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  • 1. Bay, Guillaume
    et al.
    Nahar, Nurun
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Oubre, Matthieu
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Whitehouse, Martin J.
    Wardle, David A.
    Zackrisson, Olle
    Nilsson, Marie-Charlotte
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Boreal feather mosses secrete chemical signals to gain nitrogen2013In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 200, no 1, p. 54-60Article in journal (Refereed)
    Abstract [en]

    The mechanistic basis of feather moss-cyanobacteria associations, a main driver of nitrogen (N) input into boreal forests, remains unknown. Here, we studied colonization by Nostoc sp. on two feather mosses that form these associations (Pleurozium schreberi and Hylocomium splendens) and two acrocarpous mosses that do not (Dicranum polysetum and Polytrichum commune). We also determined how N availability and moss reproductive stage affects colonization, and measured N transfer from cyanobacteria to mosses. The ability of mosses to induce differentiation of cyanobacterial hormogonia, and of hormogonia to then colonize mosses and re-establish a functional symbiosis was determined through microcosm experiments, microscopy and acetylene reduction assays. Nitrogen transfer between cyanobacteria and Pleurozium schreberi was monitored by secondary ion mass spectrometry (SIMS). All mosses induced hormogonia differentiation but only feather mosses were subsequently colonized. Colonization on Pleurozium schreberi was enhanced during the moss reproductive phase but impaired by elevated N. Transfer of N from cyanobacteria to their host moss was observed. Our results reveal that feather mosses likely secrete species-specific chemo-attractants when N-limited, which guide cyanobacteria towards them and from which they gain N. We conclude that this signalling is regulated by N demands of mosses, and serves as a control of N input into boreal forests.

  • 2.
    Bergman, Birgitta
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Rai, Amar N
    Cyanobacterial Associations2007In: Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations., Kluwer Academic Publishers, Dordrecht , 2007, p. 257-301Chapter in book (Other academic)
  • 3.
    Berntzon, Lotta
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Erasmie, Sven
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Celepli, Narin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Eriksson, Johan
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    BMAA Inhibits Nitrogen Fixation in the Cyanobacterium Nostoc sp PCC 71202013In: Marine Drugs, ISSN 1660-3397, E-ISSN 1660-3397, Vol. 11, no 8, p. 3091-3108Article in journal (Refereed)
    Abstract [en]

    Cyanobacteria produce a range of secondary metabolites, one being the neurotoxic non-protein amino acid beta-N-methylamino-L-alanine (BMAA), proposed to be a causative agent of human neurodegeneration. As for most cyanotoxins, the function of BMAA in cyanobacteria is unknown. Here, we examined the effects of BMAA on the physiology of the filamentous nitrogen-fixing cyanobacterium Nostoc sp. PCC 7120. Our data show that exogenously applied BMAA rapidly inhibits nitrogenase activity (acetylene reduction assay), even at micromolar concentrations, and that the inhibition was considerably more severe than that induced by combined nitrogen sources and most other amino acids. BMAA also caused growth arrest and massive cellular glycogen accumulation, as observed by electron microscopy. With nitrogen fixation being a process highly sensitive to oxygen species we propose that the BMAA effects found here may be related to the production of reactive oxygen species, as reported for other organisms.

  • 4. Gorelova, O. A.
    et al.
    Baulina, O. I.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Koksharova, O. A.
    The pleiotropic effects of ftn2 and ftn6 mutations in cyanobacterium Synechococcus sp PCC 79422013In: Protoplasma, ISSN 0033-183X, E-ISSN 1615-6102, Vol. 250, no 4, p. 931-942Article in journal (Refereed)
    Abstract [en]

    Two cell division mutants (Ftn2 and Ftn6) of the cyanobacterium Synechococcus sp. PCC 7942 were studied using scanning electron microscopy and transmission electron microscopy methods. This included negative staining and ultrathin section analysis. Different morphological and ultrastructural features of mutant cells were identified. Ftn2 and Ftn6 mutants exhibited particularly elongated cells characterized by significantly changed shape in comparison with the wild type. There was irregular bending, curving, spiralization, and bulges as well as cell branching. Elongated mutant cells were able to initiate cytokinesis simultaneously in several division sites which were localized irregularly along the cell. Damaged rigidity of the cell wall was typical of many cells for both mutants. Thylakoids of mutants showed modified arrangement and ultrastructural organization. Carboxysome-like structures without a shell and/or without accurate polyhedral packing protein particles were often detected in the mutants. However, in the case of Ftn2 and Ftn6, the average number of carboxysomes per section was less than in the wild type by a factor of 4 and 2, respectively. These multiple morphological and ultrastructural changes in mutant cells evinced pleiotropic responses which were induced by mutations in cell division genes ftn2 and ftn6. Ultrastructural abnormalities of Ftn2 and Ftn6 mutants were consistent with differences in their proteomes. These results could support the significance of FTN2 and FTN6 proteins for both cyanobacterial cell division and cellular physiology.

  • 5.
    Ininbergs, Karolina
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Bay, Guillaume
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Wardle, David A.
    Nilsson, Marie-Charlotte
    Composition and diversity of nifH genes of nitrogen-fixing cyanobacteria associated with boreal forest feather mosses2011In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 192, no 2, p. 507-517Article in journal (Refereed)
    Abstract [en]

    Recent studies have revealed that nitrogen fixation by cyanobacteria living in association with feather mosses is a major input of nitrogen to boreal forests. We characterized the community composition and diversity of cyanobacterial nifH phylotypes associated with each of two feather moss species (Pleurozium schreberi and Hylocomium splendens) on each of 30 lake islands varying in ecosystem properties in northern Sweden. Nitrogen fixation was measured using acetylene reduction, and nifH sequences were amplified using general and cyanobacterial selective primers, separated and analyzed using density gradient gel electrophoresis (DGGE) or cloning, and further sequenced for phylogenetic analyses. Analyses of DGGE fingerprinting patterns revealed two host-specific clusters (one for each moss species), and sequence analysis showed five clusters of nifH phylotypes originating from heterocystous cyanobacteria. For H. splendens only, N(2) fixation was related to both nifH composition and diversity among islands. We demonstrated that the cyanobacterial communities associated with feather mosses show a high degree of host specificity. However, phylotype composition and diversity, and nitrogen fixation, did not differ among groups of islands that varied greatly in their availability of resources. These results suggest that moss species identity, but not extrinsic environmental conditions, serves as the primary determinant of nitrogen-fixing cyanobacterial communities that inhabit mosses.

  • 6.
    Jiang, Liying
    et al.
    Stockholm University, Faculty of Science, Department of Analytical Chemistry.
    Eriksson, Johan
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Lage, Sandra
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Jonasson, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Shams, Shiva
    Mehine, Martin
    Stockholm University, Faculty of Science, Department of Analytical Chemistry.
    Ilag, Leopold L.
    Stockholm University, Faculty of Science, Department of Analytical Chemistry.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Diatoms: A Novel Source for the Neurotoxin BMAA in Aquatic Environments2014In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 1, article id e84578Article in journal (Refereed)
    Abstract [en]

    Amyotrophic lateral sclerosis (ALS) or Lou Gehrig's disease is a neurological disorder linked to environmental exposure to a non-protein amino acid, beta-N-methylamino-L-alanine (BMAA). The only organisms reported to be BMAA-producing, are cyanobacteria - prokaryotic organisms. In this study, we demonstrate that diatoms - eukaryotic organisms - also produce BMAA. Ultra-high-performance liquid chromatography coupled with tandem mass spectrometry revealed the occurrence of BMAA in six investigated axenic diatom cultures. BMAA was also detected in planktonic field samples collected on the Swedish west coast that display an overrepresentation of diatoms relative to cyanobacteria. Given the ubiquity of diatoms in aquatic environments and their central role as primary producers and the main food items of zooplankton, the use of filter and suspension feeders as livestock fodder dramatically increases the risk of human exposure to BMAA-contaminated food.

  • 7.
    Jonasson, Sara
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Eriksson, Johan
    Stockholm University, Faculty of Science, Department of Botany.
    Berntzon, Lotta
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Botany.
    A novel cyanobacterial toxin (BMAA) with potential neurodegenerative effects2008In: Plant Biotechnology, ISSN 1342-4580, E-ISSN 1347-6114, Vol. 25, no 3, p. 227-232Article in journal (Refereed)
    Abstract [en]

    The non-protein amino acid beta-N-methyl-amino-L-alanine (BMAA) is a neurotoxin that was recently found to be produced by most cyanobacteria. The neurotoxin was discovered in 1967 in the seeds of the cycad Cycas micronesica, but this BMAA may originate from the symbiotic cyanobacterium Nostoc, which inhabits the roots of cycads. BMAA is thought to be the cause of the deadly neurodegenerative disease amyotrophic lateral sclerosis/parkinsonism dementia complex (ALS/PDC), common among the Chamorro people of Guam. It was demonstrated that the Chamorros, in all probability, have been exposed to high levels of BMAA through dietary consumption of flying foxes which fed mainly on cycads seeds. BMAA production may be a common conserved evolutionary feature among cyanobacteria and due to their wide global distribution, the toxin may be a common concern and potentially involved in provoking degenerative diseases worldwide. BMAA may likewise be bioaccumulated in other cyanobacterial based food webs within ecosystems outside Guam, and it is proposed that such webs may exist in the Baltic Sea, with its massive occurrence of cyanobacteria (blooms).

  • 8.
    Jonasson, Sara
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Eriksson, Johan
    Stockholm University, Faculty of Science, Department of Botany.
    Berntzon, Lotta
    Stockholm University, Faculty of Science, Department of Botany.
    Spacil, Zdenek
    Stockholm University, Faculty of Science, Department of Analytical Chemistry. Charles University Prague, Czech Republic .
    Ilag, Leopold L.
    Stockholm University, Faculty of Science, Department of Analytical Chemistry.
    Ronnevi, Lars-Olof
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Botany.
    Transfer of a cyanobacterial neurotoxin within a temperate aquatic ecosystem suggests pathways for human exposure2010In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 107, no 20, p. 9252-9257Article in journal (Refereed)
    Abstract [en]

    beta-methylamino-L-alanine (BMAA), a neurotoxic nonprotein amino acid produced by most cyanobacteria, has been proposed to be the causative agent of devastating neurodegenerative diseases on the island of Guam in the Pacific Ocean. Because cyanobacteria are widespread globally, we hypothesized that BMAA might occur and bioaccumulate in other ecosystems. Here we demonstrate, based on a recently developed extraction and HPLC-MS/MS method and long-term monitoring of BMAA in cyanobacterial populations of a temperate aquatic ecosystem (Baltic Sea, 2007-2008), that BMAA is biosynthesized by cyanobacterial genera dominating the massive surface blooms of this water body. BMAA also was found at higher concentrations in organisms of higher trophic levels that directly or indirectly feed on cyanobacteria, such as zooplankton and various vertebrates (fish) and invertebrates (mussels, oysters). Pelagic and benthic fish species used for human consumption were included. The highest BMAA levels were detected in the muscle and brain of bottom-dwelling fishes. The discovery of regular biosynthesis of the neurotoxin BMAA in a large temperate aquatic ecosystem combined with its possible transfer and bioaccumulation within major food webs, some ending in human consumption, is alarming and requires attention.

  • 9.
    Klint, Johan
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Ran, Liang
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Botany.
    Identification of developmentally regulated proteins in cyanobacterial hormogonia using a proteomic approach.2006In: Symbiosis, ISSN 0334-5114, Vol. 41, no 2, p. 87-95Article in journal (Refereed)
  • 10.
    Klint, Johan
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Botany.
    FtsZ may have dual roles in the filamentous cyanobacterium Nostoc/Anabaena sp. strain PCC 7120.2007In: J Plant Physiol, ISSN 0176-1617, Vol. 164, no 1, p. 11-8Article in journal (Refereed)
  • 11. Koksharova, Olga A
    et al.
    Klint, Johan
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Comparative proteomics of cell division mutants and wild-type of Synechococcus sp. strain PCC 7942.2007In: Microbiology, ISSN 1350-0872, Vol. 153, no Pt 8, p. 2505-2517Article in journal (Refereed)
  • 12. Koksharova, Olga A
    et al.
    Klint, Johan
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    The first protein map of Synechococcus sp. strain PCC 79422006In: Mikrobiologiia, ISSN 0026-3656, Vol. 75, no 6, p. 765-74Article in journal (Refereed)
  • 13.
    Lage, Sandra
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Annadotter, Helene
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rydberg, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Biotransfer of beta-N-Methylamino-l-alanine (BMAA) in a Eutrophicated Freshwater Lake2015In: Marine Drugs, ISSN 1660-3397, E-ISSN 1660-3397, Vol. 13, no 3, p. 1185-1201Article in journal (Refereed)
    Abstract [en]

    beta-N-Methylamino-l-alanine (BMAA), a neurotoxic non-protein amino acid, plays a significant role as an environmental risk factor in neurodegenerative diseases, such as amyotrophic lateral sclerosis. BMAA producers occur globally, colonizing almost all habitats and represent species from distinct phytoplanktonic groups, i.e., cyanobacteria, diatoms, and dinoflagellates. Bioaccumulation of BMAA in invertebrate and vertebrate organisms has also been registered around the globe. In the Baltic Sea, BMAA has been detected in several commercial fish species, raising the question of the bioaccumulation of BMAA in Swedish limnic systems. Here we find the presence of BMAA in water samples from Lake Finjasjon and identify its bioaccumulation patterns in both plankti-benthivorous and piscivorous fish, according to fish species, total weight, gender, and season of collection. For the first time, a large number of fish individuals were used in order to draw conclusions on BMAA bioaccumulation in a closed ecological community based on a statistical approach. We may, therefore, conclude that feeding patterns (plankti-benthivorous) and increased age of fish may lead to a higher tissue concentration of BMAA.

  • 14.
    Lage, Sandra
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Burian, Alfred
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Costa, Pedro Reis
    Annadotter, Heléne
    Godhe, Anna
    Rydberg, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    BMAA extraction of cyanobacteria samples: which method to choose?2016In: Environmental science and pollution research international, ISSN 0944-1344, E-ISSN 1614-7499, Vol. 23, no 1, p. 338-350Article in journal (Refereed)
    Abstract [en]

    beta-N-Methylamino-l-alanine (BMAA), a neurotoxin reportedly produced by cyanobacteria, diatoms and dinoflagellates, is proposed to be linked to the development of neurological diseases. BMAA has been found in aquatic and terrestrial ecosystems worldwide, both in its phytoplankton producers and in several invertebrate and vertebrate organisms that bioaccumulate it. LC-MS/MS is the most frequently used analytical technique in BMAA research due to its high selectivity, though consensus is lacking as to the best extraction method to apply. This study accordingly surveys the efficiency of three extraction methods regularly used in BMAA research to extract BMAA from cyanobacteria samples. The results obtained provide insights into possible reasons for the BMAA concentration discrepancies in previous publications. In addition and according to the method validation guidelines for analysing cyanotoxins, the TCA protein precipitation method, followed by AQC derivatization and LC-MS/MS analysis, is now validated for extracting protein-bound (after protein hydrolysis) and free BMAA from cyanobacteria matrix. BMAA biological variability was also tested through the extraction of diatom and cyanobacteria species, revealing a high variance in BMAA levels (0.0080-2.5797 mu g g(-1) DW).

  • 15.
    Lage, Sandra
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Reis Costa, Pedro
    Moita, Teresa
    Eriksson, Johan
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Jonasson Rydberg, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    BMAA in shellfish from two Portuguese transitional water bodies suggests the marine dinoflagellate Gymnodinium catenatum as a potential BMAA source2014In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 152, p. 131-138Article in journal (Refereed)
    Abstract [en]

    The neurotoxin -N-methylamino-l-alanine (BMAA) and its putative role in multiple neurodegenera-tive diseases have been intensely studied since 2005 when the toxin was discovered to be producedby worldwide-distributed cyanobacterial species inhabiting terrestrial, marine, brackish, and freshwaterecosystems. Recently, BMAA production was also associated with one eukaryotic group, namely, diatoms,raising questions about its production by other phytoplanktonic groups. To test for BMAA bioavailabilityin ecosystems where abundant phytoplanktonic blooms regularly occur, samples of filter-feeding shell-fish were collected in two Portuguese transitional water bodies. BMAA content in cockles (Cerastodermaedule) collected weekly between September and November 2009 from Ria de Aveiro and at least once amonth from May to November from Ria Formosa, fluctuated from 0.079 ± 0.055 to 0.354 ± 0.066 g/g DWand from below the limit of detection to 0.434 ± 0.110 g/g DW, respectively. Simultaneously to BMAAoccurrence in cockles, paralytic shellfish toxins were detected in shellfish as a result of Gymnodiniumcatenatum blooms indicating a possible link between this marine dinoflagellate and BMAA production.Moreover, considerable high BMAA levels, 0.457 ± 0.186 g/g DW, were then determined in a laboratorygrown culture of G. catenatum. This work reveals for the first time the presence of BMAA in shellfishfrom Atlantic transitional water bodies and consubstantiate evidences of G. catenatum as one of the mainsources of BMAA in these ecosystems.

  • 16.
    Lindberg, Sylvia
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Premkumar, Albert
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Schulz, Alexander
    Lager, Ida
    Phospholipases AtPLD1 and AtPLD2 function differently in hypoxia2018In: Physiologia Plantarum: An International Journal for Plant Biology, ISSN 0031-9317, E-ISSN 1399-3054, Vol. 162, no 1, p. 98-108Article in journal (Refereed)
    Abstract [en]

    Besides hydrolyzing different membrane phospholipids, plant phospholipases D and molecular species of their byproducts phosphatidic acids (PLDs/PAs) are involved in diverse cellular events such as membrane-cytoskeleton dynamics, hormone regulation and biotic and/or abiotic stress responses at cellular or subcellular levels. Among the 12 Arabidopsis PLD genes, PLD1 and PLD2 uniquely possess Ca2+-independent phox (PX) and pleckstrin (PH) homology domains. Here, we report that mutants deficient in these PLDs, pld1 and pld2, show differential sensitivities to hypoxia stimulus. In the present study, we used protoplasts of wild type and mutants and compared the hypoxia-induced changes in the levels of three major signaling mediators such as cytoplasmic free calcium [Ca-cyt.(2+)], hydrogen peroxide (H2O2) and PA. The concentrations of cytosolic Ca2+ and H2O2 were determined by fluorescence microscopy and the fluorescent dyes Fura 2-AM and CM-H(2)DCFDA, specific for calcium and H2O2, respectively, while PA production was analyzed by an enzymatic method. The study reveals that AtPLD1 is involved in reactive oxygen species (ROS) signaling, whereas AtPLD2 is involved in cytosolic Ca2+ signaling pathways during hypoxic stress. Hypoxia induces an elevation of PA level both in Wt and pld1, while the PA level is unchanged in pld2. Thus, it is likely that AtPLD2 is involved in PA production by a calcium signaling pathway, while AtPLD1 is more important in ROS signaling.

  • 17. Orcutt, Karen M.
    et al.
    Gundersen, Kjell
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Another look at green Trichodesmium colonies2008In: Limnology and oceanography, Vol. 53, no 5, p. 2049-2051Article in journal (Refereed)
  • 18. Papaefthimiou, Dimitra
    et al.
    Hrouzek, Pavel
    Mugnai, Maria Angela
    Lukesova, Alena
    Turicchia, Silvia
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Ventura, Stefano
    Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria.2008In: Int J Syst Evol Microbiol, ISSN 1466-5026, Vol. 58, no Pt 3, p. 553-64Article in journal (Other academic)
    Abstract [en]

    Many cyanobacteria commonly identified as belonging to the genus Nostoc are well-known cyanobionts (symbionts) of a wide variety of plants and fungi. They form symbioses with bryophytes, pteridophytes, gymnosperms and angiosperms that are considerably different in the type of reciprocal interaction between the host and the cyanobiont. The phylogenetic and taxonomic relationships among cyanobionts isolated from different hosts and Nostoc strains isolated from free-living conditions are still not well understood. We compared phylogeny and morphology of symbiotic cyanobacteria originating from different host plants (genera Gunnera, Azolla, Cycas, Dioon, Encephalartos, Macrozamia and Anthoceros) with free-living Nostoc isolates originating from different habitats. After preliminary clustering with ARDRA (amplified rDNA restriction analysis), phylogeny was reconstructed on the basis of 16S rRNA gene sequences and compared with morphological characterization, obtaining several supported clusters. Two main Nostoc clusters harboured almost all cyanobionts of Gunnera, Anthoceros and of several cycads, together with free-living strains of the species Nostoc muscorum, Nostoc calcicola, Nostoc edaphicum, Nostoc ellipsosporum and strains related to Nostoc commune. We suggest that the frequent occurrence of symbiotic strains within these clusters is explained by the intensive hormogonia production that was observed in many of the strains studied. However, no evidence for discrimination between symbiotic and free-living strains, either by molecular or morphological approaches, could be found. Sequences of Azolla cyanobiont filaments, taken directly from leaf cavities, clustered tightly with sequences from the planktic cyanobacterium Cylindrospermopsis raciborskii, from the benthic Anabaena cylindrica 133 and from Anabaena oscillarioides HINDAK 1984/43, with high bootstrap values. The phylogenetic analysis showed that two distinct patterns of evolution of symbiotic behaviour might exist for the nostocacean cyanobacteria, one leading to symbioses of Nostoc species with a wide variety of plants, the other leading to the association of a unique cyanobacterial type with the water fern Azolla.

  • 19. Papaefthimiou, Dimitra
    et al.
    Van Hove, Charles
    Lejeune, Andre
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Wilmotte, Annick
    Diversity and specificity of Azolla cyanobionts2008In: Journal of Phycoloy, Vol. 44, p. 60-70Article in journal (Refereed)
    Abstract [en]

    A unique, hereditary symbiosis exists between the water fern Azolla and cyanobacteria that reside within a cavity in the dorsal leaf-lobe of the plant. This association has been studied extensively, and questions have frequently been raised regarding the number and diversity of cyanobionts (cyanobacterial symbionts) among the different Azolla strains and species. In this work, denaturating gradient gel electrophoresis (DGGE) and a clone library based on the 16S rRNA gene were used to study the genetic diversity and host specificity of the cyanobionts in 35 Azolla strains covering a wide taxonomic and geographic range. DNA was extracted directly from the cyanobacterial packets, isolated after enzymatic digestion of the Azolla leaves. Our results indicated the existence of different cyanobiont strains among Azolla species, and diversity within a single Azolla species, independent of the geographic origin of the host. Furthermore, the cyanobiont exhibited host-species specificity and showed most divergence between the two sections of genus Azolla, Azolla and Rhizosperma. These findings are in agreement with the recent redefinition of the taxon Azolla cristata within the section Azolla. With regard to the taxonomic status of the cyanobiont, the genus Anabaena of the Nostocaceae family was identified as the closest relative by this work.

  • 20.
    Poplawski, Andrzej Brunon
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Mårtensson, Lotta
    Stockholm University, Faculty of Science, Department of Botany.
    Wartiainen, Ingvild
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Archaeal diversity and community structure in a Swedish barley field: Specificity of the EK510R/(EURY498) 16S rDNA primer.2007In: J Microbiol Methods, ISSN 0167-7012, Vol. 69, no 1, p. 161-73Article in journal (Refereed)
  • 21. Popova, Alexandra A.
    et al.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Semashko, Tatiana A.
    Govorun, Vadim M.
    Koksharova, Olga A.
    Stress effects of cyanotoxin beta-methylamino-L-alanine (BMAA) on cyanobacterial heterocyst formation and functionality2018In: Environmental Microbiology Reports, ISSN 1758-2229, E-ISSN 1758-2229, Vol. 10, no 3, p. 369-377Article in journal (Refereed)
    Abstract [en]

    Various species of cyanobacteria, diatoms and dinoflagellates are capable of synthesizing the non-proteinogenic neurotoxic amino acid -N-methylamino-L-alanine (BMAA), which is known to be a causative agent of human neurodegeneration. Similar to most cyanotoxins, the biological and ecological functions of BMAA in cyanobacteria are unknown. In this study, we show for the first time that BMAA, in micromolar amounts, inhibits the formation of heterocysts (specialized nitrogen-fixing cells) in heterocystous, diazotrophic cyanobacteria [Anabaena sp. PCC 7120, Nostoc punctiforme PCC 73102 (ATCC 29133), Nostoc sp. strain 8963] under conditions of nitrogen starvation. The inhibitory effect of BMAA is abolished by the addition of glutamate. To understand thegenetic reason for the observed phenomenon, we used qPCR to study the expression of key genes involved in celldifferentiation and nitrogen metabolism in the model cyanobacterium Anabaena sp. PCC 7120. We observed that in the presence of BMAA, Anabaena sp. PCC 7120 does not express two essential genes associated with heterocyst differentiation, namely, hetR and hepA. We also found that addition of BMAA to cyanobacterial cultures with mature heterocysts inhibits nifH gene expression and nitrogenase activity.

  • 22. Popova, Alexandra A.
    et al.
    Semashko, Tatiana A.
    Kostina, Natalia V.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Govorun, Vadim M.
    Koksharova, Olga A.
    The Cyanotoxin BMAA Induces Heterocyst Specific Gene Expression in Anabaena sp PCC 7120 under Repressive Conditions2018In: Toxins, ISSN 2072-6651, E-ISSN 2072-6651, Vol. 10, no 11, article id 478Article in journal (Refereed)
    Abstract [en]

    Cyanobacteria synthesize neurotoxic -N-methylamino-l-alanine (BMAA). The roles of this non-protein amino acid in cyanobacterial cells are insufficiently studied. During diazotrophic growth, filamentous cyanobacteria form single differentiated cells, called heterocysts, which are separated by approximately 12-15 vegetative cells. When combined nitrogen is available, heterocyst formation is blocked and cyanobacterial filaments contain only vegetative cells. In the present study, we discovered that exogenous BMAA induces the process of heterocyst formation in filamentous cyanobacteria under nitrogen-replete conditions that normally repress cell differentiation. BMAA treated cyanobacteria form heterocyst-like dark non-fluorescent non-functional cells. It was found that glutamate eliminates the BMAA mediated derepression. Quantitative polymerase chain reaction (qPCR) permitted to detect the BMAA impact on the transcriptional activity of several genes that are implicated in nitrogen assimilation and heterocyst formation in Anabaena sp. PCC 7120. We demonstrated that the expression of several essential genes increases in the BMAA presence under repressive conditions.

  • 23.
    Premkumar, Albert
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Lindberg, Sylvia
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Lager, Ida
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Schulz, Alexander
    Arabidopsis PLDs with C2-domain function distinctively in hypoxia2019In: Physiologia Plantarum: An International Journal for Plant Biology, ISSN 0031-9317, E-ISSN 1399-3054, Vol. 167, no 1, p. 90-110Article in journal (Refereed)
    Abstract [en]

    Hypoxia (oxygen deprivation) causes metabolic disturbances at physiological, biochemical and genetic levels and results in decreased plant growth and development. Phospholipase D (PLD)-mediated signaling was reported for abiotic and biotic stress signaling events in plants. To investigate the participatory role of PLDs also in hypoxia signaling, we used wild type of Arabidopsis thaliana and 10 pld isoform mutants containing C2-domain. Hypoxia-induced changes in three major signaling players, namely, cytosolic free calcium (Ca-cyt(2+)), reactive oxygen species (ROS) and phosphatidic acid (PA), were determined in mesophyll protoplasts. The Ca-cyt(2+) and ROS levels were monitored by fluorescence microscopy and confocal imaging, while PA levels were quantified by an enzymatic method. Our findings reveal that the elevations of cytosolic calcium and PA are reduced in all the 10 mutants dysfunctional in PLD isoforms. The hypoxia-related changes in both calcium and ROS show different kinetic patterns depending on the type of PLD studied. Pharmacological experiments confirm that both external and internal sources contribute to calcium and ROS accumulation under hypoxia. PLD alpha 1-3, PLD beta 1 and PLD gamma 1-3 are likely involved in calcium signaling under hypoxia as well as in PA production, while all investigated PLDs, except for PLD gamma 3, take part in ROS elevation.

  • 24.
    Spacil, Zdenek
    et al.
    Stockholm University, Faculty of Science, Department of Analytical Chemistry.
    Eriksson, Johan
    Stockholm University, Faculty of Science, Department of Botany.
    Jonasson, Sara
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Ilag, Leopold L.
    Stockholm University, Faculty of Science, Department of Analytical Chemistry.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Botany.
    Analytical protocol for identification of BMAA and DAB in biologicalsamples2010In: The Analyst, ISSN 0003-2654, E-ISSN 1364-5528, Vol. 135, p. 127-132Article in journal (Refereed)
    Abstract [en]

     

    b

    -N-methylamino-L-alanine (BMAA) is a non-protein amino acid, thought to be inflicting neurodegenerative diseases related to ALS/PDC in human beings. Due to conflicting data concerning the presence of BMAA in various biological matrixes, we present a robust and sensitive method for high confidence identification of BMAA after derivatization by 6-aminoquinolyl-N

    -hydroxysuccinimidyl carbamate (AQC). The efficient sample pretreatment in combination with LC-MS/MS SRM enables chromatographic separation of BMAA from the isomer 2,3-diaminobutyric acid (DAB). The method is applicable for selective BMAA/DAB detection in various biological samples ranging from a prokaryotic cyanobacterium to eukaryotic fish.

  • 25.
    Warshan, Denis
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Bay, Guillaume
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Swedish University of Agricultural Sciences, Sweden.
    Nahar, Nurun
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Wardle, David A.
    Nilsson, Marie-Charlotte
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Seasonal variation in nifH abundance and expression of cyanobacterial communities associated with boreal feather mosses2016In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 10, no 9, p. 2198-2208Article in journal (Refereed)
    Abstract [en]

    Dinitrogen (N-2)-fixation by cyanobacteria living in symbiosis with pleurocarpous feather mosses (for example, Pleurozium schreberi and Hylocomium splendens) represents the main pathway of biological N input into N-depleted boreal forests. Little is known about the role of the cyanobacterial community in contributing to the observed temporal variability of N-2-fixation. Using specific nifH primers targeting four major cyanobacterial clusters and quantitative PCR, we investigated how community composition, abundance and nifH expression varied by moss species and over the growing seasons. We evaluated N-2-fixation rates across nine forest sites in June and September and explored the abundance and nifH expression of individual cyanobacterial clusters when N-2-fixation is highest. Our results showed temporal and host-dependent variations of cyanobacterial community composition, nifH gene abundance and expression. N2-fixation was higher in September than June for both moss species, explained by higher nifH gene expression of individual clusters rather than higher nifH gene abundance or differences in cyanobacterial community composition. In most cases, 'Stigonema cluster' made up less than 29% of the total cyanobacterial community, but accounted for the majority of nifH gene expression (82-94% of total nifH expression), irrespective of sampling date or moss species. Stepwise multiple regressions showed temporal variations in N-2-fixation being greatly explained by variations in nifH expression of the 'Stigonema cluster'. These results suggest that Stigonema is potentially the most influential N-2-fixer in symbiosis with boreal forest feather mosses.

  • 26.
    Warshan, Denis
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Kim, Sea-Yong
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Novotny, Andreas
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Combined effects of elevated temperature and CO2 alters epiphytic cyanobacterial community composition - consequences for nitrogen fixation activity and the host Pleurozium schreberiManuscript (preprint) (Other academic)
    Abstract [en]

    In boreal forests, N2-fixation by filamentous heterocystous cyanobacteria in symbiosis with pleurocarpous feathermosses represent the main biological input of new nitrogen (N), and greatly support the surrounding forest productivity. In these ecosystems, climate change is expected to result in 2-8°C increase in temperature and two times greater carbon dioxide (CO2) over the next century, yet little is known about the effects of these factors on the community composition of cyanobacteria in symbiosis with feathermosses. In particular, it is unknown how N2-fixation activity will change and the resulting impact on the moss growth rate (MGR). Here, we reconstructed the symbiosis between the common feathermoss Pleurozium schreberi and different cyanobacteria isolated from feathermosses. Feathermosses were inoculated with different strains of cyanobacteria and exposed to different temperature (11°C and 19°C) and CO2 (500 ppm and 1000 ppm) conditions. Changes in MGR, N2-fixation rate, and cyanobacterial community structure and composition were measured at distinct time points: 5, 10, 20, and 30 weeks of exposure. Our results indicate that both elevated temperature and CO2 levels can individually and combined have positive effects on the N2-fixation activities, and consequently on MGR. The underlying biotic mechanisms for increased N2-fixation and MGR were changes in the cyanobacterial community diversity and composition.  In general, we observed a reduction in cyanobacterial diversity and an increase in cyanobacterial strain abundance that have adapted and dominated under the elevated temperature and CO2 levels. 

  • 27.
    Warshan, Denis
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Kim, Sea-Yong
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis2017In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 11, no 12, p. 2821-2833Article in journal (Refereed)
    Abstract [en]

    Dinitrogen (N2)-fixation by cyanobacteria in symbiosis with feathermosses is the primary pathway of biological N input into boreal forests. Despite its significance, little is known about the cyanobacterial gene repertoire and regulatory rewiring needed for the establishment and maintenance of the symbiosis. To determine gene acquisitions and regulatory changes allowing cyanobacteria to form and maintain this symbiosis, we compared genomically closely related symbiotic-competent and incompetent Nostoc strains, using a proteogenomics approach and an experimental setup allowing for controlled chemical and physical contact between partners. Thirty-two gene families were found only in the genomes of symbiotic strains, including some never before associated with cyanobacterial symbiosis. We identified conserved orthologs that were differentially expressed in symbiotic strains, including protein families involved in chemotaxis and motility, NO regulation, sulfate/phosphate transport, and glycosyl-modifying and oxidative stress-mediating exoenzymes. The physical moss-cyanobacteria epiphytic symbiosis is distinct from other cyanobacteria-plant symbioses, with Nostoc retaining motility, and lacking modulation of N2-fixation, photosynthesis, GS-GOGAT cycle, and heterocyst formation. The results expand our knowledgebase of plant-cyanobacterial symbioses, provide a model of information and material exchange in this ecologically significant symbiosis, and suggest new currencies, namely nitric oxide and aliphatic sulfonates, may be involved in establishing and maintaining the cyanobacteria-feathermoss symbiosis. 

  • 28.
    Warshan, Denis
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Liaimer, Anton
    Pederson, Eric
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Kim, Sea-Yong
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Shapiro, Nicole
    Woyke, Tanja
    Altermark, Bjorn
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Weyman, Philip D.
    Dupont, Christopher L.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Genomic Changes Associated With the Evolutionary Transitions of Nostoc to a Plant Symtiont2018In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 35, no 5, p. 1160-1175Article in journal (Refereed)
    Abstract [en]

    Cyanobacteria belonging to the genus Nostoc comprise free-living strains and also facultative plant symbionts. Symbiotic strains can enter into symbiosis with taxonomically diverse range of host plants. Little is known about genomic changes associated with evolutionary transition of Nostoc from free-living to plant symbiont. Here, we compared the genomes derived from 11 symbiotic Nostoc strains isolated from different host plants and infer phylogenetic relationships between strains. Phylogenetic reconstructions of 89 Nostocales showed that symbiotic Nostoc strains with a broad host range, entering epiphytic and intracellular or extracellular endophytic interactions, form a monophyletic Glade indicating a common evolutionary history. A polyphyletic origin was found for Nostoc strains which enter only extracellular symbioses, and inference of transfer events implied that this trait was likely acquired several times in the evolution of the Nostocales. Symbiotic Nostoc strains showed enriched functions in transport and metabolism of organic sulfur, chemotaxis and motility, as well as the uptake of phosphate, branched-chain amino acids, and ammonium. The genomes of the intracellular Glade differ from that of other Nostoc strains, with a gain/enrichment of genes encoding proteins to generate i-methionine from sulfite and pathways for the degradation of the plant metabolites vanillin and vanillate, and of the macromolecule xylan present in plant cell walls. These compounds could function as C-sources for members of the intracellular Glade. Molecular clock analysis indicated that the intracellular Glade emerged ca. 600 Ma, suggesting that intracellular Nostoc symbioses predate the origin of land plants and the emergence of their extant hosts.

  • 29.
    Warshan, Denis
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pederson, Eric
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Kim, Sea-Yong
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pawlowski, Katharina
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Shared and divergent genomic changes associated with the evolutionary transitions of Nostoc to a plant symbiontManuscript (preprint) (Other academic)
    Abstract [en]

    The cyanobacteria belonging to the genus Nostoc comprise free-living strains but also facultative plant-symbionts. Symbiotic strains can enter into symbiosis with a taxonomically diverse range of host plants. Little is known about genomic changes associated with evolutionary transition of Nostoc from free-living to plant symbiont. Here we compared the genomes derived from eleven symbiotic Nostoc strains isolated from different host plants and infer phylogenetic relationships between strains. Phylogenetic reconstructions of 89 Nostocales showed that symbiotic Nostoc strains with a broad host range, entering epiphytic and intracellular or extracellular endophytic interactions, form a monophyletic clade indicating a common evolutionary history. A polyphyletic origin was found for Nostoc strains which enter only extracellular symbioses, suggesting that this trait was most likely gained several times in the evolution of the Nostocales. Facultative symbiotic Nostoc strains showed enriched functions in the transport and metabolism of organic sulfur, chemotaxis and motility, as well as the uptake of phosphate, amino acid and ammonium. The genomes of the intracellular clade differ from that of other Nostoc strains by a gain/enrichment of genes encoding proteins to generate L-methionine from sulfite and pathways for the degradation of the plant metabolites vanillin and vanillate, and of the macromolecule xylan present in plant cell-walls. These compounds could function as C sources for members of the intracellular clade. Molecular clock analysis suggested that the intracellular clade emerged ~600 million years ago, which would predate the origin of land plants. This suggest that intracellular cyanobacterial symbioses may have even predated the emergence of extant terrestrial plants.

  • 30. Wartiainen, Ingvild
    et al.
    Eriksson, Torsten
    Stockholm University, Faculty of Science, Bergianska botaniska trädgården (tills m Kungl. Vet. Ak.). Department of Botany. Bergianska stiftelsen.
    Zheng, Weiwen
    Rasmussen, Ulla
    Department of Botany. Växtfysiologi.
    Variation in the active diazotrophic community in rice paddy - nifH PCR-DGGE analysis of rhizosphere and bulk soil2008In: Applied Soil Ecology, Vol. 39, p. 65-75Article in journal (Refereed)
    Abstract [en]

    Biological nitrogen fixation (BNF) is an important source of nitrogen input in many natural ecosystems. The rice production today depends on large amounts of chemical nitrogen fertilizer, which is an environmental hazard in rice producing areas. Better exploitation of BNF is one way to reduce the use of chemical nitrogen fertilizer in the future. In this study the active diazotrophic community was investigated in nitrogen fertilized and un-fertilized rice field soils in Fujian Province, southeast China by PCR-DGGE of nifH mRNA, and the potential community by PCR-DGGE of the nifH gene. A total of 45 sequences representing 33 different sequence types were recovered from the DGGE gels. The retrieved cDNA sequences representing the active population of diazotrophs both in fertilized and un-fertilized soils dispersed throughout the nifH clades (alpha-, beta- and gamma Proteobacteria, Firmicutes and Archaea). Thirteen of the sequence types were most closely related to Azoarcus endophytes indicating widespread associations between heterotrophic nitrogen fixing bacteria and rice (Oryza sativa). The majority of the 13 sequence types were identified from the cDNA samples, showing that the Azoarcus might be an important active nitrogen fixing diazotroph in the paddy field. None of the sequence types were closely related to cyanobacteria, nevertheless previous studies from the same area had documented the presence of cyanobacteira in rice fields. The lack of identified cyanobacteria might be due to template discrimination in the PCR reactions, or low abundance of cyanobacteria compared to heterotrophic nitrogen fixing bacteria.

  • 31. Zheng, Weiwen
    et al.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Botany.
    Chen, Bin
    Zheng, Siping
    Xiang, Guan
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Cellular responses in the cyanobacterial symbiont during its vertical transfer between plant generations in the Azolla microphylla symbiosis.2009In: New Phytol, ISSN 1469-8137, Vol. 181, no 1, p. 53-61Article in journal (Refereed)
    Abstract [en]

    The nitrogen-fixing symbiosis between cyanobacteria and the water fern Azolla microphylla is, in contrast to other cyanobacteria-plant symbioses, the only one of a perpetual nature. The cyanobacterium is vertically transmitted between the plant generations, via vegetative fragmentation of the host or sexually within megasporocarps. In the latter process, subsets of the cyanobacterial population living endophytically in the Azolla leaves function as inocula for the new plant generations. Using electron microscopy and immunogold-labeling, the fate of the cyanobacterium during colonization and development of the megasporocarp was revealed. On entering the indusium chamber of the megasporocarps as small-celled motile cyanobacterial filaments (hormogonia), these differentiated into large thick-walled akinetes (spores) in a synchronized manner. This process was accompanied by cytoplasmic reorganizations and the release of numerous membrane vesicles, most of which contained DNA, and the formation of a highly structured biofilm. Taken together the data revealed complex adaptations in the cyanobacterium during its transition between plant generations.

  • 32. Zheng, Weiwen
    et al.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Zheng, Siping
    Bao, Xiaodong
    Chen, Bin
    Gao, Yuan
    Guan, Xiong
    Larsson, John
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Multiple Modes of Cell Death Discovered in a Prokaryotic (Cyanobacterial) Endosymbiont2013In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 6, p. e66147-Article in journal (Refereed)
    Abstract [en]

    Programmed cell death (PCD) is a genetically-based cell death mechanism with vital roles in eukaryotes. Although there is limited consensus on similar death mode programs in prokaryotes, emerging evidence suggest that PCD events are operative. Here we present cell death events in a cyanobacterium living endophytically in the fern Azolla microphylla, suggestive of PCD. This symbiosis is characterized by some unique traits such as a synchronized development, a vertical transfer of the cyanobacterium between plant generations, and a highly eroding cyanobacterial genome. A combination of methods was used to identify cell death modes in the cyanobacterium. Light- and electron microscopy analyses showed that the proportion of cells undergoing cell death peaked at 53.6% (average 20%) of the total cell population, depending on the cell type and host developmental stage. Biochemical markers used for early and late programmed cell death events related to apoptosis (Annexin V-EGFP and TUNEL staining assays), together with visualization of cytoskeleton alterations (FITC-phalloidin staining), showed that all cyanobacterial cell categories were affected by cell death. Transmission electron microscopy revealed four modes of cell death: apoptotic-like, autophagic-like, necrotic-like and autolytic-like. Abiotic stresses further enhanced cell death in a dose and time dependent manner. The data also suggest that dynamic changes in the peptidoglycan cell wall layer and in the cytoskeleton distribution patterns may act as markers for the various cell death modes. The presence of a metacaspase homolog (domain p20) further suggests that the death modes are genetically programmed. It is therefore concluded that multiple, likely genetically programmed, cell death modes exist in cyanobacteria, a finding that may be connected with the evolution of cell death in the plant kingdom.

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