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Granéli, Edna
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Frangoulis, C., Christou, E. D., Varkitzi, I., Zervoudaki, S., Maneiro, I., Svensen, C., . . . Granéli, E. (2022). Impact of a Dinophysis acuminata Bloom on the Copepod Acartia clausi: First Indications. Water, 14(14), Article ID 2204.
Open this publication in new window or tab >>Impact of a Dinophysis acuminata Bloom on the Copepod Acartia clausi: First Indications
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2022 (English)In: Water, E-ISSN 2073-4441, Vol. 14, no 14, article id 2204Article in journal (Refereed) Published
Abstract [en]

Faecal pellet production and content along with egg production of the dominant copepod species Acartia clausi were studied in the Thermaikos Gulf (NW Aegean Sea) during a pre-bloom and a bloom of the toxic dinoflagellate Dinophysis acuminata. Both faecal pellet production (6.8-8.6 ind(-1) d(-1)) and egg production (15.8-47.6 ind(-1) d(-1)) appeared unrelated to the D. acuminata bloom. Less than 11% of the copepod faecal pellets contained one or two D. acuminata cells, almost intact, whereas the other material in the pellets was broken into small pieces or amorphous shapes. The toxin outflux seemed to be insignificant when compared to the mean toxin concentration from the whole D. acuminata population. Finally, the potential grazing impact of A. clausi on D. acuminata during the study period was low.

Place, publisher, year, edition, pages
MDPI, 2022
Keywords
Acartia clausi, Dinophysis acuminata, egg production, faecal pellet, HAB
National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-116101 (URN)10.3390/w14142204 (DOI)000833785300001 ()2-s2.0-85137263715 (Scopus ID)
Available from: 2022-09-02 Created: 2022-09-02 Last updated: 2023-08-28Bibliographically approved
McNamee, S. E., Medlin, L. K., Kegel, J., McCoy, G. R., Raine, R., Barra, L., . . . Campbell, K. (2016). Distribution, occurrence and biotoxin composition of the main shellfish toxin producing microalgae within European waters: A comparison of methods of analysis. Harmful Algae, 55, 112-120
Open this publication in new window or tab >>Distribution, occurrence and biotoxin composition of the main shellfish toxin producing microalgae within European waters: A comparison of methods of analysis
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2016 (English)In: Harmful Algae, ISSN 1568-9883, E-ISSN 1878-1470, Vol. 55, p. 112-120Article in journal (Refereed) Published
Abstract [en]

Harmful algal blooms (HABs) are a natural global phenomena emerging in severity and extent. Incidents have many economic, ecological and human health impacts. Monitoring and providing early warning of toxic HABs are critical for protecting public health. Current monitoring programmes include measuring the number of toxic phytoplankton cells in the water and biotoxin levels in shellfish tissue. As these efforts are demanding and labour intensive, methods which improve the efficiency are essential. This study compares the utilisation of a multitoxin surface plasmon resonance (multitoxin SPR) biosensor with enzyme-linked immunosorbent assay (ELISA) and analytical methods such as high performance liquid chromatography with fluorescence detection (HPLC-FLD) and liquid chromatography-tandem mass spectrometry (LC-MS/MS) for toxic HAB monitoring efforts in Europe. Seawater samples (n = 256) from European waters, collected 2009-2011, were analysed for biotoxins: saxitoxin and analogues, okadaic acid and dinophysistoxins 1/2 (VDU /DTX2) and domoic acid responsible for paralytic shellfish poisoning (PSP), diarrheic shellfish poisoning (DSP) and amnesic shellfish poisoning (ASP), respectively. Biotoxins were detected mainly in samples from Spain and Ireland. France and Norway appeared to have the lowest number of toxic samples. Both the multitoxin SPR biosensor and the RNA microarray were more sensitive at detecting toxic HABs than standard light microscopy phytoplankton monitoring. Correlations between each of the detection methods were performed with the overall agreement, based on statistical 2 x 2 comparison tables, between each testing platform ranging between 32% and 74% for all three toxin families illustrating that one individual testing method may not be an ideal solution. An efficient early warning monitoring system for the detection of toxic HABs could therefore be achieved by combining both the multitoxin SPR biosensor and RNA microarray. (C) 2016 Elsevier B.V. All rights reserved.

Keywords
Harmful algal bloom, Microarray, Biosensor, Saxitoxin, Okadaic acid, Domoic acid
National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-54690 (URN)10.1016/j.hal.2016.02.008 (DOI)000377323300011 ()2-s2.0-84960497178 (Scopus ID)
External cooperation:
Available from: 2016-07-22 Created: 2016-07-21 Last updated: 2017-11-28Bibliographically approved
Lundgren, V., Glibert, P. M., Granéli, E., Vidyarathna, N. K., Fiori, E., Ou, L., . . . Hansen, P. J. (2016). Metabolic and physiological changes in Prymnesium parvum when grown under, and grazing on prey of, variable nitrogen:phosphorus stoichiometry. Harmful Algae, 55, 1-12
Open this publication in new window or tab >>Metabolic and physiological changes in Prymnesium parvum when grown under, and grazing on prey of, variable nitrogen:phosphorus stoichiometry
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2016 (English)In: Harmful Algae, ISSN 1568-9883, E-ISSN 1878-1470, Vol. 55, p. 1-12Article in journal (Refereed) Published
Abstract [en]

Mixotrophy is found in almost all classes of phytoplankton in a wide range of aquatic habitats ranging from oligotrophic to eutrophic marine and freshwater systems. Few studies have addressed how the nutritional status of the predator and/or the prey affects mixotrophic metabolism despite the realization that mixotrophy is important ecologically. Laboratory experiments were conducted to examine changes in growth rates and physiological states of the toxic haptophyte Prymnesium parvum when fed Rhodomonas sauna of varying nutritional status. Haemolytic activity of P. parvum and prey mortality of R. sauna were also measured. P. parvum cultures grown to be comparatively low in nitrogen (low-N), phosphorus (low-P) or low in both nutrients (low-NP) were mixed with low-NP, low-N, and low-P R. saline in all possible combinations, i.e., a 3 x 3 factorial design. N deficiency was obtained in the low-N cultures, while true P deficiency may not have been obtained in the low-P cultures. Mortality rates of R. salina (both due to ingestion and/or cell rupture as a function of grazing or toxic effects) were higher when R. sauna cells were low-P, N-rich, regardless of the nutritional state of P. parvum. Mortality rates were, however, directly related to the initial prey:predator cell ratios. On the other hand, growth of the predator was a function of nutritional status and a significant positive correlation was observed between growth rates of P. parvum and cell-specific depletion rates of N, whereas no such relationship was found between P. parvum growth rates and depletion rates of P. In addition, the greatest changes in chlorophyll content and stoichiometric ratios of P. parvum were observed in high N:P conditions. Therefore, P. parvum may show enhanced success under conditions of higher inorganic N:P, which are likely favored in the future due to increases in eutrophication and altered nutrient stoichiometry driven by anthropogenic nutrient loads that are increasingly enriched in N relative to P. (C) 2016 Elsevier B.V. All rights reserved.

Keywords
Mixotrophy, Variable stoichiometry, Nitrogen, Phosphorus, Prymnesium parvum
National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-54689 (URN)10.1016/j.hal.2016.01.002 (DOI)000377323300001 ()2-s2.0-84962162237 (Scopus ID)
Available from: 2016-07-22 Created: 2016-07-21 Last updated: 2018-11-15Bibliographically approved
Pérez Blanco, E., Karlsson, C., Pallon, J., Yasumoto, T. & Granéli, E. (2015). Cellular nutrient content measured with the nuclear microprobe and toxins produced by Dinophysis norvegica (Dinophyceae) from the Trondheim fjord (Norway). Aquatic Microbial Ecology, 75(3), 259-269
Open this publication in new window or tab >>Cellular nutrient content measured with the nuclear microprobe and toxins produced by Dinophysis norvegica (Dinophyceae) from the Trondheim fjord (Norway)
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2015 (English)In: Aquatic Microbial Ecology, ISSN 0948-3055, E-ISSN 1616-1564, Vol. 75, no 3, p. 259-269Article in journal (Refereed) Published
Abstract [en]

Dinophysis norvegica is a commonly occurring dinoflagellate species and a producer of diarrhetic shellfish poisons. Natural samples were collected from Trondheim fjord, Norway, to analyse nutrient (O, C, N, P) and toxin (dinophysitoxins [DXTs], okadaic acid [OA], pectenotoxins [PTXs]) content in D. norvegica cells. Nutrient and toxin analyses were also carried out on cells grown under nutrient-sufficient and nutrient-deficient conditions to determine how intracellular nutrient and toxin content varied under different nutrient availability conditions. Nutrient analyses were conducted using nuclear microprobe techniques that can accurately analyse single cells, and toxin analyses were carried out using liquid chromatography and mass spectroscopy. The intracellular carbon, nitrogen and phosphorus content in individual cells varied greatly, and intracellular C:N:P ratios showed that the cells were both N- and P-deficient when compared to the Redfield ratio. The ideal N:P ratio in the media for D. norvegica was found to be below the Redfield ratio, but intracellular ratios did not show a clear relationship with those in the media. N:P ratios of D. norvegica were higher than expected, which is likely due to their phagotrophy on zooplankon. The highest toxin values found were traces of PTX2, 24.72 pg PTX2SA cell(-1), 2.19 pg DTX1 cell(-1), and 1.01 pg OA cell(-1). However, we found no clear relationship between the content of intracellular nutrients and toxins.

Keywords
Dinophysis, Diarrhetic shellfish poisoning, Elemental cellular content, Mixotrophy, Nuclear microprobe, Nutrient ratios, Nutrients, Trondheim fjord
National Category
Biological Sciences
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-45825 (URN)10.3354/ame01762 (DOI)000358512400006 ()2-s2.0-84937910336 (Scopus ID)
Available from: 2015-08-21 Created: 2015-08-21 Last updated: 2017-12-07Bibliographically approved
Lundgren, V., Roelke, D. L., Brooks, B. W., Granéli, E., Davis, S. L., Baty, T. & Scott, W. C. (2015). Prymnesium parvum invasion success into coastal bays of the Gulf of Mexico: Galveston Bay case study. Harmful Algae, 43, 31-45
Open this publication in new window or tab >>Prymnesium parvum invasion success into coastal bays of the Gulf of Mexico: Galveston Bay case study
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2015 (English)In: Harmful Algae, ISSN 1568-9883, E-ISSN 1878-1470, Vol. 43, p. 31-45Article in journal (Refereed) Published
Abstract [en]

The toxic haptophyte Prymnesium parvum regularly forms fish-killing blooms in inland brackish water bodies in the south-central USA. Along the Texas coast smaller blooms have occurred in isolated areas. There appears to be an increasing risk that harmful P. parvum blooms will propagate into open coastal waters with implementation of future water plans. These plans will include increased interbasin water transfers from the Brazos River, regularly impacted by P. parvum blooms, to the San Jacinto-Brazos Coastal Basin, which ultimately flows into Galveston Bay (GB). Persisting source populations of P. parvum in inland waters elevates this risk. Thus, there is a need for an increased understanding of how P. parvum might perform in coastal waters, such as those found in GB. Here, two in-field experiments were conducted to investigate the influence of various plankton size-fractions of GB water on inoculated P. parvum during fall and winter, periods when blooms are typically initiating and developing inland. Stationary- and log-growth phase P. parvum were used to represent high and low toxicity initial conditions. Results revealed that P. parvum could grow in GB waters and cause acute mortality to silverside minnows (Menidia beryllina). Depending on season and growth phase, however, P. parvum growth and toxicity varied in different size fractions. During the fall, P. parvum inoculated from stationary-, but not log-growth phase culture, was negatively affected by bacteria-sized particles. During the winter, bacteria and nanoplankton together had a negative effect on P. parvum inoculated from stationary- and, to a lesser degree, log-growth phase cultures. Intermediate- and large-sized grazers when combined with bacteria and nanoplankton had complex relationships with inoculated P. parvum, sometimes stimulating and sometimes suppressing population growth. Toxicity to fish occurred in almost all plankton size fractions. The inclusion of progressively larger sized plankton fractions resulted in trends of decreased toxicity in treatments inoculated with stationary-, but not log-growth phase P. parvum in the fall. In the winter, however, inclusion of larger sized plankton fractions resulted in trends of increased toxicity to fish in treatments inoculated with both stationary- and log-growth phase P. parvum. This study indicates that understanding P. parvum population dynamics in open waters of estuaries and bays will be challenging, as there appears to be complex relationships with naturally occurring components of the plankton. The observations that P. parvum is able to grow to high population density and produce fish-killing levels of toxins underscores the need for advanced risk assessment studies, especially in light of water use plans that will result in P. parvum invasions of greater size. (C) 2015 Elsevier B.V. All rights reserved.

Keywords
Prymnesium parvum, Galveston Bay, Bacteria, Nanoplankton, Zooplankton, Golden algae
National Category
Biological Sciences
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-42832 (URN)10.1016/j.hal.2014.12.008 (DOI)000351968900004 ()2-s2.0-84924419892 (Scopus ID)
Available from: 2015-04-23 Created: 2015-04-23 Last updated: 2017-12-04Bibliographically approved
Ou, L., Lundgren, V., Lu, S. & Granéli, E. (2014). The effect of riverine dissolved organic matter and other nitrogen forms on the growth and physiology of the dinoflagellate Prorocentrum minimum (Pavillard) Schiller. Journal of Sea Research, 85, 499-507
Open this publication in new window or tab >>The effect of riverine dissolved organic matter and other nitrogen forms on the growth and physiology of the dinoflagellate Prorocentrum minimum (Pavillard) Schiller
2014 (English)In: Journal of Sea Research, ISSN 1385-1101, E-ISSN 1873-1414, ISSN 1385-1101, Vol. 85, p. 499-507Article in journal (Refereed) Published
Abstract [en]

The effect of various nitrogen (N) sources, including riverine dissolved organic matter (DOM), nitrate, ammonium, and urea, on the growth and physiology of the dinoflagellate Prorocentrum minimum was compared in a batch culture experiment. P. minimum grew equally well in the presence of identical amounts of nitrate, ammonium, and urea. Approximately 18 to 20% of organic N bound to the DOM was bioavailable. Although the available N added in the DOM treatment was only 1/3 of the amount of any other N sources, the cell densities of P. minimum in the DOM treatment increased to 61 ~ 65% of those in the nitrate, ammonium or urea treatment. The maximum specific growth rates did not differ significantly between the treatments with the highest in the ammonium treatment (0.55 ± 0.13 d- 1) and the lowest in the urea treatment (0.39 ± 0.04 d- 1). P. minimum assimilated the available DOM-bound N in a short period (fewer than 5 days), which was faster than utilizing urea. The increase in the cellular N:P ratios of P. minimum showed the alleviation of N stress in all the treatments after the addition of various N forms. The densities and cellular compositions of P. minimum stabilizing in all the treatments for the whole stationary phase indicated that P. minimum has adaptive physiology under sub-optimal conditions and is a competitive bloom species. We suggest that P. minimum cells utilize DOM-bound N for their growth, and the efficiency in utilizing the available DOM-bound N for growth is comparable to when P. minimum utilizes nitrate, ammonium or urea.

Place, publisher, year, edition, pages
Elsevier, 2014
Keywords
Dinoflagellates Prorocentrum minimum Dissolved organic matter Nitrogen The Baltic Sea
National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-28513 (URN)10.1016/j.seares.2013.08.005 (DOI)000329884700051 ()2-s2.0-84887824275 (Scopus ID)
Available from: 2013-08-27 Created: 2013-08-27 Last updated: 2017-12-06Bibliographically approved
Vidyarathna, N. K., Fiori, E., Lundgren, V. & Granéli, E. (2014). The effects of aeration on growth and toxicity of Prymnesium parvum grown with and without algal prey.. Harmful Algae, 39, 55-63
Open this publication in new window or tab >>The effects of aeration on growth and toxicity of Prymnesium parvum grown with and without algal prey.
2014 (English)In: Harmful Algae, ISSN 1568-9883, E-ISSN 1878-1470, Vol. 39, p. 55-63Article in journal (Refereed) Published
Abstract [en]

We investigated the effects of aeration on growth and toxicity of the haptophyte Prymnesium parvum in the presence and absence of the algal prey Rhodomonas salina. Batch monocultures of P-limited P. parvum and N and P sufficient R. salina and mixed cultures of the two microalgae were grown with no, low (20) and high (100) ml min1 aeration for 18 days. Cell growth of P. parvum and R. salina and cell toxicity of P.parvum were studied over the experimental period. The highest specific growth rates of P. parvum were found at low aeration rates. R. salina in monocultures showed typical growth patterns, while R. salina numbers declined rapidly in the mixed cultures. Of the initial cell densities, 98–100% of the R. salina cells were lysed or ingested within 24 h of mixing with P. parvum cells. The maxima P. parvum biomasses were significantly higher in the mixed cultures than in the monocultures. Cell toxicity of P. parvum increased significantly in response to aeration rates and the highest levels were found in the high aeration condition. Availability of prey and resupply of inorganic nutrients decreased P. parvum cell toxicity. Our study suggests that P. parvum is tolerant and is able to grow over a broad range of aeration and associated turbulence effects though low aeration represents an optimal condition for growth. As P. parvum toxicity was higher in the high aeration treatment we suggest that the higher concentrations of oxygen cause more toxins to be produced, as these are oxygen rich compounds. We suggest that oxygenation and turbulence of surface waters caused by mixing may be involved in promoting high toxic P. parvum blooms in shallow lakes and coastal waters.

Place, publisher, year, edition, pages
Elsevier, 2014
Keywords
Prymnesium parvum; Aeration effect; Hemolytic activity; Cell growth; Mixotrophy
National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-36271 (URN)10.1016/j.hal.2014.06.010 (DOI)000345469100006 ()2-s2.0-84908426038 (Scopus ID)
Available from: 2014-08-04 Created: 2014-08-04 Last updated: 2018-10-24Bibliographically approved
Mitra, A., Flynn, K. J., Burkholder, J., Berge, T., Calbet, A., Raven, J. A., . . . Zubkov, M. V. (2014). The role of mixotrophic protists in the biological carbon pump. Biogeosciences, 11, 995-1005
Open this publication in new window or tab >>The role of mixotrophic protists in the biological carbon pump
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2014 (English)In: Biogeosciences, ISSN 1726-4170, E-ISSN 1726-4189, Vol. 11, p. 995-1005Article in journal (Refereed) Published
Abstract [en]

The traditional view of the planktonic foodweb describes consumption of inorganic nutrientsby photo-autotrophic phytoplankton, which in turn supports zooplankton and ultimately higher trophic levels. Pathways centred on bacteria provide mechanisms for nutrient recycling. This structure lies at the foundation of most models used to explore biogeochemical cycling, functioning of the biological pump, and the impact of climate change on these processes. We suggest an alternative paradigm, which sees the bulk of the base of this foodweb supported by protist plankton (phytoplankton and microzooplankton) communities that are mixotrophic – combining phototrophy and phagotrophy within a single cell. The photoautotrophic eukaryotic plankton and their heterotrophic microzooplankton grazers dominate only within immature environments (e.g., spring bloom in temperate systems). With their flexible nutrition, mixotrophic protists dominate in more mature systems (e.g., temperate summer, established eutrophic systems and oligotrophic systems); the more stable water columns suggested under climate change may also be expected to favour these mixotrophs. We explore how such a predominantlymixotrophic structure affects microbial trophic dynamics and the biological pump. The mixotroph dominated structure differs fundamentally in its flow of energy and nutrients, with a shortened and potentially more efficient chain from nutrient regeneration to primary production. Furthermore, mixotrophy enables a direct conduit for the support of primary production from bacterial production. We show how the exclusion of an explicit mixotrophic component in studies of the pelagic microbial communities leads to a failure to capture the true dynamics of the carbon flow. In order to prevent a misinterpretation of the full implications of climate change upon biogeochemical cyclingand the functioning of the biological pump, we recommend inclusion of multi-nutrient mixotroph models within ecosystem studies.

Keywords
carbon; mixotrophy; protists; modelling
National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-28228 (URN)10.5194/bg-11-995-2014 (DOI)000334100300007 ()2-s2.0-84897646764 (Scopus ID)
Available from: 2013-08-16 Created: 2013-08-16 Last updated: 2019-01-23Bibliographically approved
Pérez Blanco, E., Karlsson, C., Pallon, J. & Granéli, E. (2013). Composition of carbon, nitrogen and phosphorus in single cells of three filamentous cyanobacteria using nuclear microprobe and traditional techniques. Aquatic Microbial Ecology, 71(1), 91-97
Open this publication in new window or tab >>Composition of carbon, nitrogen and phosphorus in single cells of three filamentous cyanobacteria using nuclear microprobe and traditional techniques
2013 (English)In: Aquatic Microbial Ecology, ISSN 0948-3055, E-ISSN 1616-1564, Vol. 71, no 1, p. 91-97Article in journal (Refereed) Published
Abstract [en]

Intracellular contents of carbon, nitrogen and phosphorus in phytoplankton cells are traditionally measured using concentrates containing thousands to millions of cells. In this study we have used a Nuclear MicroProbe (NMP) as an approach for the determination of C, N and P concentrations in single filaments of three cyanobacteria species: Anabaena sp., Nodularia spumigena and Aphanizomenon flos-aquae var. klebahnii isolated from Baltic Sea water. Estimations of C, N and P content per cell have been calculated and compared with the concentrations found with traditional bulk methods. No significant differences regarding the C, N and P cellular content were found between the two methods for each of the species tested (p < 0.05). From our results we conclude that the use of NMP can be a useful tool for studying the elemental contents in single phytoplankton cells

National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-30467 (URN)10.3354/ame01665 (DOI)000327552900007 ()2-s2.0-84889071168 (Scopus ID)
Available from: 2013-11-18 Created: 2013-11-18 Last updated: 2017-12-06Bibliographically approved
Lindh, M. V., Riemann, L., Baltar, F., Romero-Oliva, C., Salomon, P., Granéli, E. & Pinhassi, J. (2013). Consequences of increased temperature and acidification on bacterioplankton community composition during a mesocosm spring bloom in the Baltic Sea. Environmental Microbiology Reports, 5(2), 252-262
Open this publication in new window or tab >>Consequences of increased temperature and acidification on bacterioplankton community composition during a mesocosm spring bloom in the Baltic Sea
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2013 (English)In: Environmental Microbiology Reports, ISSN 1758-2229, E-ISSN 1758-2229, Vol. 5, no 2, p. 252-262Article in journal (Refereed) Published
Abstract [en]

Despite the paramount importance of bacteria for biogeochemical cycling of carbon and nutrients, little is known about the potential effects of climate change on these key organisms. The consequences of the projected climate change on bacterioplankton community dynamics were investigated in a Baltic Sea spring phytoplankton bloom mesocosm experiment by increasing temperature with 3°C and decreasing pH by approximately 0.4 units via CO2 addition in a factorial design. Temperature was the major driver of differences in community composition during the experiment, as shown by denaturing gradient gel electrophoresis (DGGE) of amplified 16S rRNA gene fragments. Several bacterial phylotypes belonging to Betaproteobacteria were predominant at 3°C but were replaced by members of the Bacteriodetes in the 6°C mesocosms. Acidification alone had a limited impact on phylogenetic composition, but when combined with increased temperature, resulted in the proliferation of specific microbial phylotypes. Our results suggest that although temperature is an important driver in structuring bacterioplankton composition, evaluation of the combined effects of temperature and acidification is necessary to fully understand consequences of climate change for marine bacterioplankton, their implications for future spring bloom dynamics, and their role in ecosystem functioning.

National Category
Ecology
Research subject
Ecology, Aquatic Ecology
Identifiers
urn:nbn:se:lnu:diva-22627 (URN)10.1111/1758-2229.12009 (DOI)000315851200008 ()23584969 (PubMedID)2-s2.0-84874716930 (Scopus ID)
Available from: 2012-11-27 Created: 2012-11-27 Last updated: 2021-05-05Bibliographically approved
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