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  • 1.
    Ahlinder, Jon
    et al.
    Division of CBRN Defence and Security, FOI, Swedish Defence Research Agency, Umeå, Sweden.
    Mathisen, Peter
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Sjödin, Andreas
    Umeå University, Faculty of Science and Technology, Department of Chemistry. Division of CBRN Defence and Security, FOI, Swedish Defence Research Agency, Umeå, Sweden.
    Nilsson, Elin
    Division of CBRN Defence and Security, FOI, Swedish Defence Research Agency, Umeå, Sweden.
    Forsman, Mats
    Division of CBRN Defence and Security, FOI, Swedish Defence Research Agency, Umeå, Sweden.
    Andersson, Agneta
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Thelaus, Johanna
    Division of CBRN Defence and Security, FOI, Swedish Defence Research Agency, Umeå, Sweden.
    Oligotyping reveals divergent responses of predation resistant bacteria to aquatic productivity and plankton compositionManuscript (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.

  • 2.
    Andersson, Agneta
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Marine Sciences Centre (UMF).
    Ahlinder, J.
    Mathisen, Peter
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Hagglund, M.
    Backman, S.
    Nilsson, E.
    Sjodin, A.
    Thelaus, J.
    Predators and nutrient availability favor protozoa-resisting bacteria in aquatic systems2018In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 8, article id 8415Article in journal (Refereed)
    Abstract [en]

    The long co-existence of bacteria and protozoa has led to the development of bacterial protozoa resistance strategies, which are suggested to serve as drivers for the evolution of pathogenic bacteria. However, the ecological mechanisms underpinning selection for protozoa-resistance in aquatic bacteria are poorly known. To assess the role of nutrient availability and predation-pressure on selection for protozoa-resisting bacteria (PRB), an enrichment-dilution experiment was designed using laboratory microcosms containing natural lake water. PRB was monitored by screening 16S rRNA amplicon sequence data for reads assigned to bacteria that previously has been shown to resist degradation by amoebae. To estimate the effects of the microbial food web dynamics (microscopy of; heterotrophic bacteria, phytoplankton, protozoa and rotifers) and physicochemical variables on the PRB abundance in the study system, a joint species distribution modelling approach was used. The predation-pressure (ratio between predator and bacterial biomass) had a positive effect on the abundance of the PRB genus Mycobacterium, while perturbation (enrichment and dilution) favored the PRB genus Pseudomonas that dominated the bacterial community in the disturbed systems. Our results show that PRB with different ecological strategies can be expected in water of high and intermediate nutrient levels and after major disturbances of an aquatic system.

  • 3.
    Andersson, Agneta
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Ahlinder, Jon
    Division of CBRN Defence and Security, Swedish Defence Research Agency, FOI, SE-901 82 Umeå, Sweden.
    Mathisen, Peter
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Bäckman, Stina
    Division of CBRN Defence and Security, Swedish Defence Research Agency, FOI, SE-901 82 Umeå, Sweden.
    Nilsson, Elin
    Division of CBRN Defence and Security, Swedish Defence Research Agency, FOI, SE-901 82 Umeå, Sweden.
    Hammarström, Moa
    Division of CBRN Defence and Security, Swedish Defence Research Agency, FOI, SE-901 82 Umeå, Sweden.
    Sjödin, Andreas
    Division of CBRN Defence and Security, Swedish Defence Research Agency, FOI, SE-901 82 Umeå, Sweden.
    Thelaus, Johanna
    Division of CBRN Defence and Security, Swedish Defence Research Agency, FOI, SE-901 82 Umeå, Sweden.
    Aquatic ecosystems at risk for occurrence of pathogenic bacteriaManuscript (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.

  • 4.
    Faithfull, Carolyn L.
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Mathisen, Peter
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Wenzel, Anja
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Bergström, Ann-Kristin
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Vrede, T.
    Food web efficiency differs between humic and clear water lake communities in response to nutrients and light2015In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 177, no 3, p. 823-835Article in journal (Refereed)
    Abstract [en]

    This study demonstrates that clear and humic freshwater pelagic communities respond differently to the same environmental stressors, i.e. nutrient and light availability. Thus, effects on humic communities cannot be generalized from existing knowledge about these environmental stressors on clear water communities. Small humic lakes are the most numerous type of lake in the boreal zone, but little is known about how these lakes will respond to increased inflows of nutrients and terrestrial dissolved organic C (t-DOC) due to climate change and increased human impacts. Therefore, we compared the effects of nutrient addition and light availability on pelagic humic and clear water lake communities in a mesocosm experiment. When nutrients were added, phytoplankton production (PPr) increased in both communities, but pelagic energy mobilization (PEM) and bacterial production (BP) only increased in the humic community. At low light conditions, the addition of nutrients led to increased PPr only in the humic community, suggesting that, in contrast to the clear water community, humic phytoplankton were already adapted to lower ambient light levels. Low light significantly reduced PPr and PEM in the clear water community, but without reducing total zooplankton production, which resulted in a doubling of food web efficiency (FWE = total zooplankton production/PEM). However, total zooplankton production was not correlated with PEM, PPr, BP, PPr:BP or C:nutrient stoichiometry for either community type. Therefore, other factors such as food chain length, food quality, ultra-violet radiation or duration of the experiment, must have determined total zooplankton production and ultimately FWE.

  • 5.
    Liess, Antonia
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Laboratoire Ecosystémes Marins Côtiers, UMR5119 CNRS, Université Montpellier2, IRD, IFREMER, Paris, France.
    Rowe, Owen
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Francoeur, S. N.
    Guo, Junwen
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Lange, K.
    Schroeder, A.
    Reichstein, Birte
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Lefèbure, Robert
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Deininger, Anne
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Mathisen, Peter
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Faithfull, Carolyn L.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Terrestrial runoff boosts phytoplankton in a Mediterranean coastal lagoon, but these effects do not propagate to higher trophic levels2016In: Hydrobiologia, ISSN 0018-8158, E-ISSN 1573-5117, Vol. 766, no 1, p. 275-291Article in journal (Refereed)
    Abstract [en]

    Heavy rainfall events causing significant terrestrial runoff into coastal marine ecosystems are predicted to become more frequent with climate change in the Mediterranean. To simulate the effects of soil runoff on the pelagic food web of an oligotrophic Mediterranean coastal lagoon, we crossed soil extract addition (increasing nutrient availability and turbidity) and fish presence in a full factorial design to coastal mesocosms containing a natural pelagic community. Soil extract addition increased both bacteria and phytoplankton biomass. Diatoms however profited most from soil extract addition, especially in the absence of fish. In contrast zooplankton and fish did not profit from soil extract addition. Furthermore, our data indicate that nutrients (instead of light or carbon) limited basal production. Presumed changes in carbon availability are relatively unimportant to primary and secondary production in strongly nutrient limited systems like the Thau Lagoon. We conclude that in shallow Mediterranean coastal ecosystems, heavy rainfall events causing soil runoff will (1) increase the relative abundance of phytoplankton in relation to bacteria and zooplankton, especially in the absence of fish (2) not lead to higher biomass of zooplankton and fish, possibly due to the brevity of the phytoplankton bloom and the slow biomass response of higher trophic levels.

  • 6.
    Mathisen, Peter
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Environmental factors selecting for predation resistant and potentially pathogenic bacteria in aquatic environments2017Doctoral 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.  

  • 7.
    Mathisen, Peter
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Andersson, Agneta
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Forsman, Mats
    Division of CBRN Defence and Security, Swedish Defence Research Agency, FOI, SE-901 82 Umeå, Sweden.
    Noppa, Laila
    Division of CBRN Defence and Security, Swedish Defence Research Agency, FOI, SE-901 82 Umeå, Sweden.
    Sjöstedt, Anders
    Umeå University, Faculty of Medicine, Department of Clinical Microbiology.
    Thelaus, Johanna
    Division of CBRN Defence and Security, Swedish Defence Research Agency, FOI, SE-901 82 Umeå, Sweden.
    Francisella tularensis subspecies holarctica´s adaptation to protozoan and mammal hostsManuscript (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.

  • 8.
    Mathisen, Peter
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Thelaus, J
    Sjöstedt de Luna, Sara
    Umeå University, Faculty of Science and Technology, Department of Mathematics and Mathematical Statistics.
    Andersson, Agneta
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Rapid adaptation of predation resistance in bacteria isolated from a seawater microcosm2016In: Aquatic Microbial Ecology, ISSN 0948-3055, E-ISSN 1616-1564, Vol. 78, no 2, p. 81-92Article in journal (Refereed)
    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.

  • 9. Thelaus, J
    et al.
    Andersson, A
    Broman, T
    Bäckman, S
    Granberg, M
    Karlsson, L
    Kuoppa, K
    Larsson, E
    Lundmark, E
    Lundström, JO
    Mathisen, Peter
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Näslund, J
    Schafer, M
    Wahab, T
    Forsman, M
    Francisella tularensis subspecies holarctica occurs in swedish mosquitoes, persists through the developmental stages of laboratory-infected mosquitoes and is transmissible during blood feeding2014In: Microbial Ecology, ISSN 0095-3628, E-ISSN 1432-184X, Vol. 67, no 1, p. 96-107Article in journal (Refereed)
    Abstract [en]

    In Sweden, mosquitoes are considered the major vectors of the bacterium Francisella tularensis subsp. holarctica, which causes tularaemia. The aim of this study was to investigate whether mosquitoes acquire the bacterium as aquatic larvae and transmit the disease as adults. Mosquitoes sampled in a Swedish area where tularaemia is endemic (A-rebro) were positive for the presence of F. tularensis deoxyribonucleic acid throughout the summer. Presence of the clinically relevant F. tularensis subsp. holarctica was confirmed in 11 out of the 14 mosquito species sampled. Experiments performed using laboratory-reared Aedes aegypti confirmed that F. tularensis subsp. holarctica was transstadially maintained from orally infected larvae to adult mosquitoes and that 25 % of the adults exposed as larvae were positive for the presence of F. tularensis-specific sequences for at least 2 weeks. In addition, we found that F. tularensis subsp. holarctica was transmitted to 58 % of the adult mosquitoes feeding on diseased mice. In a small-scale in vivo transmission experiment with F. tularensis subsp. holarctica-positive adult mosquitoes and susceptible mice, none of the animals developed tularaemia. However, we confirmed that there was transmission of the bacterium to blood vials by mosquitoes that had been exposed to the bacterium in the larval stage. Taken together, these results provide evidence that mosquitoes play a role in disease transmission in part of Sweden where tularaemia recurs.

  • 10.
    Thelaus, Johanna
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Andersson, Agneta
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Marine Sciences Centre (UMF).
    Mathisen, Peter
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Forslund, A-L
    Forsman, Mats
    Influence of nutrient status and grazing pressure on the fate of Francisella tularensis in lake water2009In: FEMS Microbiology Ecology, ISSN 0168-6496, E-ISSN 1574-6941, Vol. 67, no 1, p. 69-80Article in journal (Refereed)
    Abstract [en]

    The natural reservoir of Francisella tularensis, the causative agent of tularaemia, is yet to be identified. We investigated the possibility that Francisella persists in natural aquatic ecosystems between outbreaks. It was hypothesized that nutrientrich environments, with strong protozoan predation, favour the occurrence of the tularaemia bacterium. To investigate the differences in adaptation to aquatic environments of the species and subspecies of Francisella, we screened 23 strains for their ability to survive grazing by the ciliate Tetrahymena pyriformis. All the Francisella strains tested were consumed at a low rate, although significant differences between subspecies were found. The survival and virulence of gfp-labelled F. tularensis ssp. holarctica were then studied in a microcosm experiment using natural lake water, with varying food web complexities and nutrient availabilities. High nutrient conditions in combination with high abundances of nanoflagellates were found to favour F. tularensis ssp. holarctica. The bacterium was observed both free-living and within the cells of a nanoflagellate. Francisella tularensis entered a viable but nonculturable state during the microcosm experiment. When studied over a longer period of time, F. tularensis ssp. holarctica survived in the lake water, but loss of virulence was not prevented by either high nutrient availability or the presence of predators.

  • 11.
    Thelaus, Johanna
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Andersson, Agneta
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Marine Sciences Centre (UMF).
    Mathisen, Peter
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Forslund, Anna-Lena
    Forsman, Mats
    Influence of nutrient status and microbial food web structure on the fate of Francisella tularensis in lake waterIn: Article in journal (Refereed)
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