last updated: 2017-04-06
4. Francisella tularensis subspecies holarctica´s adaptation to protozoan and mammal hosts
Open this publication in new window or tab >>Francisella tularensis subspecies holarctica´s adaptation to protozoan and mammal hosts
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

The long co-existence of bacteria and protozoa in natural ecosystems has led to the evolution of different bacterial predation-resistance mechanisms1, which in turn may have triggered development of mammal pathogens2, such as the tularemia bacterium Francisella tularensis3. We studied links between environmental persistence and pathogenicity of Francisella tularensis subsp. holarctica (F. t. holarctica), by comparing its growth in association with an aquatic amoeba and a murine macrophage. A virulent wild-type strain and four isogenic mutations with different functional protein deletions were compared; DsbA4, 5 a membrane lipoprotein with disulfide oxidoreductase activity important for proper folding in Francisella tularensis; Hfq6 a pleiotropic regulatory RNA binding protein; PilA7, 8 a type IV pilus subunit and PglA9 a protein involved in O-linked protein glycosylation. DsbA was found to be essential for bacterial growth in association with both amoeba and macrophage, while PglA did not affect bacterial persistence in any of the hosts. Absence of PilA and Hfq had marked negative effect on the bacterial cell counts in amoeba, while growth was only slightly impaired in the macrophage. Functional similarities for bacterial persistence in both hosts highlight eco-evolutionary links between persistence of intracellular pathogenic bacteria in aquatic systems and mammal hosts.

National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-133337 (URN)
Funder
Ecosystem dynamics in the Baltic Sea in a changing climate perspective - ECOCHANGESwedish Research Council for Environment, Agricultural Sciences and Spatial Planning, 217-2008-1443Swedish Research Council, 60276201
Note

Medfinansiär var även: Swedish Ministry of Defence [A404215]

Available from: 2017-04-05 Created: 2017-04-05 Last updated: 2017-04-06

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