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Actin is one of the most highly conserved proteins in eukaryotes and distinct actin-related proteins with filament-forming properties are even found in prokaryotes. Due to these commonalities, actin-modulating proteins of many species share similar structural properties and proposed functions. The polymerization and depolymerization of actin are critical processes for a cell as they can contribute to shape changes to adapt to its environment and to move and distribute nutrients and cellular components within the cell. However, to what extent functions of actin-binding proteins are conserved between distantly related species, has only been addressed in a few cases. In this work, functions of Coronin-A (CorA) and Actin-interacting protein 1 (Aip1), two proteins involved in actin dynamics, were characterized. In addition, the interchangeability and function of Aip1 were investigated in two phylogenetically distant model organisms. The flowering plant Arabidopsis thaliana (encoding two homologs, AIP1-1 and AIP1-2) and in the amoeba Dictyostelium discoideum (encoding one homolog, DdAip1) were chosen because the functions of their actin cytoskeletons may differ in many aspects. Functional analyses between species were conducted for AIP1 homologs as flowering plants do not harbor a CorA gene.
In the first part of the study, the effect of four different mutation methods on the function of Coronin-A protein and the resulting phenotype in D. discoideum was revealed in two genetic knockouts, one RNAi knockdown and a sudden loss-of-function mutant created by chemical-induced dislocation (CID). The advantages and disadvantages of the different mutation methods on the motility, appearance and development of the amoebae were investigated, and the results showed that not all observed properties were affected with the same intensity. Remarkably, a new combination of Selection-Linked Integration and CID could be established.
In the second and third parts of the thesis, the exchange of Aip1 between plant and amoeba was carried out. For A. thaliana, the two homologs (AIP1-1 and AIP1-2) were analyzed for functionality as well as in D. discoideum. In the Aip1-deficient amoeba, rescue with AIP1-1 was more effective than with AIP1-2. The main results in the plant showed that in the aip1-2 mutant background, reintroduced AIP1-2 displayed the most efficient rescue and A. thaliana AIP1-1 rescued better than DdAip1. The choice of the tagging site was important for the function of Aip1 as steric hindrance is a problem. The DdAip1 was less effective when tagged at the C-terminus, while the plant AIP1s showed mixed results depending on the tag position. In conclusion, the foreign proteins partially rescued phenotypes of mutant plants and mutant amoebae, despite the organisms only being very distantly related in evolutionary terms.
The African weakly electric fishes (Mormyridae) exhibit a remarkable adaptive radiation possibly due to their species-specific electric organ discharges (EODs). It is produced by a muscle-derived electric organ that is located in the caudal peduncle. Divergence in EODs acts as a pre-zygotic isolation mechanism to drive species radiations. However, the mechanism behind the EOD diversification are only partially understood.
The aim of this study is to explore the genetic basis of EOD diversification from the gene expression level across Campylomormyrus species/hybrids and ontogeny. I firstly produced a high quality genome of the species C. compressirostris as a valuable resource to understand the electric fish evolution.
The next study compared the gene expression pattern between electric organs and skeletal muscles in Campylomormyrus species/hybrids with different types of EOD duration. I identified several candidate genes with an electric organ-specific expression, e.g. KCNA7a, KLF5, KCNJ2, SCN4aa, NDRG3, MEF2. The overall genes expression pattern exhibited a significant association with EOD duration in all analyzed species/hybrids. The expression of several candidate genes, e.g. KCNJ2, KLF5, KCNK6 and KCNQ5, possibly contribute to the regulation of EOD duration in Campylomormyrus due to their increasing or decreasing expression. Several potassium channel genes showed differential expression during ontogeny in species and hybrid with EOD alteration, e.g. KCNJ2.
I next explored allele specific expression of intragenus hybrids by crossing the duration EOD species C. compressirostris with the medium duration EOD species C. tshokwe and the elongated duration EOD species C. rhynchophorus. The hybrids exhibited global expression dominance of the C. compressirostris allele in the adult skeletal muscle and electric organ, as well as in the juvenile electric organ. Only the gene KCNJ2 showed dominant expression of the allele from C. rhynchophorus, and this was increasingly dominant during ontogeny. It hence supported our hypothesis that KCNJ2 is a key gene of regulating EOD duration. Our results help us to understand, from a genetic perspective, how gene expression effect the EOD diversification in the African weakly electric fish.
Arachidonsäurelipoxygenasen (ALOX-Isoformen) sind Lipid-peroxidierenden Enzyme, die bei der Zelldifferenzierung und bei der Pathogenese verschiedener Erkrankungen bedeutsam sind. Im menschlichen Genom gibt es sechs funktionelle ALOX-Gene, die als Einzelkopiegene vorliegen. Für jedes humane ALOX-Gen gibt es ein orthologes Mausgen. Obwohl sich die sechs humanen ALOX-Isoformen strukturell sehr ähnlich sind, unterscheiden sich ihre funktionellen Eigenschaften deutlich voneinander. In der vorliegenden Arbeit wurden vier unterschiedliche Fragestellungen zum Vorkommen, zur biologischen Rolle und zur Evolutionsabhängigkeit der enzymatischen Eigenschaften von Säugetier-ALOX-Isoformen untersucht:
1) Spitzhörnchen (Tupaiidae) sind evolutionär näher mit dem Menschen verwandt als Nagetiere und wurden deshalb als Alternativmodelle für die Untersuchung menschlicher Erkrankungen vorgeschlagen. In dieser Arbeit wurde erstmals der Arachidonsäurestoffwechsel von Spitzhörnchen untersucht. Dabei wurde festgestellt, dass im Genom von Tupaia belangeri vier unterschiedliche ALOX15-Gene vorkommen und die Enzyme sich hinsichtlich ihrer katalytischen Eigenschaften ähneln. Diese genomische Vielfalt, die weder beim Menschen noch bei Mäusen vorhanden ist, erschwert die funktionellen Untersuchungen zur biologischen Rolle des ALOX15-Weges. Damit scheint Tupaia belangeri kein geeigneteres Tiermodel für die Untersuchung des ALOX15-Weges des Menschen zu sein.
2) Entsprechend der Evolutionshypothese können Säugetier-ALOX15-Orthologe in Arachidonsäure-12-lipoxygenierende- und Arachidonsäure-15-lipoxygenierende Enzyme eingeteilt werden. Dabei exprimieren Säugetierspezies, die einen höheren Evolutionsgrad als Gibbons aufweisen, Arachidonsäure-15-lipoxygenierende ALOX15-Orthologe, während evolutionär weniger weit entwickelte Säugetiere Arachidonsäure-12 lipoxygenierende Enzyme besitzen. In dieser Arbeit wurden elf neue ALOX15-Orthologe als rekombinante Proteine exprimiert und funktionell charakterisiert. Die erhaltenen Ergebnisse fügen sich widerspruchsfrei in die Evolutionshypothese ein und verbreitern deren experimentelle Basis. Die experimentellen Daten bestätigen auch das Triadenkonzept.
3) Da humane und murine ALOX15B-Orthologe unterschiedliche funktionelle Eigenschaften aufweisen, können Ergebnisse aus murinen Krankheitsmodellen zur biologischen Rolle der ALOX15B nicht direkt auf den Menschen übertragen werden. Um die ALOX15B-Orthologen von Maus und Mensch funktionell einander anzugleichen, wurden im Rahmen der vorliegenden Arbeit Knock-in Mäuse durch die In vivo Mutagenese mittels CRISPR/Cas9-Technik hergestellt. Diese exprimieren eine humanisierte Mutante (Doppelmutation von Tyrosin603Asparaginsäure+Histidin604Valin) der murinen Alox15b. Diese Mäuse waren lebens- und fortpflanzungsfähig, zeigten aber geschlechtsspezifische Unterschiede zu ausgekreuzten Wildtyp-Kontrolltieren im Rahmen ihre Individualentwicklung.
4) In vorhergehenden Untersuchungen zur Rolle der ALOX15B in Rahmen der Entzündungsreaktion wurde eine antiinflammatorische Wirkung des Enzyms postuliert. In der vorliegenden Arbeit wurde untersucht, ob eine Humanisierung der murinen Alox15b die Entzündungsreaktion in zwei verschiedenen murinen Entzündungsmodellen beeinflusst. Eine Humanisierung der murinen Alox15b führte zu einer verstärkten Ausbildung von Entzündungssymptomen im induzierten Dextran-Natrium-Sulfat-Kolitismodell. Im Gegensatz dazu bewirkte die Humanisierung der Alox15b eine Abschwächung der Entzündungssymptome im Freund‘schen Adjuvans Pfotenödemmodell. Diese Daten deuten darauf hin, dass sich die Rolle der ALOX15B in verschiedenen Entzündungsmodellen unterscheidet.
Ribosomes decode mRNA to synthesize proteins. Ribosomes, once considered static, executing machines, are now viewed as dynamic modulators of translation. Increasingly detailed analyses of structural ribosome heterogeneity led to a paradigm shift toward ribosome specialization for selective translation. As sessile organisms, plants cannot escape harmful environments and evolved strategies to withstand. Plant cytosolic ribosomes are in some respects more diverse than those of other metazoans. This diversity may contribute to plant stress acclimation. The goal of this thesis was to determine whether plants use ribosome heterogeneity to regulate protein synthesis through specialized translation. I focused on temperature acclimation, specifically on shifts to low temperatures. During cold acclimation, Arabidopsis ceases growth for seven days while establishing the responses required to resume growth. Earlier results indicate that ribosome biogenesis is essential for cold acclimation. REIL mutants (reil-dkos) lacking a 60S maturation factor do not acclimate successfully and do not resume growth. Using these genotypes, I ascribed cold-induced defects of ribosome biogenesis to the assembly of the polypeptide exit tunnel (PET) by performing spatial statistics of rProtein changes mapped onto the plant 80S structure. I discovered that growth cessation and PET remodeling also occurs in barley, suggesting a general cold response in plants. Cold triggered PET remodeling is consistent with the function of Rei-1, a REIL homolog of yeast, which performs PET quality control. Using seminal data of ribosome specialization, I show that yeast remodels the tRNA entry site of ribosomes upon change of carbon sources and demonstrate that spatially constrained remodeling of ribosomes in metazoans may modulate protein synthesis. I argue that regional remodeling may be a form of ribosome specialization and show that heterogeneous cytosolic polysomes accumulate after cold acclimation, leading to shifts in the translational output that differs between wild-type and reil-dkos. I found that heterogeneous complexes consist of newly synthesized and reused proteins. I propose that tailored ribosome complexes enable free 60S subunits to select specific 48S initiation complexes for translation. Cold acclimated ribosomes through ribosome remodeling synthesize a novel proteome consistent with known mechanisms of cold acclimation. The main hypothesis arising from my thesis is that heterogeneous/ specialized ribosomes alter translation preferences, adjust the proteome and thereby activate plant programs for successful cold acclimation.
Following the extinction of dinosaurs, the great adaptive radiation of mammals occurred, giving rise to an astonishing ecological and phenotypic diversity of mammalian species. Even closely related species often inhabit vastly different habitats, where they encounter diverse environmental challenges and are exposed to different evolutionary pressures. As a response, mammals evolved various adaptive phenotypes over time, such as morphological, physiological and behavioural ones. Mammalian genomes vary in their content and structure and this variation represents the molecular mechanism for the long-term evolution of phenotypic variation. However, understanding this molecular basis of adaptive phenotypic variation is usually not straightforward.
The recent development of sequencing technologies and bioinformatics tools has enabled a better insight into mammalian genomes. Through these advances, it was acknowledged that mammalian genomes differ more, both within and between species, as a consequence of structural variation compared to single-nucleotide differences. Structural variant types investigated in this thesis - such as deletion, duplication, inversion and insertion, represent a change in the structure of the genome, impacting the size, copy number, orientation and content of DNA sequences. Unlike short variants, structural variants can span multiple genes. They can alter gene dosage, and cause notable gene expression differences and subsequently phenotypic differences. Thus, they can lead to a more dramatic effect on the fitness (reproductive success) of individuals, local adaptation of populations and speciation.
In this thesis, I investigated and evaluated the potential functional effect of structural variations on the genomes of mustelid species. To detect the genomic regions associated with phenotypic variation I assembled the first reference genome of the tayra (Eira barbara) relying on linked-read sequencing technology to achieve a high level of genome completeness important for reliable structural variant discovery. I then set up a bioinformatics pipeline to conduct a comparative genomic analysis and explore variation between mustelid species living in different environments. I found numerous genes associated with species-specific phenotypes related to diet, body condition and reproduction among others, to be impacted by structural variants.
Furthermore, I investigated the effects of artificial selection on structural variants in mice selected for high fertility, increased body mass and high endurance. Through selective breeding of each mouse line, the desired phenotypes have spread within these populations, while maintaining structural variants specific to each line. In comparison to the control line, the litter size has doubled in the fertility lines, individuals in the high body mass lines have become considerably larger, and mice selected for treadmill performance covered substantially more distance. Structural variants were found in higher numbers in these trait-selected lines than in the control line when compared to the mouse reference genome. Moreover, we have found twice as many structural variants spanning protein-coding genes (specific to each line) in trait-selected lines. Several of these variants affect genes associated with selected phenotypic traits. These results imply that structural variation does indeed contribute to the evolution of the selected phenotypes and is heritable.
Finally, I suggest a set of critical metrics of genomic data that should be considered for a stringent structural variation analysis as comparative genomic studies strongly rely on the contiguity and completeness of genome assemblies. Because most of the available data used to represent reference genomes of mammalian species is generated using short-read sequencing technologies, we may have incomplete knowledge of genomic features. Therefore, a cautious structural variation analysis is required to minimize the effect of technical constraints.
The impact of structural variants on the adaptive evolution of mammalian genomes is slowly gaining more focus but it is still incorporated in only a small number of population studies. In my thesis, I advocate the inclusion of structural variants in studies of genomic diversity for a more comprehensive insight into genomic variation within and between species, and its effect on adaptive evolution.
Aquatic ecosystems are frequently overlooked as fungal habitats, although there is increasing evidence that their diversity and ecological importance are greater than previously considered. Aquatic fungi are critical and abundant components of nutrient cycling and food web dynamics, e.g., exerting top-down control on phytoplankton communities and forming symbioses with many marine microorganisms. However, their relevance for microphytobenthic communities is almost unexplored. In the light of global warming, polar regions face extreme changes in abiotic factors with a severe impact on biodiversity and ecosystem functioning. Therefore, this study aimed to describe, for the first time, fungal diversity in Antarctic benthic habitats along the salinity gradient and to determine the co-occurrence of fungal parasites with their algal hosts, which were dominated by benthic diatoms. Our results reveal that Ascomycota and Chytridiomycota are the most abundant fungal taxa in these habitats. We show that also in Antarctic waters, salinity has a major impact on shaping not just fungal but rather the whole eukaryotic community composition, with a diversity of aquatic fungi increasing as salinity decreases. Moreover, we determined correlations between putative fungal parasites and potential benthic diatom hosts, highlighting the need for further systematic analysis of fungal diversity along with studies on taxonomy and ecological roles of Chytridiomycota.
Hantaviruses (HVs) are a group of zoonotic viruses that infect human beings primarily through aerosol transmission of rodent excreta and urine samplings. HVs are classified geographically into: Old World HVs (OWHVs) that are found in Europe and Asia, and New World HVs (NWHVs) that are observed in the Americas. These different strains can cause severe hantavirus diseases with pronounced renal syndrome or severe cardiopulmonary system distress. HVs can be extremely lethal, with NWHV infections reaching up to 40 % mortality rate. HVs are known to generate epidemic outbreaks in many parts of the world including Germany, which has seen periodic HV infections over the past decade. HV has a trisegmented genome. The small segment (S) encodes the nucleocapsid protein (NP), the middle segment (M) encodes the glycoproteins (GPs) Gn and Gc which forms up to tetramers and primarily monomers \& dimers upon independent expression respectively and large segment (L) encodes RNA dependent RNA polymerase (RdRp). Interactions between these viral proteins are crucial in providing mechanistic insights into HV virion development. Despite best efforts, there continues to be lack of quantification of these associations in living cells. This is required in developing the mechanistic models for HV viral assembly. This dissertation focuses on three key questions pertaining to the initial steps of virion formation that primarily involves the GPs and NP.
The research investigations in this work were completed using Fluorescence Correlation Spectroscopy (FCS) approaches. FCS is frequently used in assessing the biophysical features of bio-molecules including protein concentration and diffusion dynamics and circumvents the requirement of protein overexpression. FCS was primarily applied in this thesis to evaluate protein multimerization, at single cell resolution.
The first question addressed which GP spike formation model proposed by Hepojoki et al.(2010) appropriately describes the evidence in living cells. A novel in cellulo assay was developed to evaluate the amount of fluorescently labelled and unlabeled GPs upon co-expression. The results clearly showed that Gn and Gc initially formed a heterodimeric Gn:Gc subunit. This sub-unit then multimerizes with congruent Gn:Gc subunits to generate the final GP spike. Based on these interactions, models describing the formation of GP complex (with multiple GP spike subunits) were additionally developed.
HV GP assembly primarily takes place in the Golgi apparatus (GA) of infected cells. Interestingly, NWHV GPs are hypothesized to assemble at the plasma membrane (PM). This led to the second research question in this thesis, in which a systematic comparison between OWHV and NWHV GPs was conducted to validate this hypothesis. Surprisingly, GP localization at the PM was congruently observed with OWHV and NWHV GPs. Similar results were also discerned with OWHV and NWHV GP localization in the absence of cytoskeletal factors that regulate HV trafficking in cells.
The final question focused on quantifying the NP-GP interactions and understanding their influence of NP and GP multimerization. Gc mutlimers were detected in the presence of NP and complimented by the presence of localized regions of high NP-Gc interactions in the perinuclear region of living cells. Gc-CT domain was shown to influence NP-Gc associations. Gn, on the other hand, formed up to tetrameric complexes, independent from the presence of NP.
The results in this dissertation sheds light on the initial steps of HV virion formation by quantifying homo and heterotypic interactions involving NP and GPs, which otherwise are very difficult to perform. Finally, the in cellulo methodologies implemented in this work can be potentially extended to understand other key interactions involved in HV virus assembly.
Development of electrochemical antibody-based and enzymatic assays for mycotoxin analysis in food
(2023)
Electrochemical methods are promising to meet the demand for easy-to-use devices monitoring key parameters in the food industry. Many companies run own lab procedures for mycotoxin analysis, but it is a major goal to simplify the analysis. The enzyme-linked immunosorbent assay using horseradish peroxidase as enzymatic label, together with 3,3',5,5' tetramethylbenzidine (TMB)/H2O2 as substrates allows sensitive mycotoxin detection with optical detection methods. For the miniaturization of the detection step, an electrochemical system for mycotoxin analysis was developed. To this end, the electrochemical detection of TMB was studied by cyclic voltammetry on different screen-printed electrodes (carbon and gold) and at different pH values (pH 1 and pH 4). A stable electrode reaction, which is the basis for the further construction of the electrochemical detection system, could be achieved at pH 1 on gold electrodes. An amperometric detection method for oxidized TMB, using a custom-made flow cell for screen-printed electrodes, was established and applied for a competitive magnetic bead-based immunoassay for the mycotoxin ochratoxin A. A limit of detection of 150 pM (60 ng/L) could be obtained and the results were verified with optical detection. The applicability of the magnetic bead-based immunoassay was tested in spiked beer using a handheld potentiostat connected via Bluetooth to a smartphone for amperometric detection allowing to quantify ochratoxin A down to 1.2 nM (0.5 µg/L).
Based on the developed electrochemical detection system for TMB, the applicability of the approach was demonstrated with a magnetic bead-based immunoassay for the ergot alkaloid, ergometrine. Under optimized assay conditions a limit of detection of 3 nM (1 µg/L) was achieved and in spiked rye flour samples ergometrine levels in a range from 25 to 250 µg/kg could be quantified. All results were verified with optical detection. The developed electrochemical detection method for TMB gives great promise for the detection of TMB in many other HRP-based assays.
A new sensing approach, based on an enzymatic electrochemical detection system for the mycotoxin fumonisin B1 was established using an Aspergillus niger fumonisin amine oxidase (AnFAO). AnFAO was produced recombinantly in E. coli as maltose-binding protein fusion protein and catalyzes the oxidative deamination of fumonisins, producing hydrogen peroxide. It was found that AnFAO has a high storage and temperature stability. The enzyme was coupled covalently to magnetic particles, and the enzymatically produced H2O2 in the reaction with fumonisin B1 was detected amperometrically in a flow injection system using Prussian blue/carbon electrodes and the custom-made wall-jet flow cell. Fumonisin B1 could be quantified down to 1.5 µM (≈ 1 mg/L). The developed system represents a new approach to detect mycotoxins using enzymes and electrochemical methods.
Climate change of anthropogenic origin is affecting Earth’s biodiversity and therefore ecosystems and their services. High latitude ecosystems are even more impacted than the rest of Northern Hemisphere because of the amplified polar warming. Still, it is challenging to predict the dynamics of high latitude ecosystems because of complex interaction between abiotic and biotic components. As the past is the key to the future, the interpretation of past ecological changes to better understand ongoing processes is possible. In the Quaternary, the Pleistocene experienced several glacial and interglacial stages that affected past ecosystems. During the last Glacial, the Pleistocene steppe-tundra was covering most of unglaciated northern hemisphere and disappeared in parallel to the megafauna’s extinction at the transition to the Holocene (~11,700 years ago). The origin of the steppe-tundra decline is not well understood and knowledge on the mechanisms, which caused shifts in past communities and ecosystems, is of high priority as they are likely comparable to those affecting modern ecosystems. Lake or permafrost core sediments can be retrieved to investigate past biodiversity at transitions between glacial and interglacial stages. Siberia and Beringia were the origin of dispersal of the steppe-tundra, which make investigation this area of high priority. Until recently, macrofossils and pollen were the most common approaches. They are designed to reconstruct past composition changes but have limit and biases. Since the end of the 20th century, sedimentary ancient DNA (sedaDNA) can also be investigated. My main objectives were, by using sedaDNA approaches to provide scientific evidence of compositional and diversity changes in the Northern Hemisphere ecosystems at the transition between Quaternary glacial and interglacial stages.
In this thesis, I provide snapshots of entire ancient ecosystems and describe compositional changes between Quaternary glacial and interglacial stages, and confirm the vegetation composition and the spatial and temporal boundaries of the Pleistocene steppe-tundra. I identify a general loss of plant diversity with extinction events happening in parallel of megafauna’ extinction. I demonstrate how loss of biotic resilience led to the collapse of a previously well-established system and discuss my results in regards to the ongoing climate change. With further work to constrain biases and limits, sedaDNA can be used in parallel or even replace the more established macrofossils and pollen approaches as my results support the robustness and potential of sedaDNA to answer new palaeoecological questions such as plant diversity changes, loss and provide snapshots of entire ancient biota.
Movement is a mechanism that shapes biodiversity patterns across spatialtemporal scales. Thereby, the movement process affects species interactions, population dynamics and community composition. In this thesis, I disentangled the effects of movement on the biodiversity of zooplankton ranging from the individual to the community level. On the individual movement level, I used video-based analysis to explore the implication of movement behavior on preypredator interactions. My results showed that swimming behavior was of great importance as it determined their survival in the face of predation. The findings also additionally highlighted the relevance of the defense status/morphology of prey, as it not only affected the prey-predator relationship by the defense itself but also by plastic movement behavior. On the community movement level, I used a field mesocosm experiment to explore the role of dispersal (time i.e., from the egg bank into the water body and space i.e., between water bodies) in shaping zooplankton metacommunities. My results revealed that priority effects and taxon-specific dispersal limitation influenced community composition. Additionally, different modes of dispersal also generated distinct community structures. The egg bank and biotic vectors (i.e. mobile links) played significant roles in the colonization of newly available habitat patches. One crucial aspect that influences zooplankton species after arrival in new habitats is the local environmental conditions. By using common garden experiments, I assessed the performance of zooplankton communities in their home vs away environments in a group of ponds embedded within an agricultural landscape. I identified environmental filtering as a driving factor as zooplankton communities from individual ponds developed differently in their home and away environments. On the individual species level, there was no consistent indication of local adaptation. For some species, I found a higher abundance/fitness in their home environment, but for others, the opposite was the case, and some cases were indifferent.
Overall, the thesis highlights the links between movement and biodiversity patterns, ranging from the individual active movement to the community level.