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Antimicrobials in Constructed Wetlands Can Cause in Planta Dysbiosis

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Antimicrobials in Constructed Wetlands Can Cause in Planta Dysbiosis Antimicrobials in constructed wetlands can cause in planta dysbiosis Von der Fakultät für Mathematik, Informatik und Naturwissenschaften der RWTH Aachen University zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften genehmigte Dissertation vorgelegt von Muhammad Arslan aus Kasur, Pakistan Berichter: Universitätsprofessor Dr. Rolf Altenburger Universitätsprofessor Dr. Henner Hollert Tag der mündlichen Prüfung: 27.06.2019 Diese Dissertation ist auf den Internetseiten der Universitätsbibliothek verfügbar. During this study, I have learned that we as humans do not have any privilege over any biome except our capability of interference. Muhammad Arslan ABSTRACT Constructed wetlands (CWs) are engineered phytoremediation systems. They comprise of the two main biotic components, namely plants and bacterial community, which work synergistically to remove a wide range of pollutants from wastewater. CWs have been used as sole treatment systems or as integrated module within other types of wastewater Antimicrobials treatment plants (WWTPs), e.g. as tertiary treatment unit. Recent are inhibitors of investigations have shown that WWTPs are typically not able to remove bacterial growth hence may inhibit low concentrations of certain pollutants, known as organic the beneficial micropollutants (OMPs). This class of pollutant is of emerging concern bacterial for ecotoxicologists because of their unknown toxic effects. A prominent endophytes in category among OMPs comprises antimicrobials whose presence in the planta. wastewater may disturb plant-microbe interplay in CWs due to the active biological nature of the compounds. To date, nothing is known about what consequences can arise for the plant-associated bacterial communities, mainly endophytes, upon exposure of antimicrobials. Endophytic bacteria are described as being analogous to the gut bacteria that provide health benefits to the host, i.e. phytohormones production, stress alleviation, and defense against pathogens. Therefore, any disturbance in the endophytic community that This dissertation may affect the performance of plants is a subject of interest. This addresses dissertation strives to illuminate the response of endophytic bacteria response of (Chapter 2) and Juncus effusus (Chapter 3) upon exposure of two endophytic antimicrobials, namely sulfamethoxazole (SMX) and trimethoprim community and (TMP). J. effusus (soft or common rush) is a model wetland plant and Juncus effusus to two has been extensively used in phytoremediation studies; whereas, SMX antimicrobials. and TMP are commonly found antimicrobials in European wastewaters whose harmful effects are still unknown to the in planta bacterial community. In two studies, repeated exposures of antimicrobials were found to decrease plant fitness in the model wetlands (tested through visual and physiological observations). Subsequently, microbiological analyses were carried out to see if the decrease in plant fitness resulted due to changes in plant microflora. In the first study, initial high concentrations of antimicrobials (10 and 100 µg/L of SMX and TMP, respectively) caused a drop in evapotranspiration (a surrogate for plant fitness) within a few days. Evapotranspiration recouped after omitting the antimicrobials, albeit to the lower values than prior exposure. After IV ABSTRACT several exposures at lower concentrations, plants became infested with insects, evapotranspiration was almost zero, and plant tissue turned necrotic. The response of the endophytic bacterial community was therefore recorded through cultivation-dependent and cultivation- independent analyses. Cultivation-dependent analysis illustrated an increase of the bacterial community in the post-exposure period. This increase was significantly Culture-dependent higher in the exposed roots than the exposed shoots. In vitro biochemical and independent approaches characterization was conducted to see if there were any bacterial strains revealed possessing plant growth promoting (PGP) characteristics. Assays substantial confirmed that many of the isolated strains possessed a stress alleviation changes in trait [i.e., 1-aminocyclopropane-1-carboxylate (ACC) deaminase community activity], whereas some of the strains also exhibited other PGP composition, which were characteristics, i.e., phosphorus solubilization, siderophore production, particularly and indole acetic acid (IAA) formation. Cultivation-independent pronounced in the analysis through quantitative PCR (qPCR) revealed an at least 8-fold roots. increase of endophytic bacteria in exposed roots as compared to the community present in un-exposed roots. Taxon-specific observations, made via both cultivation-dependent and independent analysis, revealed that Gammaproteobacteria was the dominant group, followed by Firmicutes and Actinobacteria. To test whether this new community was accepted by the plant itself or not, a study on production of reactive oxygen species (ROS) and reactive nitrogen species (RNS) was carried out in the post-exposure period when there were no antimicrobials in the system for at least three months. High ROS and RNS were detected in Invasion of the exposed roots, which suggested an invasion of detrimental bacteria pervasive bacteria or opportunistic behavior of the pre-existing community. Concomitantly, was indicated by fluorescent in situ hybridization (FISH) confirmed that intensive production of Gammaproteobacteria and Firmicutes were intensively colonizing the reactive oxygen plant root interior as biofilms were found along the inner walls of the species (ROS) and conducting elements and aerenchyma. To develop a further reactive nitrogen understanding about the community structure, 16S rRNA gene amplicon species (RNS). sequencing was carried out. Results indicated that before exposure, the community composition was similar for both roots and shoots, however, the post-exposure period exhibited drastic changes, i.e., the pre-exposure community was replaced with a new community. These changes occurred mainly in the exposed roots but less in exposed shoots. To understand how plant and bacterial community responded temporally to the presence of the antimicrobials, a second study was carried out with different experimental conditions. Concentrations of antimicrobials were increased in a step-wise manner and plant fitness was evaluated in terms ABSTRACT V of evapotranspiration, chlorophyll fluorescence, and visual inspections. No significant change in evapotranspiration was seen until plants were exposed to 50 and 17 µg/L of SMX and TMP, respectively. Then, chlorophyll fluorescence was reduced and plants roots started turning porous and blackish. The further increase in concentrations resulted in insect infestation on exposed plant shoots. The cultivation-independent analysis (16S amplicon sequencing) revealed a dose-dependent effect on Temporal study the root endophytic community. A decline in Fisher's alpha diversity elucidated that endophytic index was observed up to the concentration of 50 µg/L SMX and 17 µg/L community was TMP. Further increase in concentrations resulted in regain in the inhibited first and diversity, however, coordinate analyses revealed that this improvement then new was not due to the recovery of the previous microbiome but rather that a community took new community took over the system. Thus, a change in microbial over the system. community appeared before the physiological and morphological changes of the plants. Finally, at concentrations of 100 µg/L SMX and 33 µg/L TMP, changes in the endophytic community structure were highly significant for the roots, and they were in accordance to the results of 16S amplicon sequencing made in the first experiment. Additionally, it was shown that the rhizospheric community did not change significantly. Apparently, the endophytic community is more prone to face dysbiosis as compared to the rhizospheric community. Next, to advance our understandings on plant defense/stress response in the post-exposure period, the first genomic database of J. effusus was developed (Chapter 3). The de novo transcriptome assembly was previously prepared by sequencing the transcriptome of 19 genotypes of J. effusus. The accuracy of the assembly was tested through functional analysis with closer phylogenetic relatives of J. effusus. After confirming the high quality of the assembly via computational, statistical, and manual analyses, targeted investigations on specific genes involved in plant defense were carried out. It was revealed that the KEGG pathway Genes involved in stress response for “plant-pathogen interaction” was almost complete, including for J. effusus expressed genes related to “hypersensitive response”, “defense-related were identified gene induction”, and “programmed cell death”. The developed database for plant- was further tested in preliminary metaproteomics, which was performed pathogen interactions on a subset of exposed and un-exposed plant tissues. The extraction of pathway. proteins from plants in the post-exposure period were less efficient, nevertheless, pre-exposure proteins were identified to be involved in typical plant processes such as photosynthesis, biosynthesis of polyphenol compounds, and others were related to general metabolic processes such as glycolysis, citric acid cycle, cell division, oxidative VI ABSTRACT pentose phosphate pathway. The bacterial proteins matching in the post- exposure period were mostly related to the bacteria involved in oxidation of one-carbon (C1) compounds.
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