Publications

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Publications in peer reviewed journals

15 Publications found
  • Machine learning and phylogenetic analysis allow for predicting antibiotic resistance in M. tuberculosis

    Yurtseven A, Buyanova S, Agrawal AA, Bochkareva OO, Kalinina OV
    2023 - in press
  • The Fish Pathogen "Candidatus Clavichlamydia salmonicola"-A Missing Link in the Evolution of Chlamydial Pathogens of Humans.

    Collingro A, Köstlbacher S, Siegl A, Toenshoff ER, Schulz F, Mitchell SO, Weinmaier T, Rattei T, Colquhoun DJ, Horn M
    2023 - Genome Biol Evol, 8: in press

    Abstract: 

    Chlamydiae like Chlamydia trachomatis and Chlamydia psittaci are well-known human and animal pathogens. Yet, the chlamydiae are a much larger group of evolutionary ancient obligate intracellular bacteria that includes predominantly symbionts of protists and diverse animals. This makes them ideal model organisms to study evolutionary transitions from symbionts in microbial eukaryotes to pathogens of humans. To this end, comparative genome analysis has served as an important tool. Genome sequence data for many chlamydial lineages are, however, still lacking, hampering our understanding of their evolutionary history. Here, we determined the first high-quality draft genome sequence of the fish pathogen "Candidatus Clavichlamydia salmonicola", representing a separate genus within the human and animal pathogenic Chlamydiaceae. The "Ca. Clavichlamydia salmonicola" genome harbors genes that so far have been exclusively found in Chlamydia species suggesting that basic mechanisms important for the interaction with chordate hosts have evolved stepwise in the history of chlamydiae. Thus, the genome sequence of "Ca. Clavichlamydia salmonicola" allows to constrain candidate genes to further understand the evolution of chlamydial virulence mechanisms required to infect mammals.

  • Genome Dynamics and Temperature Adaptation During Experimental Evolution of Obligate Intracellular Bacteria.

    Herrera P, Schuster L, Zojer M, Na H, Schwarz J, Wascher F, Kempinger T, Regner A, Rattei T, Horn M
    2023 - Genome Biol Evol, 8: in press

    Abstract: 

    Evolution experiments with free-living microbes have radically improved our understanding of genome evolution and how microorganisms adapt. Yet there is a paucity of such research focusing on strictly host-associated bacteria, even though they are widespread in nature. Here, we used the Acanthamoeba symbiont Protochlamydia amoebophila, a distant relative of the human pathogen Chlamydia trachomatis and representative of a large group of protist-associated environmental chlamydiae, as a model to study how obligate intracellular symbionts evolve and adapt to elevated temperature, a prerequisite for the pivotal evolutionary leap from protist to endothermic animal hosts. We established 12 replicate populations under two temperatures (20 °C, 30 °C) for 510 bacterial generations (38 months). We then used infectivity assays and pooled whole-genome resequencing to identify any evolved phenotypes and the molecular basis of adaptation in these bacteria. We observed an overall reduction in infectivity of the symbionts evolved at 30 °C, and we identified numerous nonsynonymous mutations and small indels in these symbiont populations, with several variants persisting throughout multiple time points and reaching high frequencies. This suggests that many mutations may have been beneficial and played an adaptive role. Mutated genes within the same temperature regime were more similar than those between temperature regimes. Our results provide insights into the molecular evolution of intracellular bacteria under the constraints of strict host dependance and highly structured populations and suggest that for chlamydial symbionts of protists, temperature adaptation was facilitated through attenuation of symbiont infectivity as a tradeoff to reduce host cell burden.

  • A predicted CRISPR-mediated symbiosis between uncultivated archaea.

    Esser SP, Rahlff J, Zhao W, Predl M, Plewka J, Sures K, Wimmer F, Lee J, Adam PS, McGonigle J, Turzynski V, Banas I, Schwank K, Krupovic M, Bornemann TLV, Figueroa-Gonzalez PA, Jarett J, Rattei T, Amano Y, Blaby IK, Cheng JF, Brazelton WJ, Beisel CL, Woyke T, Zhang Y, Probst AJ
    2023 - Nat Microbiol, 9: 1619-1633

    Abstract: 

    CRISPR-Cas systems defend prokaryotic cells from invasive DNA of viruses, plasmids and other mobile genetic elements. Here, we show using metagenomics, metatranscriptomics and single-cell genomics that CRISPR systems of widespread, uncultivated archaea can also target chromosomal DNA of archaeal episymbionts of the DPANN superphylum. Using meta-omics datasets from Crystal Geyser and Horonobe Underground Research Laboratory, we find that CRISPR spacers of the hosts Candidatus Altiarchaeum crystalense and Ca. A. horonobense, respectively, match putative essential genes in their episymbionts' genomes of the genus Ca. Huberiarchaeum and that some of these spacers are expressed in situ. Metabolic interaction modelling also reveals complementation between host-episymbiont systems, on the basis of which we propose that episymbionts are either parasitic or mutualistic depending on the genotype of the host. By expanding our analysis to 7,012 archaeal genomes, we suggest that CRISPR-Cas targeting of genomes associated with symbiotic archaea evolved independently in various archaeal lineages.

  • Food systems microbiome-related educational needs.

    Olmo R, Wetzels SU, Berg G, Cocolin L, Hartmann M, Hugas M, Kostic T, Rattei T, Ruthsatz M, Rybakova D, Sessitsch A, Shortt C, Timmis K, Selberherr E, Wagner M
    2023 - Microb Biotechnol, 7: 1412-1422

    Abstract: 

    Within the European-funded Coordination and Support Action MicrobiomeSupport (https://www.microbiomesupport.eu/), the Workshop 'Education in Food Systems Microbiome Related Sciences: Needs for Universities, Industry and Public Health Systems' brought together over 70 researchers, public health and industry partners from all over the world to work on elaborating microbiome-related educational needs in food systems. This publication provides a summary of discussions held during and after the workshop and the resulting recommendations.

  • Antiviral immune response reveals host-specific virus infections in natural ant populations.

    Viljakainen L, Fürst MA, Grasse AV, Jurvansuu J, Oh J, Tolonen L, Eder T, Rattei T, Cremer S
    2023 - Front Microbiol, 1119002

    Abstract: 

    Hosts can carry many viruses in their bodies, but not all of them cause disease. We studied ants as a social host to determine both their overall viral repertoire and the subset of actively infecting viruses across natural populations of three subfamilies: the Argentine ant (, Dolichoderinae), the invasive garden ant (, Formicinae) and the red ant (, Myrmicinae). We used a dual sequencing strategy to reconstruct complete virus genomes by RNA-seq and to simultaneously determine the small interfering RNAs (siRNAs) by small RNA sequencing (sRNA-seq), which constitute the host antiviral RNAi immune response. This approach led to the discovery of 41 novel viruses in ants and revealed a host ant-specific RNAi response (21 vs. 22 nt siRNAs) in the different ant species. The efficiency of the RNAi response (sRNA/RNA read count ratio) depended on the virus and the respective ant species, but not its population. Overall, we found the highest virus abundance and diversity per population in , followed by and . Argentine ants also shared a high proportion of viruses between populations, whilst overlap was nearly absent in . Only one of the 59 viruses was found to infect two of the ant species as hosts, revealing high host-specificity in active infections. In contrast, six viruses actively infected one ant species, but were found as contaminants only in the others. Disentangling spillover of disease-causing infection from non-infecting contamination across species is providing relevant information for disease ecology and ecosystem management.

  • Metagenomic Antimicrobial Susceptibility Testing from Simulated Native Patient Samples.

    Lüftinger L, Májek P, Rattei T, Beisken S
    2023 - Antibiotics (Basel), 2: in press

    Abstract: 

    Genomic antimicrobial susceptibility testing (AST) has been shown to be accurate for many pathogens and antimicrobials. However, these methods have not been systematically evaluated for clinical metagenomic data. We investigate the performance of in-silico AST from clinical metagenomes (MG-AST). Using isolate sequencing data from a multi-center study on antimicrobial resistance (AMR) as well as shotgun-sequenced septic urine samples, we simulate over 2000 complicated urinary tract infection (cUTI) metagenomes with known resistance phenotype to 5 antimicrobials. Applying rule-based and machine learning-based genomic AST classifiers, we explore the impact of sequencing depth and technology, metagenome complexity, and bioinformatics processing approaches on AST accuracy. By using an optimized metagenomics assembly and binning workflow, MG-AST achieved balanced accuracy within 5.1% of isolate-derived genomic AST. For poly-microbial infections, taxonomic sample complexity and relatedness of taxa in the sample is a key factor influencing metagenomic binning and downstream MG-AST accuracy. We show that the reassignment of putative plasmid contigs by their predicted host range and investigation of whole resistome capabilities improved MG-AST performance on poly-microbial samples. We further demonstrate that machine learning-based methods enable MG-AST with superior accuracy compared to rule-based approaches on simulated native patient samples.

  • Extending and improving metagenomic taxonomic profiling with uncharacterized species using MetaPhlAn 4.

    Blanco-Míguez A, Beghini F, Cumbo F, McIver LJ, Thompson KN, Zolfo M, Manghi P, Dubois L, Huang KD, Thomas AM, Nickols WA, Piccinno G, Piperni E, Punčochář M, Valles-Colomer M, Tett A, Giordano F, Davies R, Wolf J, Berry SE, Spector TD, Franzosa EA, Pasolli E, Asnicar F, Huttenhower C, Segata N
    2023 - Nat Biotechnol, in press

    Abstract: 

    Metagenomic assembly enables new organism discovery from microbial communities, but it can only capture few abundant organisms from most metagenomes. Here we present MetaPhlAn 4, which integrates information from metagenome assemblies and microbial isolate genomes for more comprehensive metagenomic taxonomic profiling. From a curated collection of 1.01 M prokaryotic reference and metagenome-assembled genomes, we define unique marker genes for 26,970 species-level genome bins, 4,992 of them taxonomically unidentified at the species level. MetaPhlAn 4 explains ~20% more reads in most international human gut microbiomes and >40% in less-characterized environments such as the rumen microbiome and proves more accurate than available alternatives on synthetic evaluations while also reliably quantifying organisms with no cultured isolates. Application of the method to >24,500 metagenomes highlights previously undetected species to be strong biomarkers for host conditions and lifestyles in human and mouse microbiomes and shows that even previously uncharacterized species can be genetically profiled at the resolution of single microbial strains.

  • One to host them all: genomics of the diverse bacterial endosymbionts of the spider .

    Halter T, Köstlbacher S, Rattei T, Hendrickx F, Manzano-Marín A, Horn M
    2023 - Microb Genom, 2: in press

    Abstract: 

    Bacterial endosymbionts of the groups , and are well known for their diverse effects on their arthropod hosts, ranging from mutualistic relationships to reproductive phenotypes. Here, we analysed a unique system in which the dwarf spider is co-infected with up to five different endosymbionts affiliated with , ' Tisiphia' (formerly Torix group ), and . Using short-read genome sequencing data, we show that the endosymbionts are heterogeneously distributed among populations and are frequently found co-infecting spider individuals. To study this intricate host-endosymbiont system on a genome-resolved level, we used long-read sequencing to reconstruct closed genomes of the , '. Tisiphia' and endosymbionts. We provide insights into the ecology and evolution of the endosymbionts and shed light on the interactions with their spider host. We detected high quantities of transposable elements in all endosymbiont genomes and provide evidence that ancestors of the , '. Tisiphia' and endosymbionts have co-infected the same hosts in the past. Our findings contribute to broadening our knowledge about endosymbionts infecting one of the largest animal phyla on Earth and show the usefulness of transposable elements as an evolutionary 'contact-tracing' tool.

  • Secondary Metabolite Production Potential in a Microbiome of the Freshwater Sponge Spongilla lacustris.

    Graffius S, Garzón JFG, Zehl M, Pjevac P, Kirkegaard R, Flieder M, Loy A, Rattei T, Ostrovsky A, Zotchev SB
    2023 - Microbiol Spectr, e0435322

    Abstract: 

    Marine and freshwater sponges harbor diverse communities of bacteria with vast potential to produce secondary metabolites that may play an important role in protecting the host from predators and infections. In this work, we initially used cultivation and metagenomics to investigate the microbial community of the freshwater sponge Spongilla lacustris collected in an Austrian lake. Representatives of 41 bacterial genera were isolated from the sponge sample and classified according to their 16S rRNA gene sequences. The genomes of 33 representative isolates and the 20 recovered metagenome-assembled genomes (MAGs) contained in total 306 secondary metabolite biosynthesis gene clusters (BGCs). Comparative 16S rRNA gene and genome analyses showed very little taxon overlap between the recovered isolates and the sponge community as revealed by cultivation-independent methods. Both culture-independent and -dependent analyses suggested high biosynthetic potential of the S. lacustris microbiome, which was confirmed experimentally even at the subspecies level for two isolates. To our knowledge, this is the most thorough description of the secondary metabolite production potential of a freshwater sponge microbiome to date. A large body of research is dedicated to marine sponges, filter-feeding animals harboring rich bacterial microbiomes believed to play an important role in protecting the host from predators and infections. Freshwater sponges have received so far much less attention with respect to their microbiomes, members of which may produce bioactive secondary metabolites with potential to be developed into drugs to treat a variety of diseases. In this work, we investigated the potential of bacteria associated with the freshwater sponge to biosynthesize diverse secondary metabolites. Using culture-dependent and -independent methods, we discovered over 300 biosynthetic gene clusters in sponge-associated bacteria and proved production of several compounds by selected isolates using genome mining. Our results illustrate the importance of a complex approach when dealing with microbiomes of multicellular organisms that may contain producers of medically important secondary metabolites.

  • Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies.

    Kennedy KM, de Goffau MC, Perez-Muñoz ME, Arrieta MC, Bäckhed F, Bork P, Braun T, Bushman FD, Dore J, de Vos WM, Earl AM, Eisen JA, Elovitz MA, Ganal-Vonarburg SC, Gänzle MG, Garrett WS, Hall LJ, Hornef MW, Huttenhower C, Konnikova L, Lebeer S, Macpherson AJ, Massey RC, McHardy AC, Koren O, Lawley TD, Ley RE, O'Mahony L, O'Toole PW, Pamer EG, Parkhill J, Raes J, Rattei T, Salonen A, Segal E, Segata N, Shanahan F, Sloboda DM, Smith GCS, Sokol H, Spector TD, Surette MG, Tannock GW, Walker AW, Yassour M, Walter J
    2023 - Nature, 7945: 639-649

    Abstract: 

    Whether the human fetus and the prenatal intrauterine environment (amniotic fluid and placenta) are stably colonized by microbial communities in a healthy pregnancy remains a subject of debate. Here we evaluate recent studies that characterized microbial populations in human fetuses from the perspectives of reproductive biology, microbial ecology, bioinformatics, immunology, clinical microbiology and gnotobiology, and assess possible mechanisms by which the fetus might interact with microorganisms. Our analysis indicates that the detected microbial signals are likely the result of contamination during the clinical procedures to obtain fetal samples or during DNA extraction and DNA sequencing. Furthermore, the existence of live and replicating microbial populations in healthy fetal tissues is not compatible with fundamental concepts of immunology, clinical microbiology and the derivation of germ-free mammals. These conclusions are important to our understanding of human immune development and illustrate common pitfalls in the microbial analyses of many other low-biomass environments. The pursuit of a fetal microbiome serves as a cautionary example of the challenges of sequence-based microbiome studies when biomass is low or absent, and emphasizes the need for a trans-disciplinary approach that goes beyond contamination controls by also incorporating biological, ecological and mechanistic concepts.

  • The person-to-person transmission landscape of the gut and oral microbiomes.

    Valles-Colomer M, Blanco-Míguez A, Manghi P, Asnicar F, Dubois L, Golzato D, Armanini F, Cumbo F, Huang KD, Manara S, Masetti G, Pinto F, Piperni E, Punčochář M, Ricci L, Zolfo M, Farrant O, Goncalves A, Selma-Royo M, Binetti AG, Becerra JE, Han B, Lusingu J, Amuasi J, Amoroso L, Visconti A, Steves CM, Falchi M, Filosi M, Tett A, Last A, Xu Q, Qin N, Qin H, May J, Eibach D, Corrias MV, Ponzoni M, Pasolli E, Spector TD, Domenici E, Collado MC, Segata N
    2023 - Nature, 7946: 125-135

    Abstract: 

    The human microbiome is an integral component of the human body and a co-determinant of several health conditions. However, the extent to which interpersonal relations shape the individual genetic makeup of the microbiome and its transmission within and across populations remains largely unknown. Here, capitalizing on more than 9,700 human metagenomes and computational strain-level profiling, we detected extensive bacterial strain sharing across individuals (more than 10 million instances) with distinct mother-to-infant, intra-household and intra-population transmission patterns. Mother-to-infant gut microbiome transmission was considerable and stable during infancy (around 50% of the same strains among shared species (strain-sharing rate)) and remained detectable at older ages. By contrast, the transmission of the oral microbiome occurred largely horizontally and was enhanced by the duration of cohabitation. There was substantial strain sharing among cohabiting individuals, with 12% and 32% median strain-sharing rates for the gut and oral microbiomes, and time since cohabitation affected strain sharing more than age or genetics did. Bacterial strain sharing additionally recapitulated host population structures better than species-level profiles did. Finally, distinct taxa appeared as efficient spreaders across transmission modes and were associated with different predicted bacterial phenotypes linked with out-of-host survival capabilities. The extent of microorganism transmission that we describe underscores its relevance in human microbiome studies, especially those on non-infectious, microbiome-associated diseases.

  • Thermal acclimation of methanotrophs from the genus Methylobacter.

    Tveit AT, Söllinger A, Rainer EM, Didriksen A, Hestnes AG, Motleleng L, Hellinger HJ, Rattei T, Svenning MM
    2023 - ISME J, 4: 502-513

    Abstract: 

    Methanotrophs oxidize most of the methane (CH) produced in natural and anthropogenic ecosystems. Often living close to soil surfaces, these microorganisms must frequently adjust to temperature change. While many environmental studies have addressed temperature effects on CH oxidation and methanotrophic communities, there is little knowledge about the physiological adjustments that underlie these effects. We have studied thermal acclimation in Methylobacter, a widespread, abundant, and environmentally important methanotrophic genus. Comparisons of growth and CH oxidation kinetics at different temperatures in three members of the genus demonstrate that temperature has a strong influence on how much CH is consumed to support growth at different CH concentrations. However, the temperature effect varies considerably between species, suggesting that how a methanotrophic community is composed influences the temperature effect on CH uptake. To understand thermal acclimation mechanisms widely we carried out a transcriptomics experiment with Methylobacter tundripaludum SV96. We observed, at different temperatures, how varying abundances of transcripts for glycogen and protein biosynthesis relate to cellular glycogen and ribosome concentrations. Our data also demonstrated transcriptional adjustment of CH oxidation, oxidative phosphorylation, membrane fatty acid saturation, cell wall composition, and exopolysaccharides between temperatures. In addition, we observed differences in M. tundripaludum SV96 cell sizes at different temperatures. We conclude that thermal acclimation in Methylobacter results from transcriptional adjustment of central metabolism, protein biosynthesis, cell walls and storage. Acclimation leads to large shifts in CH consumption and growth efficiency, but with major differences between species. Thus, our study demonstrates that physiological adjustments to temperature change can substantially influence environmental CH uptake rates and that consideration of methanotroph physiology might be vital for accurate predictions of warming effects on CH emissions.

  • Cytoscape stringApp 2.0: Analysis and Visualization of Heterogeneous Biological Networks.

    Doncheva NT, Morris JH, Holze H, Kirsch R, Nastou KC, Cuesta-Astroz Y, Rattei T, Szklarczyk D, von Mering C, Jensen LJ
    2023 - J Proteome Res, 2: 637-646

    Abstract: 

    Biological networks are often used to represent complex biological systems, which can contain several types of entities. Analysis and visualization of such networks is supported by the Cytoscape software tool and its many apps. While earlier versions of stringApp focused on providing intraspecies protein-protein interactions from the STRING database, the new stringApp 2.0 greatly improves the support for heterogeneous networks. Here, we highlight new functionality that makes it possible to create networks that contain proteins and interactions from STRING as well as other biological entities and associations from other sources. We exemplify this by complementing a published SARS-CoV-2 interactome with interactions from STRING. We have also extended stringApp with new data and query functionality for protein-protein interactions between eukaryotic parasites and their hosts. We show how this can be used to retrieve and visualize a cross-species network for a malaria parasite, its host, and its vector. Finally, the latest stringApp version has an improved user interface, allows retrieval of both functional associations and physical interactions, and supports group-wise enrichment analysis of different parts of a network to aid biological interpretation. stringApp is freely available at https://apps.cytoscape.org/apps/stringapp.

  • eggNOG 6.0: enabling comparative genomics across 12 535 organisms.

    Hernández-Plaza A, Szklarczyk D, Botas J, Cantalapiedra CP, Giner-Lamia J, Mende DR, Kirsch R, Rattei T, Letunic I, Jensen LJ, Bork P, von Mering C, Huerta-Cepas J
    2023 - Nucleic Acids Res, 1: D389-D394

    Abstract: 

    The eggNOG (evolutionary gene genealogy Non-supervised Orthologous Groups) database is a bioinformatics resource providing orthology data and comprehensive functional information for organisms from all domains of life. Here, we present a major update of the database and website (version 6.0), which increases the number of covered organisms to 12 535 reference species, expands functional annotations, and implements new functionality. In total, eggNOG 6.0 provides a hierarchy of over 17M orthologous groups (OGs) computed at 1601 taxonomic levels, spanning 10 756 bacterial, 457 archaeal and 1322 eukaryotic organisms. OGs have been thoroughly annotated using recent knowledge from functional databases, including KEGG, Gene Ontology, UniProtKB, BiGG, CAZy, CARD, PFAM and SMART. eggNOG also offers phylogenetic trees for all OGs, maximising utility and versatility for end users while allowing researchers to investigate the evolutionary history of speciation and duplication events as well as the phylogenetic distribution of functional terms within each OG. Furthermore, the eggNOG 6.0 website contains new functionality to mine orthology and functional data with ease, including the possibility of generating phylogenetic profiles for multiple OGs across species or identifying single-copy OGs at custom taxonomic levels. eggNOG 6.0 is available at http://eggnog6.embl.de.

Book chapters and other publications

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