TY - THES
A1 - Bolius, Sarah
T1 - Microbial invasions in aquatic systems – strain identity, genetic diversity and timing
N2 - Biological invasions are the dispersal and following establishment of species outside their native habitat. Due to globalisation, connectivity of regions and climate changes the number of invasive species and their successful establishment is rising. The impact of these species is mostly negative, can induce community and habitat alterations, and is one main cause for biodiversity loss. This impact is particularly high and less researched in aquatic systems and microbial organisms and despite the high impact, the knowledge about overall mechanisms and specific factors affecting invasions are not fully understood. In general, the characteristics of the habitat, native community and invader determine the invasiveness.
In this thesis, I aimed to provide a better understanding of aquatic invasions focusing on the invader and its traits and identity. This thesis used a set of 12 strains of the invasive cyanobacterium Cylindrospermopsis raciborskii to examine the effect and impact of the invaders’ identity and genetic diversity. Further, the effect of timing on the invasion potential and success was determined, because aquatic systems in particular undergo seasonal fluctuations.
Most studies revealed a higher invasion success with increasing genetic diversity. Here, the increase of the genetic diversity, by either strain richness or phylogenetic dissimilarity, is not firstly driving the invasion, but the strain-identity. The high variability among the strains in traits important for invasions led to the highly varying strain-specific invasion success. This success was most dependent on nitrogen uptake and efficient resource use. The lower invasion success into communities comprising further N-fixing species indicates C. raciborskii can use this advantage only without the presence of competitive species. The relief of grazing pressure, which is suggested to be more important in aquatic invasions, was only promoting the invasion when unselective and larger consumers were present. High abundances of unselective consumers hampered the invasion success.
This indicates a more complex and temporal interplay of competitive and consumptive resistance mechanisms during the invasion process. Further, the fluctuation abundance and presence of competitors (= primary producers) and consumers (= zooplankton) in lakes can open certain ‘invasion windows’.
Remarkably, the composition of the resident community was also strain-specific affected and altered, independent of a high or low invasion success. Prior, this was only documented on the species level. Further, investigations on the population of invasive strains can reveal more about the invasion patterns and how multiple strain invasions change resident communities.
The present dissertation emphasises the importance of invader-addition experiments with a community context and the importance of the strain-level for microbial invasions and in general, e.g. for community assemblies and the outcome of experiments. The strain-specific community changes, also after days, may explain some sudden changes in communities, which have not been explained yet. This and further knowledge may also facilitate earlier and less cost-intensive management to step in, because these species are rarely tracked until they reach a high abundance or bloom, because of their small size.
Concluded for C. raciborskii, it shows that this species is no ‘generalistic’ invader and its invasion success depends more on the competitor presence than grazing pressure. This may explain its, still unknown, invasion pattern, as C. raciborskii is not found in all lakes of a region.
N2 - Biologische Invasionen beschreiben die Ausbreitung und Etablierung von Arten außerhalb ihres natürlichen Verbreitungsgebiets. Das Eindringen dieser invasiven Arten in ein neues Ökosystem hat meist negative Auswirkungen. Beispiele sind unter anderem veränderte Ökosystemprozesse, Lebensräume und Zusammensetzungen der einheimischen Arten, die zu einem Verlust der biologischen Vielfalt führen. Durch die fortschreitende Globalisierung und den Klimawandel steigt die Anzahl invasiver Arten weltweit. Um dies möglichst zu verhindern, müssen die zugrundeliegenden Mechanismen und Faktoren verstanden sein. Besonders bei aquatischen Mikroorganismen ist die Wissenslücke dabei groß und umso drängender, da diese Arten ein hohes Invasionspotential und potentiell stärkere negative Auswirkungen haben.
Die vorliegende Dissertation untersuchte anhand der invasiven Cyanobakterie Cylindrospermopsis raciborskii, den anfänglichen Invasionsprozess, unter besonderer Berücksichtigung der Stamm-Identität, der genetischen Diversität und des Zeitpunkts der Invasion.
Die meisten Studien zu Invasionen zeigen einen positiven Effekt der genetischen Diversität auf Invasionen. Diese Arbeit konnte zeigen, dass der Invasionserfolg auf bestimmte Stamm-spezifische Eigenschaften zurückzuführen ist. Für C. raciborskii war dies eine erhöhte Aufnahme von Stickstoff und eine effizientere Nutzung von Ressourcen. Wie einige andere aquatischen Arten hat C. raciborskii die Fähigkeit über differenzierte Zellen Stickstoff aus der Luft zu fixieren. Des Weiteren fördern bestimmte Umweltbedingungen, wie eine niedrige Nährstoffkonzentration, das Wachstum von C. raciborskii.
Fraßdruck wirkte sich nur negativ aus, wenn unselektive Prädatoren anwesend waren. Zudem zeigten weitere Versuche, dass ihr Konkurrenzvorteil nur in Gemeinschaften ohne weitere Stickstoff-Fixierer und in Stickstoff-reduzierten Habitaten die Etablierung positiv beeinflusst.
Diese Erkenntnisse lassen darauf schließen, dass diverse Eigenschaften und eine zeitliche Abfolge dieser, den Invasionserfolg beeinflussen. Dieser kann einerseits durch den Widerstand der heimischen Arten-Gemeinschaft und zum anderem durch die herrschenden abiotischen Bedingungen verhindert werden. Gerade aquatische Systeme unterlaufen saisonalen Schwankungen und diese erlauben somit bestimmte, temporäre Invasionsmöglichkeiten. Zusätzlich führte die Stamm-Identität zu Änderungen in der einheimischen Artenzusammensetzung, unabhängig vom Erfolg der Invasion - dies wurde bis jetzt nur Art-spezifisch gezeigt.
Damit betont die vorliegende Arbeit die Bedeutung von Stamm-Identitäten auf Invasionen und deren Auswirkungen auf ökologische Prozesse und den Ausgang von Experimenten. Zusammengefasst für C. raciborskii zeigt die Arbeit, dass diese Art keine ‚generell‘ erfolgreiche invasive Art ist und dass der Invasionserfolg eher von den vorhanden konkurrierenden Arten abhängt. Dies könnte das noch unklare Ausbreitungs-Muster erklären.
KW - invasion
KW - cyanobacteria
KW - population
KW - Cylindrospermopsis raciborskii
Y1 - 2018
ER -
TY - JOUR
A1 - Bolius, Sarah
A1 - Karoline Morling,
A1 - Wiedner, Claudia
A1 - Weithoff, Guntram
T1 - Genetic Identity and Herbivory Drive the Invasion of a Common Aquatic Microbial Invader
JF - Frontiers in Microbiology
N2 - Despite the increasing number of species invasions, the factors driving invasiveness are still under debate. This is particularly the case for “invisible” invasions by aquatic microbial species. Since in many cases only a few individuals or propagules enter a new habitat, their genetic variation is low and might limit their invasion success, known as the genetic bottleneck. Thus, a key question is, how genetic identity and diversity of invading species influences their invasion success and, subsequently, affect the resident community. We conducted invader-addition experiments using genetically different strains of the globally invasive, aquatic cyanobacterium Raphidiopsis raciborskii (formerly: Cylindrospermopsis raciborskii) to determine the role of invader identity and genetic diversity (strain richness) at four levels of herbivory. We tested the invasion success of solitary single strain invasions against the invader genetic diversity, which was experimentally increased up to ten strains (multi-strain populations). By using amplicon sequencing we determined the strain-specific invasion success in the multi-strain treatments and compared those with the success of these strains in the single-strain treatments. Furthermore, we tested for the invasion success under different herbivore pressures. We showed that high grazing pressure by a generalist herbivore prevented invasion, whereas a specialist herbivore enabled coexistence of consumer and invader. We found a weak effect of diversity on invasion success only under highly competitive conditions. When invasions were successful, the magnitude of this success was strain-specific and consistent among invasions performed with single-strain or multi-strain populations. A strain-specific effect was also observed on the resident phytoplankton community composition, highlighting the strong role of invader genetic identity. Our results point to a strong effect of the genetic identity on the invasion success under low predation pressure. The genetic diversity of the invader population, however, had little effect on invasion success in our study, in contrast to most previous findings. Instead, it is the interaction between the consumer abundance and type together with the strain identity of the invader that defined invasion success. This study underlines the importance of strain choice in invasion research and in ecological studies in general.
KW - alien species
KW - genotype
KW - invasibility
KW - cyanobacteria
KW - consumptive resistance
KW - phytoplankton
KW - Raphidiopsis
KW - genetic diversity
Y1 - 2019
U6 - https://doi.org/10.3389/fmicb.2020.01598
SN - 1664-302X
VL - 11
PB - Frontiers Media
CY - Lausanne
ER -
TY - JOUR
A1 - Coloma, Sebastian
A1 - Gaedke, Ursula
A1 - Sivonen, Kaarina
A1 - Hiltunen, Teppo
T1 - Frequency of virus-resistant hosts determines experimental community dynamics
JF - Ecology : a publication of the Ecological Society of America
N2 - Parasites, such as bacterial viruses (phages), can have large effects on host populations both at the ecological and evolutionary levels. In the case of cyanobacteria, phages can reduce primary production and infected hosts release intracellular nutrients influencing planktonic food web structure, community dynamics, and biogeochemical cycles. Cyanophages may be of great importance in aquatic food webs during large cyanobacterial blooms unless the host population becomes resistant to phage infection. The consequences on plankton community dynamics of the evolution of phage resistance in bloom forming cyanobacterial populations are still poorly studied. Here, we examined the effect of different frequencies of a phage-resistant genotype within a filamentous nitrogen-fixing Nodularia spumigena population on an experimental plankton community. Three Nodularia populations with different initial frequencies (0%, 5%, and 50%) of phage-resistant genotypes were inoculated in separate treatments with the phage 2AV2, the green alga Chlorella vulgaris, and the rotifer Brachionus plicatilis, which formed the experimental plankton community subjected to either nitrogen-limited or nitrogen-rich conditions. We found that the frequency of the phage-resistant Nodularia genotype determined experimental community dynamics. Cyanobacterial populations with a high frequency (50%) of the phage-resistant genotype dominated the cultures despite the presence of phages, retaining most of the intracellular nitrogen in the plankton community. In contrast, populations with low frequencies (0% and 5%) of the phage-resistant genotype were lysed and reduced to extinction by the phage, transferring the intracellular nitrogen held by Nodularia to Chlorella and rotifers, and allowing Chlorella to dominate the communities and rotifers to survive. This study shows that even though phages represent minuscule biomass, they can have key effects on community composition and eco-evolutionary feedbacks in plankton communities.
KW - cyanobacteria
KW - eco-evolutionary feedbacks
KW - experimental evolution
KW - host-parasite interaction
KW - phage resistance
KW - predator-prey interaction
Y1 - 2018
U6 - https://doi.org/10.1002/ecy.2554
SN - 0012-9658
SN - 1939-9170
VL - 100
IS - 1
PB - Wiley
CY - Hoboken
ER -
TY - JOUR
A1 - Dittmann-Thünemann, Elke
A1 - Fewer, David P.
A1 - Neilan, Brett A.
T1 - Cyanobacterial toxins biosynthetic routes and evolutionary roots
JF - FEMS microbiology reviews
N2 - Cyanobacteria produce an unparalleled variety of toxins that can cause severe health problems or even death in humans, and wild or domestic animals. In the last decade, biosynthetic pathways have been assigned to the majority of the known toxin families. This review summarizes current knowledge about the enzymatic basis for the production of the hepatotoxins microcystin and nodularin, the cytotoxin cylindrospermopsin, the neurotoxins anatoxin and saxitoxin, and the dermatotoxin lyngbyatoxin. Elucidation of the biosynthetic pathways of the toxins has paved the way for the development of molecular techniques for the detection and quantification of the producing cyanobacteria in different environments. Phylogenetic analyses of related clusters from a large number of strains has also allowed for the reconstruction of the evolutionary scenarios that have led to the emergence, diversification, and loss of such gene clusters in different strains and genera of cyanobacteria. Advances in the understanding of toxin biosynthesis and evolution have provided new methods for drinking-water quality control and may inspire the development of techniques for the management of bloom formation in the future.
KW - microcystin
KW - cylindrospermopsin
KW - anatoxin
KW - saxitoxin
KW - cyanobacteria
Y1 - 2013
U6 - https://doi.org/10.1111/j.1574-6976.2012.12000.x
SN - 0168-6445
SN - 1574-6976
VL - 37
IS - 1
SP - 23
EP - 43
PB - Wiley-Blackwell
CY - Hoboken
ER -
TY - JOUR
A1 - Kehr, Jan-Christoph
A1 - Picchi, Douglas Gatte
A1 - Dittmann-Thünemann, Elke
T1 - Natural product biosyntheses in cyanobacteria a treasure trove of unique enzymes
JF - Beilstein journal of organic chemistry
N2 - Cyanobacteria are prolific producers of natural products. Investigations into the biochemistry responsible for the formation of these compounds have revealed fascinating mechanisms that are not, or only rarely, found in other microorganisms. In this article, we survey the biosynthetic pathways of cyanobacteria isolated from freshwater, marine and terrestrial habitats. We especially emphasize modular nonribosomal peptide synthetase (NRPS) and polyketide synthase (PKS) pathways and highlight the unique enzyme mechanisms that were elucidated or can be anticipated for the individual products. We further include ribosomal natural products and UV-absorbing pigments from cyanobacteria. Mechanistic insights obtained from the biochemical studies of cyanobacterial pathways can inspire the development of concepts for the design of bioactive compounds by synthetic-biology approaches in the future.
KW - cyanobacteria
KW - natural products
KW - NRPS
KW - PKS
KW - ribosomal peptides
Y1 - 2011
U6 - https://doi.org/10.3762/bjoc.7.191
SN - 1860-5397
VL - 7
IS - 2
SP - 1622
EP - 1635
PB - Beilstein-Institut zur Förderung der Chemischen Wissenschaften
CY - Frankfurt, Main
ER -
TY - JOUR
A1 - Meyer, Sabine
A1 - Mainz, Andi
A1 - Kehr, Jan-Christoph
A1 - Suessmuth, Roderich
A1 - Dittmann, Elke
T1 - Prerequisites of Isopeptide Bond Formation in Microcystin Biosynthesis
JF - ChemBioChem : a European journal of chemical biology
N2 - The biosynthesis of the potent cyanobacterial hepatotoxin microcystin involves isopeptide bond formation through the carboxylic acid side chains of d-glutamate and -methyl d-aspartate. Analysis of the in vitro activation profiles of the two corresponding adenylation domains, McyE-A and McyB-A(2), either in a didomain or a tridomain context with the cognate thiolation domain and the upstream condensation domain revealed that substrate activation of both domains strictly depended on the presence of the condensation domains. We further identified two key amino acids in the binding pockets of both adenylation domains that could serve as a bioinformatic signature of isopeptide bond-forming modules incorporating d-glutamate or d-aspartate. Our findings further contribute to the understanding of the multifaceted role of condensation domains in nonribosomal peptide synthetase assembly lines.
KW - amino acids
KW - biosynthesis
KW - cyanobacteria
KW - nonribosomal peptide
KW - substrate specificity
Y1 - 2017
U6 - https://doi.org/10.1002/cbic.201700389
SN - 1439-4227
SN - 1439-7633
VL - 18
SP - 2376
EP - 2379
PB - Wiley-VCH
CY - Weinheim
ER -
TY - JOUR
A1 - Reyna-González, Emmanuel
A1 - Schmid, Bianca
A1 - Petras, Daniel
A1 - Süssmuth, Roderich D.
A1 - Dittmann, Elke
T1 - Leader Peptide-Free In Vitro Reconstitution of Microviridin Biosynthesis Enables Design of Synthetic Protease-Targeted Libraries
JF - Angewandte Chemie : a journal of the Gesellschaft Deutscher Chemiker ; International edition
N2 - Microviridins are a family of ribosomally synthesized and post-translationally modified peptides with a highly unusual architecture featuring non-canonical lactone as well as lactam rings. Individual variants specifically inhibit different types of serine proteases. Here we have established an efficient in vitro reconstitution approach based on two ATP-grasp ligases that were constitutively activated using covalently attached leader peptides and a GNAT-type N-acetyltransferase. The method facilitates the efficient in vitro one-pot transformation of microviridin core peptides to mature microviridins. The engineering potential of the chemo-enzymatic technology was demonstrated for two synthetic peptide libraries that were used to screen and optimize microviridin variants targeting the serine proteases trypsin and subtilisin. Successive analysis of intermediates revealed distinct structure-activity relationships for respective target proteases.
KW - biosynthesis
KW - cyanobacteria
KW - microviridins
KW - natural products
KW - peptides
Y1 - 2016
U6 - https://doi.org/10.1002/anie.201604345
SN - 1433-7851
SN - 1521-3773
VL - 55
SP - 9398
EP - 9401
PB - Wiley-VCH
CY - Weinheim
ER -
TY - JOUR
A1 - Weiz, Annika R.
A1 - Ishida, Keishi
A1 - Quitterer, Felix
A1 - Meyer, Sabine
A1 - Kehr, Jan-Christoph
A1 - Mueller, Kristian M.
A1 - Groll, Michael
A1 - Hertweck, Christian
A1 - Dittmann-Thünemann, Elke
T1 - Harnessing the evolvability of tricyclic microviridins to dissect protease-inhibitor interactions
JF - Angewandte Chemie : a journal of the Gesellschaft Deutscher Chemiker ; International edition
N2 - Understanding and controlling proteolysis is an important goal in therapeutic chemistry. Among the natural products specifically inhibiting proteases microviridins are particularly noteworthy. Microviridins are ribosomally produced and posttranslationally modified peptides that are processed into a unique, cagelike architecture. Here, we report a combined rational and random mutagenesis approach that provides fundamental insights into selectivity-conferring moieties of microviridins. The potent variant microviridin J was co-crystallized with trypsin, and for the first time the three-dimensional structure of microviridins was determined and the mode of inhibition revealed.
KW - cyanobacteria
KW - peptide engineering
KW - protease inhibitors
KW - RiPPs
KW - structure elucidation
Y1 - 2014
U6 - https://doi.org/10.1002/anie.201309721
SN - 1433-7851
SN - 1521-3773
VL - 53
IS - 14
SP - 3735
EP - 3738
PB - Wiley-VCH
CY - Weinheim
ER -