Publications

Publications in peer reviewed journals

12 Publications found
  • The cooling tower water microbiota: seasonal dynamics and co-occurrence of bacterial and protist phylotypes

    Tsao HF, Scheikl U, Herbold C, Indra A, Walochnik J, Horn M
    2019 - Water Res., 464-479

    Abstract: 

    Cooling towers for heating, ventilation and air conditioning are ubiquitous in the built environment. Often located on rooftops, their semi-open water basins provide a suitable environment for microbial growth. They are recognized as a potential source of bacterial pathogens and have been associated with disease outbreaks such as Legionnaires' disease. While measures to minimize public health risks are in place, the general microbial and protist community structure and dynamics in these systems remain largely elusive. In this study, we analysed the microbiome of the bulk water from the basins of three cooling towers by 16S and 18S rRNA gene amplicon sequencing over the course of one year. Bacterial diversity in all three towers was broadly comparable to other freshwater systems, yet less diverse than natural environments; the most abundant taxa are also frequently found in freshwater or drinking water. While each cooling tower had a pronounced site-specific microbial community, taxa shared among all locations mainly included groups generally associated with biofilm formation. We also detected several groups related to known opportunistic pathogens, such as Legionella, Mycobacterium, and Pseudomonas species, albeit at generally low abundance. Although cooling towers represent a rather stable environment, microbial community composition was highly dynamic and subject to seasonal change. Protists are important members of the cooling tower water microbiome and known reservoirs for bacterial pathogens. Co-occurrence analysis of bacteria and protist taxa successfully captured known interactions between amoeba-associated bacteria and their hosts, and predicted a large number of additional relationships involving ciliates and other protists. Together, this study provides an unbiased and comprehensive overview of microbial diversity of cooling tower water basins, establishing a framework for investigating and assessing public health risks associated with these man-made freshwater environments.

  • Bacterial interactions during sequential degradation of cyanobacterial necromass in a sulfidic arctic marine sediment.

    Müller AL, Pelikan C, de Rezende JR, Wasmund K, Putz M, Glombitza C, Kjeldsen KU, Jørgensen BB, Loy A
    2018 - Environ. Microbiol., 8: 2927-2940

    Abstract: 

    Seafloor microorganisms impact global carbon cycling by mineralizing vast quantities of organic matter (OM) from pelagic primary production, which is predicted to increase in the Arctic because of diminishing sea ice cover. We studied microbial interspecies-carbon-flow during anaerobic OM degradation in arctic marine sediment using stable isotope probing. We supplemented sediment incubations with C-labeled cyanobacterial necromass (spirulina), mimicking fresh OM input, or acetate, an important OM degradation intermediate and monitored sulfate reduction rates and concentrations of volatile fatty acids (VFAs) during substrate degradation. Sequential 16S rRNA gene and transcript amplicon sequencing and fluorescence in situ hybridization combined with Raman microspectroscopy revealed that only few bacterial species were the main degraders of C-spirulina necromass. Psychrilyobacter, Psychromonas, Marinifilum, Colwellia, Marinilabiaceae and Clostridiales species were likely involved in the primary hydrolysis and fermentation of spirulina. VFAs, mainly acetate, produced from spirulina degradation were mineralized by sulfate-reducing bacteria and an Arcobacter species. Cellular activity of Desulfobacteraceae and Desulfobulbaceae species during acetoclastic sulfate reduction was largely decoupled from relative 16S rRNA gene abundance shifts. Our findings provide new insights into the identities and physiological constraints that determine the population dynamics of key microorganisms during complex OM degradation in arctic marine sediments.© 2018 Society for Applied Microbiology and John Wiley & Sons Ltd.

  • Bottled aqua incognita: microbiota assembly and dissolved organic matter diversity in natural mineral waters.

    Lesaulnier CC, Herbold CW, Pelikan C, Berry D, Gérard C, Le Coz X, Gagnot S, Niggemann J, Dittmar T, Singer GA, Loy A
    2017 - Microbiome, 1: 126

    Abstract: 

    Non-carbonated natural mineral waters contain microorganisms that regularly grow after bottling despite low concentrations of dissolved organic matter (DOM). Yet, the compositions of bottled water microbiota and organic substrates that fuel microbial activity, and how both change after bottling, are still largely unknown.
    We performed a multifaceted analysis of microbiota and DOM diversity in 12 natural mineral waters from six European countries. 16S rRNA gene-based analyses showed that less than 10 species-level operational taxonomic units (OTUs) dominated the bacterial communities in the water phase and associated with the bottle wall after a short phase of post-bottling growth. Members of the betaproteobacterial genera Curvibacter, Aquabacterium, and Polaromonas (Comamonadaceae) grew in most waters and represent ubiquitous, mesophilic, heterotrophic aerobes in bottled waters. Ultrahigh-resolution mass spectrometry of DOM in bottled waters and their corresponding source waters identified thousands of molecular formulae characteristic of mostly refractory, soil-derived DOM.
    The bottle environment, including source water physicochemistry, selected for growth of a similar low-diversity microbiota across various bottled waters. Relative abundance changes of hundreds of multi-carbon molecules were related to growth of less than ten abundant OTUs. We thus speculate that individual bacteria cope with oligotrophic conditions by simultaneously consuming diverse DOM molecules.

  • AmoA-Targeted Polymerase Chain Reaction Primers for the Specific Detection and Quantification of Comammox in the Environment.

    Pjevac P, Schauberger C, Poghosyan L, Herbold CW, van Kessel MAHJ, Daebeler A, Steinberger M, Jetten MSM, Lücker S, Wagner M, Daims H
    2017 - Front Microbiol, 1508

    Abstract: 

    Nitrification, the oxidation of ammonia via nitrite to nitrate, has always been considered to be catalyzed by the concerted activity of ammonia- and nitrite-oxidizing microorganisms. Only recently, complete ammonia oxidizers ("comammox"), which oxidize ammonia to nitrate on their own, were identified in the bacterial genus , previously assumed to contain only canonical nitrite oxidizers. are widespread in nature, but for assessments of the distribution and functional importance of comammox in ecosystems, cultivation-independent tools to distinguish comammox from strictly nitrite-oxidizing are required. Here we developed new PCR primer sets that specifically target the genes coding for subunit A of the distinct ammonia monooxygenase of comammox . While existing primers capture only a fraction of the known comammox diversity, the new primer sets cover as much as 95% of the comammox clade A and 92% of the clade B sequences in a reference database containing 326 comammox genes with sequence information at the primer binding sites. Application of the primers to 13 samples from engineered systems (a groundwater well, drinking water treatment and wastewater treatment plants) and other habitats (rice paddy and forest soils, rice rhizosphere, brackish lake sediment and freshwater biofilm) detected comammox in all samples and revealed a considerable diversity of comammox in most habitats. Excellent primer specificity for comammox was achieved by avoiding the use of highly degenerate primer preparations and by using equimolar mixtures of oligonucleotides that match existing comammox genes. Quantitative PCR with these equimolar primer mixtures was highly sensitive and specific, and enabled the efficient quantification of clade A and clade B comammox gene copy numbers in environmental samples. The measured relative abundances of comammox , compared to canonical ammonia oxidizers, were highly variable across environments. The new comammox -targeted primers enable more encompassing future studies of nitrifying microorganisms in diverse habitats. For example, they may be used to monitor the population dynamics of uncultured comammox organisms under changing environmental conditions and in response to altered treatments in engineered and agricultural ecosystems.

  • Evaluating the Detection of Hydrocarbon-Degrading Bacteria in 16S rRNA Gene Sequencing Surveys.

    Berry D, Gutierrez T
    2017 - Front Microbiol, 896

    Abstract: 

    Hydrocarbonoclastic bacteria (HCB) play a key role in the biodegradation of oil hydrocarbons in marine and other environments. A small number of taxa have been identified as obligate HCB, notably the Gammaproteobacterial genera , and , as well as the Alphaproteobacterial genus . Detection of HCB in amplicon-based sequencing surveys relies on high coverage by PCR primers and accurate taxonomic classification. In this study, we performed a phylogenetic analysis to identify 16S rRNA gene sequence regions that represent the breadth of sequence diversity within these taxa. Using validated sequences, we evaluated 449 universal 16S rRNA gene-targeted bacterial PCR primer pairs for their coverage of these taxa. The results of this analysis provide a practical framework for selection of suitable primer sets for optimal detection of HCB in sequencing surveys.

  • Members of the Oral Microbiota Are Associated with IL-8 Release by Gingival Epithelial Cells in Healthy Individuals.

    Schueller K, Riva A, Pfeiffer S, Berry D, Somoza V
    2017 - Front Microbiol, 416

    Abstract: 

    The triggers for the onset of oral diseases are still poorly understood. The aim of this study was to characterize the oral bacterial community in healthy humans and its association with nutrition, oral hygiene habits, and the release of the inflammatory marker IL-8 from gingival epithelial cells (GECs) with and without stimulation by bacterial endotoxins to identify possible indicator operational taxonomic units (OTUs) associated with inflammatory marker status. GECs from 21 healthy participants (13 females, 8 males) were incubated with or without addition of bacterial lipopolysaccharides (LPSs), and the oral microbiota was profiled using 16S rRNA gene-targeted sequencing. The basal IL-8 release after 6 h was between 9.9 and 98.2 pg/ml, and bacterial communities were characteristic for healthy oral microbiota. The composition of the oral microbiota was associated with basal IL-8 levels, the intake of meat, tea, white wine, sweets and the use of chewing gum, as well as flossing habits, allergies, gender and body mass index. Additionally, eight OTUs were associated with high basal levels of IL-8 and GEC response to LPS, with high basal levels of IL-8, and 1 with low basal levels of IL8. The identification of indicator bacteria in healthy subjects with high levels of IL-8 release is of importance as they may be promising early warning indicators for the possible onset of oral diseases.

  • A 12-week intervention with nonivamide, a TRPV1 agonist, prevents a dietary-induced body fat gain and increases peripheral serotonin in moderately overweight subjects.

    Hochkogler CM, Lieder B, Rust P, Berry D, Meier SM, Pignitter M, Riva A, Leitinger A, Bruk A, Wagner S, Hans J, Widder S, Ley JP, Krammer GE, Somoza V
    2017 - Mol Nutr Food Res, 1600731

    Abstract: 

    A bolus administration of 0.15 mg nonivamide has previously been demonstrated to reduce energy intake in moderately overweight men. This 12-week intervention investigated whether a daily consumption of nonivamide in a protein-based product formulation promotes a reduction in body weight in healthy overweight subjects and affects outcome measures associated with mechanisms regulating food intake, e.g. plasma concentrations of (an)orexigenic hormones, energy substrates as well as changes in fecal microbiota.
    Nineteen overweight subjects were randomly assigned to either a control (C) or a nonivamide (NV) group. Changes in the body composition and plasma concentrations of satiating hormones were determined at fasting and 15, 30, 60, 90, and 120 min after a glucose load. Participants were instructed to consume 0.15 mg nonivamide per day in 450 mL of a milk shake additionally to their habitual diet. After treatment, a group difference in body fat mass change (-0.61 ± 0.36% in NV and +1.36 ± 0.38% in C) and an increase in postprandial plasma serotonin were demonstrated. Plasma metabolome and fecal microbiome read outs were not affected.
    A daily intake of 0.15 mg nonivamide helps to support to maintain a healthy body composition.

  • Pediatric obesity is associated with an altered gut microbiota and discordant shifts in Firmicutes populations.

    Riva A, Borgo F, Lassandro C, Verduci E, Morace G, Borghi E, Berry D
    2017 - Environ. Microbiol., 1: 95-105

    Abstract: 

    An altered gut microbiota has been linked to obesity in adulthood, although little is known about childhood obesity. The aim of this study was to characterize the composition of the gut microbiota in obese (n = 42) and normal-weight (n = 36) children aged 6 to 16. Using 16S rRNA gene-targeted sequencing, we evaluated taxa with differential abundance according to age- and sex-normalized body mass index (BMI z-score). Obesity was associated with an altered gut microbiota characterized by elevated levels of Firmicutes and depleted levels of Bacteroidetes. Correlation network analysis revealed that the gut microbiota of obese children also had increased correlation density and clustering of operational taxonomic units (OTUs). Members of the Bacteroidetes were generally better predictors of BMI z-score and obesity than Firmicutes, which was likely due to discordant responses of Firmicutes OTUs. In accordance with these observations, the main metabolites produced by gut bacteria, short chain fatty acids (SCFAs), were higher in obese children, suggesting elevated substrate utilisation. Multiple taxa were correlated with SCFA levels, reinforcing the tight link between the microbiota, SCFAs and obesity. Our results suggest that gut microbiota dysbiosis and elevated fermentation activity may be involved in the etiology of childhood obesity.

  • Intensive cryptic microbial iron cycling in the low iron water column of the meromictic Lake Cadagno.

    Berg JS, Michellod D, Pjevac P, Martinez-Perez C, Buckner CR, Hach PF, Schubert CJ, Milucka J, Kuypers MM
    2016 - Environ. Microbiol., 12: 5288-5302

    Abstract: 

    Iron redox reactions play an important role in carbon remineralization, supporting large microbial communities in iron-rich terrestrial and aquatic sediments. Stratified water columns with comparably low iron concentrations are globally widespread, but microbial iron cycling in these systems has largely been ignored. We found evidence for unexpectedly high iron turnover rates in the low (1-2 µmol·l ) iron waters of Lake Cadagno. Light-dependent, biological iron oxidation rates (1.4-13.8 µmol·l ·d ) were even higher than in ferruginous lakes with well-studied microbial iron cycles. This photoferrotrophic iron oxidation may account for up to 10% of total primary production in the chemocline. Iron oxides could not be detected and were presumably reduced immediately by iron-reducing microorganisms. Sequences of putative iron oxidizers and reducers were retrieved from in situ 16S rRNA gene amplicon libraries and some of these bacteria were identified in our enrichment cultures supplemented with Fe(II) and FeS. Based on our results, we propose a model in which iron is oxidized by photoferrotrophs and microaerophiles, and iron oxides are immediately reduced by heterotrophic iron reducers, resulting in a cryptic iron cycle. We hypothesize that microbial iron cycling may be more prevalent in water column redoxclines, especially those within the photic zone, than previously believed.

  • Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms.

    Hausmann B, Knorr KH, Schreck K, Tringe SG, Glavina Del Rio T, Loy A, Pester M
    2016 - ISME J, 10: 2365-75

    Abstract: 

    Dissimilatory sulfate reduction in peatlands is sustained by a cryptic sulfur cycle and effectively competes with methanogenic degradation pathways. In a series of peat soil microcosms incubated over 50 days, we identified bacterial consortia that responded to small, periodic additions of individual fermentation products (formate, acetate, propionate, lactate or butyrate) in the presence or absence of sulfate. Under sulfate supplementation, net sulfate turnover (ST) steadily increased to 16-174 nmol cm(-3) per day and almost completely blocked methanogenesis. 16S rRNA gene and cDNA amplicon sequencing identified microorganisms whose increases in ribosome numbers strongly correlated to ST. Natively abundant (⩾0.1% estimated genome abundance) species-level operational taxonomic units (OTUs) showed no significant response to sulfate. In contrast, low-abundance OTUs responded significantly to sulfate in incubations with propionate, lactate and butyrate. These OTUs included members of recognized sulfate-reducing taxa (Desulfosporosinus, Desulfopila, Desulfomonile, Desulfovibrio) and also members of taxa that are either yet unknown sulfate reducers or metabolic interaction partners thereof. Most responsive OTUs markedly increased their ribosome content but only weakly increased in abundance. Responsive Desulfosporosinus OTUs even maintained a constantly low population size throughout 50 days, which suggests a novel strategy of rare biosphere members to display activity. Interestingly, two OTUs of the non-sulfate-reducing genus Telmatospirillum (Alphaproteobacteria) showed strongly contrasting preferences towards sulfate in butyrate-amended microcosms, corroborating that closely related microorganisms are not necessarily ecologically coherent. We show that diverse consortia of low-abundance microorganisms can perform peat soil sulfate reduction, a process that exerts control on methane production in these climate-relevant ecosystems.

  • Diversity analysis of sulfite- and sulfate-reducing microorganisms by multiplex dsrA and dsrB amplicon sequencing using new primers and mock community-optimized bioinformatics.

    Pelikan C, Herbold CW, Hausmann B, Müller AL, Pester M, Loy A
    2016 - Environ. Microbiol., 9: 2994-3009

    Abstract: 

    Genes encoding dissimilatory sulfite reductase (DsrAB) are commonly used as diagnostic markers in ecological studies of sulfite- and sulfate-reducing microorganisms. Here, we developed new high-coverage primer sets for generation of reductive bacterial-type dsrA and dsrB polymerase chain reaction (PCR) products for highly parallel amplicon sequencing and a bioinformatics workflow for processing and taxonomic classification of short dsrA and dsrB reads. We employed two diverse mock communities that consisted of 45 or 90 known dsrAB sequences derived from environmental clones to precisely evaluate the performance of individual steps of our amplicon sequencing approach on the Illumina MiSeq platform. Although PCR cycle number, gene-specific primer mismatches and stringent filtering for high-quality sequences had notable effects on the observed dsrA and dsrB community structures, recovery of most mock community sequences was generally proportional to their relative input abundances. Successful dsrA and dsrB diversity analysis in selected environmental samples further proved that the multiplex amplicon sequencing approach is adequate for monitoring spatial distribution and temporal abundance dynamics of dsrAB-containing microorganisms. Although tested for reductive bacterial-type dsrAB, this method is readily applicable for oxidative-type dsrAB of sulfur-oxidizing bacteria and also provides guidance for processing short amplicon reads of other functional genes.

  • A flexible and economical barcoding approach for highly multiplexed amplicon sequencing of diverse target genes.

    Herbold CW, Pelikan C, Kuzyk O, Hausmann B, Angel R, Berry D, Loy A
    2015 - Front Microbiol, 731

    Abstract: 

    High throughput sequencing of phylogenetic and functional gene amplicons provides tremendous insight into the structure and functional potential of complex microbial communities. Here, we introduce a highly adaptable and economical PCR approach to barcoding and pooling libraries of numerous target genes. In this approach, we replace gene- and sequencing platform-specific fusion primers with general, interchangeable barcoding primers, enabling nearly limitless customized barcode-primer combinations. Compared to barcoding with long fusion primers, our multiple-target gene approach is more economical because it overall requires lower number of primers and is based on short primers with generally lower synthesis and purification costs. To highlight our approach, we pooled over 900 different small-subunit rRNA and functional gene amplicon libraries obtained from various environmental or host-associated microbial community samples into a single, paired-end Illumina MiSeq run. Although the amplicon regions ranged in size from approximately 290 to 720 bp, we found no significant systematic sequencing bias related to amplicon length or gene target. Our results indicate that this flexible multiplexing approach produces large, diverse, and high quality sets of amplicon sequence data for modern studies in microbial ecology.

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