Publications

Publications in peer reviewed journals

15 Publications found
  • Is Too Much Fertilizer a Problem?

    Sedlacek C, Giguere A, Pjevac P
    2020 - Front. Young Minds, 8: 63

    Abstract: 

    Fertilizers are added to crops in order to produce enough food to feed the human population. Fertilizers provide crops with nutrients like potassium, phosphorus, and nitrogen, which allow crops to grow bigger, faster, and to produce more food. Nitrogen in particular is an essential nutrient for the growth of every organism on Earth. Nitrogen is all around us and makes up about 78% of the air you breathe. However, plants and animals cannot use the nitrogen gas in the air. To grow, plants require nitrogen compounds from the soil, which can be produced naturally or be provided by fertilizers. However, applying excessive amounts of fertilizer leads to the release of harmful greenhouse gases into the atmosphere and the eutrophication of our waterways. Scientists are currently trying to find solutions to reduce the environmentally harmful effects of fertilizers, without reducing the amount of food we can produce when using them.

  • Conversion of Rutin, a Prevalent Dietary Flavonol, by the Human Gut Microbiota.

    Riva A, Kolimár D, Spittler A, Wisgrill L, Herbold CW, Abrankó L, Berry D
    2020 - Front Microbiol, 585428

    Abstract: 

    The gut microbiota plays a pivotal role in the conversion of dietary flavonoids, which can affect their bioavailability and bioactivity and thereby their health-promoting properties. The ability of flavonoids to metabolically-activate the microbiota has, however, not been systematically evaluated. In the present study, we used a fluorescence-based single-cell activity measure [biorthogonal non-canonical ammino acid-tagging (BONCAT)] combined with fluorescence activated cell sorting (FACS) to determine which microorganisms are metabolically-active after amendment of the flavonoid rutin. We performed anaerobic incubations of human fecal microbiota amended with rutin and in the presence of the cellular activity marker L-azidohomoalanine (AHA) to detect metabolically-active cells. We found that 7.3% of cells in the gut microbiota were active after a 6 h incubation and 26.9% after 24 h. We then sorted BONCAT-positive cells and observed an enrichment of ( and ), , and species in the rutin-responsive fraction of the microbiota. There was marked inter-individual variability in the appearance of rutin conversion products after incubation with rutin. Consistent with this, there was substantial variability in the abundance of rutin-responsive microbiota among different individuals. Specifically, we observed that were associated with conversion of rutin into quercetin-3-glucoside (Q-glc) and were associated with quercetin (Q) production. This suggests that individual microbiotas differ in their ability to metabolize rutin and utilize different conversion pathways.

  • Polyphenol Exposure, Metabolism, and Analysis: A Global Exposomics Perspective.

    Oesterle I, Braun D, Berry D, Wisgrill L, Rompel A, Warth B
    2020 - Annu Rev Food Sci Technol, .

    Abstract: 

    Polyphenols are generally known for their health benefits and estimating actual exposure levels in health-related studies can be improved by human biomonitoring. Here, the application of newly available exposomic and metabolomic technology, notably high-resolution mass spectrometry, in the context of polyphenols and their biotransformation products, is reviewed. Comprehensive workflows for investigating these important bioactives in biological fluids or microbiome-related experiments are scarce. Consequently, this new era of nontargeted analysis and omic-scale exposure assessment offers a unique chance for better assessing exposure to, as well as metabolism of, polyphenols. In clinical and nutritional trials, polyphenols can be investigated simultaneously with the plethora of other chemicals to which we are exposed, i.e., the exposome, which may interact abundantly and modulate bioactivity. This research direction aims at ultimately eluting into a true systems biology/toxicology evaluation of health effects associated with polyphenol exposure, especially during early life, to unravel their potential for preventing chronic diseases. Expected final online publication date for the , Volume 12 is March 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

  • Optofluidic Raman-activated cell sorting for targeted genome retrieval or cultivation of microbial cells with specific functions.

    Lee KS, Pereira FC, Palatinszky M, Behrendt L, Alcolombri U, Berry D, Wagner M, Stocker R
    2020 - Nat Protoc, -

    Abstract: 

    Stable isotope labeling of microbial taxa of interest and their sorting provide an efficient and direct way to answer the question "who does what?" in complex microbial communities when coupled with fluorescence in situ hybridization or downstream 'omics' analyses. We have developed a platform for automated Raman-based sorting in which optical tweezers and microfluidics are used to sort individual cells of interest from microbial communities on the basis of their Raman spectra. This sorting of cells and their downstream DNA analysis, such as by mini-metagenomics or single-cell genomics, or cultivation permits a direct link to be made between the metabolic roles and the genomes of microbial cells within complex microbial communities, as well as targeted isolation of novel microbes with a specific physiology of interest. We describe a protocol from sample preparation through Raman-activated live cell sorting. Subsequent cultivation of sorted cells is described, whereas downstream DNA analysis involves well-established approaches with abundant methods available in the literature. Compared with manual sorting, this technique provides a substantially higher throughput (up to 500 cells per h). Furthermore, the platform has very high sorting accuracy (98.3 ± 1.7%) and is fully automated, thus avoiding user biases that might accompany manual sorting. We anticipate that this protocol will empower in particular environmental and host-associated microbiome research with a versatile tool to elucidate the metabolic contributions of microbial taxa within their complex communities. After a 1-d preparation of cells, sorting takes on the order of 4 h, depending on the number of cells required.

  • Anaerobic bacterial degradation of protein and lipid macromolecules in subarctic marine sediment.

    Pelikan C, Wasmund K, Glombitza C, Hausmann B, Herbold CW, Flieder M, Loy A
    2020 - ISME J, .

    Abstract: 

    Microorganisms in marine sediments play major roles in marine biogeochemical cycles by mineralizing substantial quantities of organic matter from decaying cells. Proteins and lipids are abundant components of necromass, yet the taxonomic identities of microorganisms that actively degrade them remain poorly resolved. Here, we revealed identities, trophic interactions, and genomic features of bacteria that degraded C-labeled proteins and lipids in cold anoxic microcosms containing sulfidic subarctic marine sediment. Supplemented proteins and lipids were rapidly fermented to various volatile fatty acids within 5 days. DNA-stable isotope probing (SIP) suggested Psychrilyobacter atlanticus was an important primary degrader of proteins, and Psychromonas members were important primary degraders of both proteins and lipids. Closely related Psychromonas populations, as represented by distinct 16S rRNA gene variants, differentially utilized either proteins or lipids. DNA-SIP also showed C-labeling of various Deltaproteobacteria within 10 days, indicating trophic transfer of carbon to putative sulfate-reducers. Metagenome-assembled genomes revealed the primary hydrolyzers encoded secreted peptidases or lipases, and enzymes for catabolism of protein or lipid degradation products. Psychromonas species are prevalent in diverse marine sediments, suggesting they are important players in organic carbon processing in situ. Together, this study provides new insights into the identities, functions, and genomes of bacteria that actively degrade abundant necromass macromolecules in the seafloor.

  • Rational design of a microbial consortium of mucosal sugar utilizers reduces Clostridiodes difficile colonization.

    Pereira FC, Wasmund K, Cobankovic I, Jehmlich N, Herbold CW, Lee KS, Sziranyi B, Vesely C, Decker T, Stocker R, Warth B, von Bergen M, Wagner M, Berry D
    2020 - Nat Commun, 1: 5104

    Abstract: 

    Many intestinal pathogens, including Clostridioides difficile, use mucus-derived sugars as crucial nutrients in the gut. Commensals that compete with pathogens for such nutrients are therefore ecological gatekeepers in healthy guts, and are attractive candidates for therapeutic interventions. Nevertheless, there is a poor understanding of which commensals use mucin-derived sugars in situ as well as their potential to impede pathogen colonization. Here, we identify mouse gut commensals that utilize mucus-derived monosaccharides within complex communities using single-cell stable isotope probing, Raman-activated cell sorting and mini-metagenomics. Sequencing of cell-sorted fractions reveals members of the underexplored family Muribaculaceae as major mucin monosaccharide foragers, followed by members of Lachnospiraceae, Rikenellaceae, and Bacteroidaceae families. Using this information, we assembled a five-member consortium of sialic acid and N-acetylglucosamine utilizers that impedes C. difficile's access to these mucosal sugars and impairs pathogen colonization in antibiotic-treated mice. Our findings underscore the value of targeted approaches to identify organisms utilizing key nutrients and to rationally design effective probiotic mixtures.

  • A refined set of rRNA-targeted oligonucleotide probes for in situ detection and quantification of ammonia-oxidizing bacteria.

    Lukumbuzya M, Kristensen JM, Kitzinger K, Pommerening-Roser A, Nielsen PH, Wagner M, Daims H, Pjevac P
    2020 - Water Res, 116372

    Abstract: 

    Ammonia-oxidizing bacteria (AOB) of the betaproteobacterial genera Nitrosomonas and Nitrosospira are key nitrifying microorganisms in many natural and engineered ecosystems. Since many AOB remain uncultured, fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes has been one of the most widely used approaches to study the community composition, abundance, and other features of AOB directly in environmental samples. However, the established and widely used AOB-specific 16S rRNA-targeted FISH probes were designed up to two decades ago, based on much smaller rRNA gene sequence datasets than available today. Several of these probes cover their target AOB lineages incompletely and suffer from a weak target specificity, which causes cross-hybridization of probes that should detect different AOB lineages. Here, a set of new highly specific 16S rRNA-targeted oligonucleotide probes was developed and experimentally evaluated that complements the existing probes and enables the specific detection and differentiation of the known, major phylogenetic clusters of betaproteobacterial AOB. The new probes were successfully applied to visualize and quantify AOB in activated sludge and biofilm samples from seven pilot- and full-scale wastewater treatment systems. Based on its improved target group coverage and specificity, the refined probe set will facilitate future in situ analyses of AOB.

  • Composition and activity of nitrifier communities in soil are unresponsive to elevated temperature and CO, but strongly affected by drought.

    Séneca J, Pjevac P, Canarini A, Herbold CW, Zioutis C, Dietrich M, Simon E, Prommer J, Bahn M, Pötsch EM, Wagner M, Wanek W, Richter A
    2020 - ISME J,

    Abstract: 

    Nitrification is a fundamental process in terrestrial nitrogen cycling. However, detailed information on how climate change affects the structure of nitrifier communities is lacking, specifically from experiments in which multiple climate change factors are manipulated simultaneously. Consequently, our ability to predict how soil nitrogen (N) cycling will change in a future climate is limited. We conducted a field experiment in a managed grassland and simultaneously tested the effects of elevated atmospheric CO, temperature, and drought on the abundance of active ammonia-oxidizing bacteria (AOB) and archaea (AOA), comammox (CMX) Nitrospira, and nitrite-oxidizing bacteria (NOB), and on gross mineralization and nitrification rates. We found that N transformation processes, as well as gene and transcript abundances, and nitrifier community composition were remarkably resistant to individual and interactive effects of elevated CO and temperature. During drought however, process rates were increased or at least maintained. At the same time, the abundance of active AOB increased probably due to higher NH availability. Both, AOA and comammox Nitrospira decreased in response to drought and the active community composition of AOA and NOB was also significantly affected. In summary, our findings suggest that warming and elevated CO have only minor effects on nitrifier communities and soil biogeochemical variables in managed grasslands, whereas drought favors AOB and increases nitrification rates. This highlights the overriding importance of drought as a global change driver impacting on soil microbial community structure and its consequences for N cycling.

  • Gut microbiota and undigested food constituents modify toxin composition and suppress the genotoxicity of a naturally occurring mixture of Alternaria toxins in vitro.

    Crudo F, Aichinger G, Mihajlovic J, Dellafiora L, Varga E, Puntscher H, Warth B, Dall'Asta C, Berry D, Marko D
    2020 - Arch. Toxicol.,

    Abstract: 

    Molds of the genus Alternaria produce several mycotoxins, some of which may pose a threat for health due to their genotoxicity. Due to the lack of adequate toxicological and occurrence data, they are currently not regulated. Interactions between mycotoxins, gut microbiota and food constituents might occur after food ingestion, modifying the bioavailability and, therefore, overall toxicity of mycotoxins. The present work aimed to investigate the impact of in vitro short-term fecal incubation on the in vitro DNA-damaging effects exerted by 5 µg/mL of an Alternaria alternata extract, containing, among others, 15 nM alternariol, 12 nM alternariol monomethyl ether, 241 nM altertoxin II and 301 nM stemphyltoxin III, all of which are known as genotoxic. The involvement of microorganisms, undigested food constituents and soluble substances of human fecal samples in modifying the composition and the genotoxicity of the extract was investigated through the application of LC-MS/MS analysis and comet assays in HT-29 cells. Results showed that the potential of the mycotoxins to induce DNA strand breaks was almost completely quenched, even before anaerobic incubation, by contact with the different fractions of the fecal samples, while the potency to induce formamidopyrimidine DNA glycosylase (FPG)-sensitive sites was only slightly reduced. These effects were in line with a reduction of mycotoxin concentrations found in samples analyzed by LC-MS/MS. Although a direct correlation between the metabolic activity of the gut microbiota and modifications in mycotoxin contents was not clearly observed, adsorptive phenomena to bacterial cells and to undigested food constituents might explain the observed modifications.

  • The role of metal contamination in shaping microbial communities in heavily polluted marine sediments.

    Di Cesare A, Pjevac P, Eckert E, Curkov N, Miko Šparica M, Corno G, Orlić S
    2020 - Environ. Pollut., 114823

    Abstract: 

    Microorganisms in coastal sediments are fundamental for ecosystem functioning, and regulate processes relevant in global biogeochemical cycles. Still, our understanding of the effects anthropogenic perturbation and pollution can have on microbial communities in marine sediments is limited. We surveyed the microbial diversity, and the occurrence and abundance of metal and antibiotic resistance genes is sediments collected from the Pula Bay (Croatia), one of the most significantly polluted sites along the Croatian coast. With a collection of 14 samples from the bay area, we were able to generate a detailed status quo picture of a site that only recently started a cleaning and remediation process (closing of sewage pipes and reduction of industrial activity). The concentrations of heavy metals in Pula Bay sediments are significantly higher than in pristine sediments from the Adriatic Sea, and in some cases, manifold exceed international sediment quality guidelines. While the sedimentary concentrations of heavy metals did significantly influence the abundance of the tested metal resistance genes, no strong effect of heavy metal pollution on the overall microbial community composition was observed. Like in many other marine sediments, Gammaproteobacteria, Bacteroidota and Desulfobacterota dominated the microbial community composition in most samples, and community assembly was primarily driven by water column depth and nutrient (carbon and nitrogen) availability, regardless of the degree of heavy metal pollution.

  • Crypt residing bacteria and proximal colonic carcinogenesis in a mouse model of Lynch syndrome.

    Lang M, Baumgartner M, Rożalska A, Frick A, Riva A, Jarek M, Berry D, Gasche C
    2020 - Int. J. Cancer, 8: 2316-2326

    Abstract: 

    Colorectal cancer is a multifactorial disease involving inherited DNA mutations, environmental factors, gut inflammation and intestinal microbiota. Certain germline mutations within the DNA mismatch repair system are associated with Lynch syndrome tumors including right-sided colorectal cancer with mucinous phenotype and presence of an inflammatory infiltrate. Such tumors are more often associated with bacterial biofilms, which may contribute to disease onset and progression. Inflammatory bowel diseases are also associated with colorectal cancer and intestinal dysbiosis. Herein we addressed the question, whether inflammation can aggravate colorectal cancer development under mismatch repair deficiency. MSH2 mice were crossed into the IL-10 background to study the importance of inflammation and mucosal bacteria as a driver of tumorigenesis in a Lynch syndrome mouse model. An increase in large bowel tumorigenesis was found in double knockout mice both under conventional housing and under specific pathogen-free conditions. This increase was mostly due to the development of proximal tumors, a hotspot for tumorigenesis in Lynch syndrome, and was associated with a higher degree of inflammation. Additionally, bacterial invasion into the mucus of tumor crypts was observed in the proximal tumors. Inflammation shifted fecal and mucosal microbiota composition and was associated with enrichment in Escherichia-Shigella as well as Akkermansia, Bacteroides and Parabacteroides genera in fecal samples. Tumor-bearing double knockout mice showed a similar enrichment for Escherichia-Shigella and Parabacteroides. Lactobacilli, Lachnospiraceae and Muribaculaceae family members were depleted upon inflammation. In summary, chronic inflammation aggravates colonic tumorigenesis under mismatch repair deficiency and is associated with a shift in microbiota composition.

  • Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems.

    Yang Y, Daims H, Liu Y, Herbold CW, Pjevac P, Lin JG, Li M, Gu JD
    2020 - MBio, 2: e03175-19

    Abstract: 

    The recent discovery of complete ammonia oxidizers (comammox) contradicts the paradigm that chemolithoautotrophic nitrification is always catalyzed by two different microorganisms. However, our knowledge of the survival strategies of comammox in complex ecosystems, such as full-scale wastewater treatment plants (WWTPs), remains limited. Analyses of genomes and transcriptomes of four comammox organisms from two full-scale WWTPs revealed that comammox were active and showed a surprisingly high metabolic versatility. A gene cluster for the utilization of urea and a gene encoding cyanase suggest that comammox may use diverse organic nitrogen compounds in addition to free ammonia as the substrates. The comammox organisms also encoded the genomic potential for multiple alternative energy metabolisms, including respiration with hydrogen, formate, and sulfite as electron donors. Pathways for the biosynthesis and degradation of polyphosphate, glycogen, and polyhydroxyalkanoates as intracellular storage compounds likely help comammox survive unfavorable conditions and facilitate switches between lifestyles in fluctuating environments. One of the comammox strains acquired from the anaerobic tank encoded and transcribed genes involved in homoacetate fermentation or in the utilization of exogenous acetate, both pathways being unexpected in a nitrifying bacterium. Surprisingly, this strain also encoded a respiratory nitrate reductase which has not yet been found in any other genome and might confer a selective advantage to this strain over other strains in anoxic conditions. The discovery of comammox in the genus changes our perception of nitrification. However, genomes of comammox organisms have not been acquired from full-scale WWTPs, and very little is known about their survival strategies and potential metabolisms in complex wastewater treatment systems. Here, four comammox metagenome-assembled genomes and metatranscriptomic data sets were retrieved from two full-scale WWTPs. Their impressive and-among nitrifiers-unsurpassed ecophysiological versatility could make comammox an interesting target for optimizing nitrification in current and future bioreactor configurations.

  • Single cell analyses reveal contrasting life strategies of the two main nitrifiers in the ocean.

    Kitzinger K, Marchant HK, Bristow LA, Herbold CW, Padilla CC, Kidane AT, Littmann S, Daims H, Pjevac P, Stewart FJ, Wagner M, Kuypers MMM
    2020 - Nat Commun, 1: 767

    Abstract: 

    Nitrification, the oxidation of ammonia via nitrite to nitrate, is a key process in marine nitrogen (N) cycling. Although oceanic ammonia and nitrite oxidation are balanced, ammonia-oxidizing archaea (AOA) vastly outnumber the main nitrite oxidizers, the bacterial Nitrospinae. The ecophysiological reasons for this discrepancy in abundance are unclear. Here, we compare substrate utilization and growth of Nitrospinae to AOA in the Gulf of Mexico. Based on our results, more than half of the Nitrospinae cellular N-demand is met by the organic-N compounds urea and cyanate, while AOA mainly assimilate ammonium. Nitrospinae have, under in situ conditions, around four-times higher biomass yield and five-times higher growth rates than AOA, despite their ten-fold lower abundance. Our combined results indicate that differences in mortality between Nitrospinae and AOA, rather than thermodynamics, biomass yield and cell size, determine the abundances of these main marine nitrifiers. Furthermore, there is no need to invoke yet undiscovered, abundant nitrite oxidizers to explain nitrification rates in the ocean.

  • Transcriptomic Response of Nitrosomonas europaea Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth.

    Sedlacek CJ, Giguere AT, Dobie MD, Mellbye BL, Ferrell RV, Woebken D, Sayavedra-Soto LA, Bottomley PJ, Daims H, Wagner M, Pjevac P
    2020 - mSystems, 1: e00562-19

    Abstract: 

    Ammonia-oxidizing microorganisms perform the first step of nitrification, the oxidation of ammonia to nitrite. The bacterium is the best-characterized ammonia oxidizer to date. Exposure to hypoxic conditions has a profound effect on the physiology of , e.g., by inducing nitrifier denitrification, resulting in increased nitric and nitrous oxide production. This metabolic shift is of major significance in agricultural soils, as it contributes to fertilizer loss and global climate change. Previous studies investigating the effect of oxygen limitation on have focused on the transcriptional regulation of genes involved in nitrification and nitrifier denitrification. Here, we combine steady-state cultivation with whole-genome transcriptomics to investigate the overall effect of oxygen limitation on Under oxygen-limited conditions, growth yield was reduced and ammonia-to-nitrite conversion was not stoichiometric, suggesting the production of nitrogenous gases. However, the transcription of the principal nitric oxide reductase (cNOR) did not change significantly during oxygen-limited growth, while the transcription of the nitrite reductase-encoding gene () was significantly lower. In contrast, both heme-copper-containing cytochrome oxidases encoded by were upregulated during oxygen-limited growth. Particularly striking was the significant increase in transcription of the B-type heme-copper oxidase, proposed to function as a nitric oxide reductase (sNOR) in ammonia-oxidizing bacteria. In the context of previous physiological studies, as well as the evolutionary placement of sNOR with regard to other heme-copper oxidases, these results suggest sNOR may function as a high-affinity terminal oxidase in and other ammonia-oxidizing bacteria. Nitrification is a ubiquitous microbially mediated process in the environment and an essential process in engineered systems such as wastewater and drinking water treatment plants. However, nitrification also contributes to fertilizer loss from agricultural environments, increasing the eutrophication of downstream aquatic ecosystems, and produces the greenhouse gas nitrous oxide. As ammonia-oxidizing bacteria are the most dominant ammonia-oxidizing microbes in fertilized agricultural soils, understanding their responses to a variety of environmental conditions is essential for curbing the negative environmental effects of nitrification. Notably, oxygen limitation has been reported to significantly increase nitric oxide and nitrous oxide production during nitrification. Here, we investigate the physiology of the best-characterized ammonia-oxidizing bacterium, , growing under oxygen-limited conditions.

  • The role of gut microbiota, butyrate and proton pump inhibitors in amyotrophic lateral sclerosis: a systematic review.

    Erber AC, Cetin H, Berry D, Schernhammer ES
    2020 - Int J Neurosci, 7: 727-735

    Abstract: 

    We conducted a systematic review on existing literature in humans and animals, linking the gut microbiome with amyotrophic lateral sclerosis (ALS). Additionally, we sought to explore the role of the bacterially produced metabolite butyrate as well as of proton pump inhibitors (PPIs) in these associations. Following PRISMA guidelines for systematic literature reviews, four databases (Medline, Scopus, Embase and Web of Science) were searched and screened by two independent reviewers against defined inclusion criteria. Six studies in humans and six animal studies were identified, summarized and reviewed. Overall, the evidence accrued to date is supportive of changes in the gut microbiome being associated with ALS risk, and potentially progression, though observational studies are small (describing a total of 145 patients with ALS across all published studies), and not entirely conclusive. With emerging studies beginning to apply metagenome sequencing, more clarity regarding the importance and promise of the gut microbiome in ALS can be expected. Future studies may also help establish the therapeutic potential of butyrate, and the role of PPIs in these associations.

Book chapters and other publications

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