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March 2007 - present
January 1993 - October 2006
December 1991 - November 1992
Publications
Publications (92)
To orchestrate a complex life style in changing environments, the filamentous cyanobacterium Nostoc punctiforme facilitates communication between neighboring cells through septal junction complexes. This is achieved by nanopores that perforate the peptidoglycan ( PGN ) layer and traverse the cell septa. The N ‐acetylmuramoyl‐ l ‐alanine amidase Ami...
Multicellular cyanobacteria, like Nostoc punctiforme , rely on septal junctions for cell-cell communication, which is crucial for coordinating various physiological processes including differentiation of N 2 -fixing heterocysts, spore-like akinetes and hormogonia - short, motile filaments important for dispersal. In this study we functionally chara...
Anabaena sp. PCC 7120 grows by forming filaments of communicating cells and is considered a paradigm of bacterial multicellularity. Molecular exchanges between contiguous cells in the filament take place through multiprotein channels that traverse the septal peptidoglycan through nanopores connecting their cytoplasms. Besides, the septal-junction c...
Multicellular organisms require controlled intercellular communication for their survival. Strains of the filamentous cyanobacterium Nostoc regulate cell–cell communication between sister cells via a conformational change in septal junctions. These multi-protein cell junctions consist of a septum spanning tube with a membrane-embedded plug at both...
Several filamentous cyanobacteria like Nostoc differentiate specialized cells in response to changes in environmental factors, such as low light or nutrient starvation. These specialized cells are termed heterocysts and akinetes. Under conditions of nitrogen limitation, nitrogen-fixing heterocysts form in a semi-regular pattern and provide the fila...
Planktonic freshwater filamentous cyanobacterium Trichormus variabilis ATCC 29413 (previously known as Anabaena variabilis) can differentiate heterocysts and akinetes to survive under different stress conditions. Whilst heterocysts enable diazotrophic growth, akinetes are spore-like resting cells that make the survival of the species possible under...
Contractile injection systems (CISs) mediate cell–cell interactions by phage tail-like structures, using two distinct modes of action: extracellular CISs are released into the medium, while type 6 secretion systems (T6SSs) are attached to the cytoplasmic membrane and function upon cell–cell contact. Here, we characterized a CIS in the multicellular...
The multicellular life style of filamentous cyanobacteria like Nostoc sp. PCC7120 relies on a cell-cell communication system involving so called septal junctions. These are multiprotein complexes, which traverse the septal peptidoglycan through nanopores, connecting the neighboring cells and enabling molecule transfer along the filament. The interc...
Some cyanobacteria of the order Nostocales can form akinetes, spore-like dormant cells resistant to various unfavorable environmental fluctuations. Akinetes are larger than vegetative cells and contain large quantities of reserve products, mainly glycogen and the nitrogen storage polypeptide polymer cyanophycin. Akinetes are enveloped in a thick pr...
Anabaena variabilis is a filamentous cyanobacterium that is capable to differentiate specialized cells, the heterocysts and akinetes, to survive under different stress conditions. Under nitrogen limited condition, heterocysts provide the filament with nitrogen by fixing N 2 . Akinetes are spore-like dormant cells that allow survival during adverse...
Septal junctions are cell-cell connections that mediate intercellular communication in filamentous cyanobacteria. The septal peptidoglycan is perforated by dozens of 20 nm-wide nanopores, through which these proteinaceous structures traverse, physically connecting adjacent cells. On each cytoplasmic side, every septal junction contains a flexible c...
Aerobic life on Earth evolved about 3 [...]
Polymerizing and filament‐forming proteins are instrumental for numerous cellular processes such as cell division and growth. Their function in stabilization and localization of protein complexes and replicons is achieved by a filamentous structure. Known filamentous proteins assemble into homopolymers consisting of single subunits – for example, M...
Acid stress is an environmental problem for plants and fresh water cyanobacteria like the filamentous, heterocyst forming species Anabaena sp. PCC 7120 (hereafter Anabaena sp.). Heterocyst differentiation, cell-cell communication, and nitrogen fixation has been deeply studied in this model organism, but little is known about the cellular response o...
Cyanobacteria occupy almost all illuminated aquatic and terrestrial habitats and developed sohpisticated cellular stragteies of survival under fluctuating conditions. In recent years, our knowledge on cyanobacterial survival strategies has increased tremendously by applying global studies like transcriptomics and proteomics, advanced microscopic te...
Cyanobacteria are phototrophic bacteria carrying out oxygen‐producing photosynthesis. Besides showing the capability of building their cellular carbon from carbon dioxide (CO 2 ), available in the atmosphere, several strains of cyanobacteria have also acquired the ability to fix molecular dinitrogen (N 2 ), a ubiquitous source of nitrogen. As the e...
Multicellular lifestyle requires cell-cell connections. In multicellular cyanobacteria, septal junctions enable molecular exchange between sister cells and are required for cellular differentiation. The structure of septal junctions is poorly understood, and it is unknown whether they are capable of controlling intercellular communication. Here, we...
The filamentous heterocyst‐forming cyanobacterium Anabaena sp. PCC 7120 is an important model organism for studying cell differentiation, nitrogen fixation, and photosynthesis. This cyanobacterium possesses a high number of membrane transporters. Not much is known about the roles of the membrane transporters, especially the ATP‐binding cassette (AB...
The filamentous, photosynthetic cyanobacterium Anabaena sp. PCC 7120 can be considered as a true multicellular bacterium. Along the filament of cells, nitrogen fixation is spatially separated from the incompatible process of oxygenic photosynthesis by the formation of specialized heterocysts in a semiregular pattern. Heterocyst development involves...
Some filamentous cyanobacteria are phototrophic bacteria with a true multicellular life style. They show patterned cell differentiation with the distribution of metabolic tasks between different cell types. This life style requires a system of cell-cell communication and metabolite exchange along the filament. During our study of the cell wall of s...
The nitrogenase complex in the heterocysts of the filamentous freshwater cyanobacterium Anabaenasp. PCC 7120 fixes atmospheric nitrogen to allow diazotrophic growth. The heterocyst cell envelope protects the nitrogenase from oxygen and consists of a polysaccharide and a glycolipid layer that are formed by a complex process involving the recruitment...
Bacterial cell shape is an important determinant of the organism physiology, its interaction with the environment and the coordination of myriad intracellular processes. The cell shape is determined by peptidoglycan (PG) biogenesis and its spatial distribution, which is coordinated by components of the bacterial cytoskeleton. Those proteins typical...
The nitrogenase complex in the heterocysts of the filamentous freshwater cyanobacterium Anabaena sp. PCC 7120 fixes atmospheric nitrogen to allow diazotrophic growth. The heterocyst cell envelope protects the nitrogenase from oxygen and consists of a polysaccharide and a glycolipid layer that are formed by a complex process involving the recruitmen...
Multicellular lifestyle requires cell-cell connections. In multicellular cyanobacteria, septal junctions enable molecular exchange between sister cells and are required for cellular differentiation. The structure of septal junctions is poorly understood and it is unknown whether they regulate intercellular communication.
Here we resolved the in sit...
Anabaena sp. PCC 7120 is a filamentous cyanobacterium able to fix atmospheric nitrogen in semi-regularly spaced heterocysts. For correct heterocyst function, a special cell envelope consisting of a glycolipid layer and a polysaccharide layer is essential. We investigated the role of the genes hgdB and hgdC, encoding domains of a putative ABC transp...
Heterocyst-forming cyanobacteria are organized as multicellular filaments of tightly interacting, functionally specialized cells. N2-fixing heterocysts differentiate from vegetative cells under nitrogen limitation in a semi-regular pattern along the filament. Diazotrophic growth requires metabolite exchange between neighboring cells within the fila...
Two hundred genes or 3% of the known or putative protein-coding genes of the filamentous freshwater cyanobacterium Anabaena sp. PCC 7120 encode domains of ATP-binding cassette (ABC) transporters. Detailed characterization of some of these transporters (14 - 15 importers and 5 exporters) has revealed their crucial roles in the complex lifestyle of t...
Germination of akinetes of filamentous heterocyst-forming cyanobacteria of the order Nostocales is an essential process that ensures survival and recolonization after long periods of unfavorable conditions, as desiccation, cold and low light. We studied the morphological, physiological, and metabolic changes that occur during germination of akinete...
Filamentous cyanobacteria have developed a strategy to perform incompatible processes in one filament by differentiating specialized cell types, N2-fixing heterocysts and CO2-fixing, photosynthetic, vegetative cells. These bacteria can be considered true multicellular organisms with cells exchanging metabolites and signaling molecules via septal ju...
Classical microbial carbon polymers such as glycogen and polyhydroxybutyrate (PHB) have a crucial impact as both a sink and a reserve under macronutrient stress conditions. Most microbial species exclusively synthesize and degrade either glycogen or PHB. A few bacteria such as the phototrophic model organism Synechocystis sp. PCC 6803 surprisingly...
Akinetes are resting spore-like cells formed by some heterocyst-forming filamentous cyanobacteria for surviving long periods of unfavourable conditions. We studied the development of akinetes in two model strains of cyanobacterial cell differentiation, the planktonic freshwater Anabaena variabilis ATCC 29413 and the terrestrial or symbiotic Nostoc...
In the filaments of heterocyst-forming cyanobacteria, septal junctions that traverse the septal peptidoglycan join adjacent cells, allowing intercellular communication. Perforations in the septal peptidoglycan have been observed, and proteins involved in the formation of such perforations and putative protein components of the septal junctions have...
Background:
PII signal processor proteins are wide spread in prokaryotes and plants where they control a multitude of anabolic reactions. Efficient overproduction of metabolites requires relaxing the tight cellular control circuits. Here we demonstrate that a single point mutation in the PII signaling protein from the cyanobacterium Synechocystis...
Akinetes are spore-like non-motile cells that differentiate from vegetative cells of filamentous cyanobacteria from the order Nostocales. They play a key role in the survival and distribution of these species and contribute to their perennial blooms. Here, we demonstrate variations in cellular ultrastructure during akinete formation concomitant wit...
Cyanobacteria of the order Nostocales form filaments of hundreds of interacting cells exchanging metabolites and signal molecules, similar to multicellular eukaryotes. Here, we show a structural requisite for intrafilament communication: perforation of a single layered septal cell wall by an array of nanopores. An autolytic enzyme was identified in...
Akinetes are spore-like non-motile cells that differentiate from vegetative cells of filamentous cyanobacteria from the order Nostocales. They play a key role in the survival and distribution of these species and contribute to their perennial blooms. Here, we demonstrate variations in cellular ultrastructure during akinete formation concomitant wit...
Unlabelled:
Many filamentous cyanobacteria produce specialized nitrogen-fixing cells called heterocysts, which are located at semiregular intervals along the filament with about 10 to 20 photosynthetic vegetative cells in between. Nitrogen fixation in these complex multicellular bacteria depends on metabolite exchange between the two cell types, w...
The polyphosphate glucokinases can phosphorylate glucose to glucose-6-phosphate using polyphosphate as the substrate. ORF all1371 encodes a putative polyphosphate glucokinase in the filamentous heterocyst-forming cyanobacterium, Anabaena sp. PCC 7120. Here, ORF all1371 was heterologously expressed in Escherichia coli, and its purified product was c...
In diesem Jahr wurde das Cyanobakterium Nostoc durch die VAAM zur “Mikrobe des Jahres” gekürt. Nostoc ist ein vielzelliges Bakterium, das sich an verschiedene Umweltbedingungen anpassen und dementsprechend vielfältige Habitate besiedeln kann. Das von Licht und Luft lebende Bakterium kann sporenähnliche Zellen bilden, sich mithilfe von Pili fortbewe...
Thylakoids and photosystem I (PS I) preparations from Euglena gracilis and from the cyanobacterium Atzacystis nidulans were analyzed for their prenylquinone content. Both organisms contained 5′-monohydroxyphylloquinone as the dominant quinone of PS I. and not phylloquinone as other organisms. A stoichiometry of about two 5′-monohydroxyphylloquinone...
In Gram-negative bacteria, trans-envelope efflux pumps have periplasmic membrane fusion proteins (MFPs) as essential components. MFPs act as mediators between outer membrane factors (OMFs) and inner membrane factors (IMFs). In this study, structure-function relations of the ATP-driven glycolipid efflux pump DevBCA-TolC/HgdD from the cyanobacterium...
Changes of photosynthetic activity in vivo of individual heterocysts and vegetative cells in the diazotrophic cyanobacterium Anabaena sp. strain PCC 7120 during the course of diazotrophic acclimation were determined using fluorescence kinetic microscopy (FKM). Distinct phases of stress and acclimation following nitrogen step-down were observed. The...
The transition from unicellular to multicellular life, which occurred several times during evolution, requires tight interaction and communication of neighboring cells. The multicellular cyanobacterium Nostoc punctiforme ATCC 29133 forms filaments of hundreds of interacting cells exchanging metabolites and signal molecules and is able to differenti...
Filamentous cyanobacteria of the order Nostocales display typical properties of multicellular organisms. In response to nitrogen starvation, some vegetative cells differentiate into heterocysts, where fixation of N(2) takes place. Heterocysts provide a micro-oxic compartment to protect nitrogenase from the oxygen produced by the vegetative cells. D...
Efflux pumps export a wide variety of proteinaceous and non-proteinaceous substrates across the Gram-negative cell wall. For the filamentous cyanobacterium Anabaena sp. strain PCC 7120, the ATP-driven glycolipid efflux pump DevBCA-TolC has been shown to be crucial for the differentiation of N(2)-fixing heterocysts from photosynthetically active veg...
In the filamentous, heterocyst-forming cyanobacteria, two different cell types, the CO(2)-fixing vegetative cells and the N(2)-fixing heterocysts, exchange nutrients and regulators for diazotrophic growth. In the model organism Anabaena sp. strain PCC 7120, inactivation of fraH produces filament fragmentation under conditions of combined nitrogen d...
Streptomyces coelicolor contains two gene clusters putatively involved in wall teichoic acid biosynthesis. Inactivation of the tagF homologue SCO2997 or SCO2584, a component of the Streptomyces spore wall synthesizing complex, affected sporulation. The mutant phenotypes resembled those of mre mutants, suggesting a function of wall teichoic acids in...
Upon depletion of combined nitrogen, N(2)-fixing heterocysts are formed from vegetative cells in the case of the filamentous cyanobacterium Anabaena sp. strain PCC 7120. A heterocyst-specific layer composed of glycolipids (heterocyst envelope glycolipids (HGLs)) that functions as an O(2) diffusion barrier is deposited over the heterocyst outer memb...
The filamentous, heterocyst-forming cyanobacteria are multicellular organisms in which two different cell types, the CO₂-fixing vegetative cells and the N₂-fixing heterocysts, exchange nutrients and regulators. In Anabaena sp. strain PCC 7120, inactivation of sepJ or genes in the fraC operon (fraC, fraD and fraE) produce filament fragmentation. Sep...
Most bacteria with a rod-shaped morphology contain an actin-like cytoskeleton consisting of MreB polymers, which form helical
spirals underneath the cytoplasmic membrane to direct peptidoglycan synthesis for the elongation of the cell wall. In contrast,
MreB of Streptomyces coelicolor is not required for vegetative growth but has a role in sporulat...
It is still an open question how an intracellular cytoskeleton directs the synthesis of the peptidoglycan exoskeleton. In contrast to MreB of rod-shaped bacteria, which is essential for lateral cell wall synthesis, MreB of Streptomyces coelicolor has a role in sporulation. To study the function of the S. coelicolor mre gene cluster consisting of mr...
Filamentous cyanobacteria of the order Nostocales are primordial multicellular organisms, a property widely considered unique to eukaryotes. Their filaments are composed of hundreds of mutually dependent vegetative cells and regularly spaced N(2)-fixing heterocysts, exchanging metabolites and signalling molecules. Furthermore, they may differentiat...
Heterocyst-forming cyanobacteria are able to perform oxygenic photosynthesis and nitrogen fixation simultaneously in the same filament, by restricting the highly O(2)-sensitive nitrogenase to specialized cells, the heterocysts. A remarkable change in morphology and metabolism accompanies the differentiation of heterocysts, which only occurs when no...
Chlorophyll d is a photosynthetic pigment that, based on chemical analyses, has only recently been recognized to be widespread in oceanic and lacustrine environments. However, the diversity of organisms harbouring this pigment is not known. Until now, the unicellular cyanobacterium Acaryochloris marina is the only characterized organism that uses c...
Iron uptake is essential for Gram-negative bacteria including cyanobacteria. In cyanobacteria, however, the iron demand is higher than in proteobacteria due to the function of iron as a cofactor in photosynthesis and nitrogen fixation, but our understanding of iron uptake by cyanobacteria stands behind the knowledge in proteobacteria. Here, two gen...
Cyanobacteria are phototrophic bacteria carrying out oxygen‐producing photosynthesis. Indeed, cyanobacteria were the inventors of oxygenic photosynthesis carried out by eukaryotic algae and plants. Besides showing the capability of building their cellular carbon from carbon dioxide, available in the atmosphere, several strains of cyanobacteria have...
The multicellular Anabaena sp. strain PCC 7120 is a filamentous cyanobacterium that can fix N(2) in differentiated cells called heterocysts, which exchange nutritional and regulatory compounds with the neighbour photosynthetic vegetative cells. The outer membrane of this bacterium is continuous along the filament defining a continuous periplasmic s...
Iron uptake in proteobacteria by TonB-dependent outer membrane transporters represents a well-explored subject. In contrast,
the same process has been scarcely investigated in cyanobacteria. The heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 is known to secrete the siderophore schizokinen, but its transport system has remained unide...
Heterocyst development was analyzed in mutants of the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 bearing inactivated cox2 and/or cox3 genes, encoding heterocyst-specific terminal respiratory oxidases. At the morphological level, the cox2 cox3 double mutant (strain CSAV141) was impaired in membrane reorganization involving the so...
Heterocysts, formed when filamentous cyanobacteria, such as Anabaena sp. strain PCC 7120, are grown in the absence of combined nitrogen, are cells that are specialized in fixing atmospheric
nitrogen (N2) under oxic conditions and that transfer fixed nitrogen to the vegetative cells of the filament. Anabaena sp. mutants whose sepJ gene (open reading...
The filamentous cyanobacterium Anabaena sp. strain PCC 7120 forms heterocysts in a semiregular pattern when it is grown on N2 as the sole nitrogen source. The transition from vegetative cells to heterocysts requires marked metabolic and morphological
changes. We show that a trimeric pore-forming outer membrane β-barrel protein belonging to the TolC...
Filamentous, heterocyst-forming cyanobacteria are multicellular organisms in which individual cells exchange nutrients and, presumably, regulatory molecules. Unknown mechanisms underlie this exchange. Classical electron microscopy shows that filamentous cyanobacteria bear a Gram-negative cell wall comprising a peptidoglycan layer and an outer membr...
When growing on N(2) as sole nitrogen source, the filamentous cyanobacterium Anabaena sp. PCC 7120 forms N(2) fixing heterocysts in a semi-regular pattern. To identify genes involved in heterocyst differentiation we characterised five transposon-generated mutants that were not able to form mature heterocysts. After recovering the transposon togethe...
When growing on N2 as sole nitrogen source, the filamentous cyanobacterium Anabaena sp. PCC 7120 forms N2 fixing heterocysts in a semi-regular pattern. To identify genes involved in heterocyst differentiation we characterised five transposon-generated mutants that were not able to form mature heterocysts. After recovering the transposon together wi...
The devBCA operon, encoding subunits of an ATP-binding cassette exporter, is essential for differentiation of N2-fixing heterocysts in Anabaena spp. Nitrogen deficiency-dependent transcription of the operon and the use of its transcriptional start point, located 762
(Anabaena variabilis strain ATCC 29413-FD) or 704 (Anabaena sp. strain PCC 7120) bp...
The entire sequence of the 3.5-kb fragment of genomic DNA from Rhodobacter capsulatus which contains the sqr gene and a second complete and two further partial open reading frames has been determined. A correction of the previously published sqr gene sequence (M. Schütz, Y. Shahak, E. Padan, and G. Hauska, J. Biol. Chem. 272:9890-9894, 1997) which...
To perform oxygenic photosynthesis and fix dinitrogen simultaneously the filamentous cyanobacterium Anabaena sp. protects the extremely oxygen-sensitive nitrogenase by spatial separation of the two processes in two different cell types, the oxygen evolving vegetative cell and the N2-f?xing heterocyst. A thick envelope, consisting of heterocyst-spec...
The devBCA gene cluster (dev for development), shown to be essential for envelope formation in heterocysts of Anabaena sp. strain PCC 7120, was identified in the gene bank of a second heterocyst-forming strain, Anabaena variabilis ATCC 29413. Sequence and structural organization of the three genes, encoding subunits of a presumptive ABC transporter...
The gene devA of the filamentous heterocyst-form-ing cyanobacterium Anabaena sp. strain PCC 7120 encodes a protein with high similarity to ATP-binding cassettes of ABC transporters. Mutant M7 defective in the devA gene is arrested in the development of heterocysts at an early stage and is not able to fix N2 under aerobic conditions. The devA gene i...
Inorganic reduced sulfur compounds serve as electron donors in many phototrophic and chemotrophic bacteria¹’². Sulfide-quinone reductase (SQR; E.C.1.8.5. “.) is one of the main enzymes involved in the oxidation of sulfide to sulfur. This sulfide induced membrane bound flavoprotein with an apparent MW of approximately 56-kDa was shown to be widely d...
The Ca2+-dependent protease of the cyanobacterium Anabaena variabilis is a cytoplasmic enzyme with a substrate specificity like trypsin. Its previously published DNA sequence [Maldener, I., Lockau, W., Cai, Y. & Wolk, C. P. (1991)Mol. Gen. Genet. 225, 113–120] contained a sequencing error. Here we report the corrected sequence which shows, that the...
Mutant M7, obtained by transposon mutagenesis of the cyanobacterium Anabaena sp. strain PCC 7120, is impaired in the development of mature heterocysts. Under aerobic conditions, the mutant is unable to fix N2 because of a deficiency of at least two components of the oxygen-protective mechanisms: a hemoprotein-coupled oxidative reaction and heterocy...
Two large, hydrophobic polypeptides termed PSI-A and PSI-B of Photosystem I are thought, as a heterodimer, to harbor all redox centers and pigments required for primary charge separation. The gene psaB coding for PSI-B was cloned from Anabaena variabilis, a segment replaced by a drug-resistance cassette, and returned to Anabaena on a suicide plasmi...
It has been suggested that a calcium-dependent intracellular protease of the cyanobacterium, Anabaena sp., participates in the differentiation of heterocysts, cells that are specialized for fixation of N2. Clones of the structural gene (designated prcA) for this protease from Anabaena variabilis strain ATCC 29413 and Anabaena sp. strain PCC 7120 we...
Kurzfassung von: Regensburg, Univ., Diss., 1991.
