Biology subjects

Esser, S. P.

Publications and source records attributed to Esser, S. P..

10 recordsLinked to original sources

bioRxiv2023

Metaproteogenomics resolution of a high-CO2 aquifer community suggests an active symbiotic lifestyle of groundwater Gracilibacteria

BackgroundBacteria of the Candidate Phyla Radiation (CPR), constituting about 25% of the bacterial biodiversity, are characterized by small cell size and patchy genomes without complete key metabolic pathways, suggesting a symbiotic lifestyle. Gracilibacteria (BD1-5), which are part of the CPR branch, possess alternate coded genomes and have not yet been cultivated. However, besides genomic evidence, little is known about the lifestyle of Gracilibacteria, their temporal dynamics, and activity in natural ecosystems, particularly in groundwater, where they were initially been genomically resolved. Therefore, we here aimed to investigate Gracilibacteria activity in situ and to discern expressed genes involved in their lifestyle, using the metaproteogenome of Gracilibacteria as a function of time in the cold-water geyser Wallender Born in the Volcanic Eifel region in Germany. ResultsWe coupled genome-resolved metagenomics and metaproteomics to investigate a cold-water geyser microbial community enriched in Gracilibacteria across a 12-day time-series. Groundwater was collected and sequentially filtered to fraction CPR and other bacteria. Based on 670 Gbps of metagenomic data, 1129 different ribosomal protein S3 marker genes and 751 high-quality genomes (123 population genomes after dereplication), we identified dominant bacteria belonging to Galionellales and Gracilibacteria along with keystone microbes, which were low in genomic abundance but substantially contributing to proteomic abundance. Seven high-quality Gracilibacteria genomes showed typical limitations, such as limited amino acid or nucleotide synthesis, in their central metabolism but no co-occurrence with potential hosts. The genomes of these Gracilibacteria encoded for a high number of proteins related to a symbiotic or even predatory lifestyle, e.g., type IV and type II secretion system subunits and features related to cell-cell interactions and cell motility, which were also detected on protein level. ConclusionsCoupling metagenomics to metaproteomics enabled us to identify microbial keystone taxa in a high-CO2 aquifer, and to reveal microbial dynamics of Gracilibacteria. We posit that Gracilibacteria might be successful microbial predators in this ecosystem, potentially aiding in population control of this highly perturbed microbial geyser community from the deep biosphere.

ecology↗

bioRxiv2023

Differential expression of core metabolic functions in Candidatus Altiarchaeum inhabiting distinct subsurface ecosystems

Candidatus Altiarchaea are widespread across aquatic subsurface ecosystems and possess a highly conserved core genome, yet adaptations of this core genome to different biotic and abiotic factors based on gene expression remain unknown. Here, we investigated the metatranscriptome of two Ca. Altiarchaeum populations that thrive in two substantially different subsurface ecosystems. In Crystal Geyser, a high-CO2 groundwater system in the USA, Ca. Altiarchaeum crystalense co-occurs with the symbiont Ca. Huberiarchaeum crystalense, while in the Muehlbacher sulfidic spring in Germany, an artesian spring high in sulfide concentration, Ca. A. hamiconexum is heavily infected with viruses. We here mapped metatranscriptome reads against their genomes to analyze the in situ expression profile of their core genomes. Out of 537 shared gene clusters, 331 were functionally annotated and 130 differed significantly in expression between the two sites. Main differences were related to genes involved in cell defense like CRISPR-Cas, virus defense, replication, and transcription as well as energy and carbon metabolism. Our results demonstrate that altiarchaeal populations in the subsurface are likely adapted to their environment while influenced by other biological entities that tamper with their core metabolism. We consequently posit that viruses and symbiotic interactions can be major energy sinks for organisms in the deep biosphere. (Originality-Significance StatementOrganisms of the uncultivated phylum Ca. Altiarchaeota are globally widespread and fulfill essential roles in carbon cycling, e.g., carbon fixation in the continental subsurface. Here, we show that the transcriptional activity of organisms in the continental subsurface differ significantly depending on the geological and microbial setting of the ecosystem explaining many of the previously observed physiological traits of this organism group.)

microbiology↗

bioRxiv2023

Virus-host dynamics in archaeal groundwater biofilms and the associated bacterial community composition

Lytic viruses can be prevalent in deep groundwater, yet their spatial and temporal distribution in such an ecosystem remains unexplored. Here, we tackle this gap of knowledge by studying viral infections in individual, archaea-dominated biofilm flocks sampled from deep anoxic groundwater over a period of three years. Using virusFISH whose detection efficiency for individual viral particles was 15%, we show a significant and steady increase of virus infections between the years 2019 and 2022. Based on various fluorescence micrographs of individual biofilm flocks, we determined different stages of viral infections in biofilms for single sampling events, demonstrating the progression of infection of biofilms in deep groundwater. Biofilms associated with many host cells undergoing lysis showed a substantial accumulation of filamentous microbes around infected cells probably feeding off host cell debris. Using 16S rRNA gene sequencing across ten individual biofilm flocks from one sampling event, we determined that the associated bacterial community remains relatively constant and was dominated by Desulfobacterota. Given the stability of the virus-host interaction in these deep groundwater samples, we postulate that the virus-host dynamics of Ca. Altiarchaeum hamiconexum and its abundant virus Altivir_l_MSI described herein represent a suitable model system for studying deep biosphere virus-host interactions in future research endeavors.

microbiology↗

bioRxiv2023

Co-evolutionary patterns shown in Ostreococcus-virus system from the Western Baltic Sea in freshly isolated hosts and viruses.

Marine viruses are a major driver of phytoplankton mortality and thereby influence biogeochemical cycling of carbon and other nutrients. In recent years, an understanding of the potential importance of phytoplankton-targeting viruses on ecosystem dynamics has emerged, but experimental investigations of host-virus interactions on a broad spatial and temporal scale are still missing. Here, we investigated in detail a phytoplankton hosts responses reacting to infections by species-specific viruses from i) distinct geographical regions and ii) different sampling seasons. Specifically, we used two species of picophytoplankton (1 {micro}m) Ostreococcus tauri and O. mediterraneus and their viruses (size ca. 100 nm), which represent systems well-known in marine biology, but almost entirely ignored in evolutionary biology. The strains stem from different regions of the Southwestern Baltic Sea that vary in salinity and temperature. Using an experimental cross-infection set-up, we show that in this natural system evolutionary history, and thus the timing of when hosts and their associated viruses coexisted, was the main driver of infection patterns. In addition species and strain specificity underline the present understanding of rapid host-virus co-evolution.

microbiology↗

bioRxiv2022

Environmental activity-based protein profiling for function-driven enzyme discovery from natural communities

Microbial communities are significant drivers of global biogeochemical cycles, yet accurate function prediction of their proteome and discerning their activity in situ for bioprospecting remains challenging. Here, we present environmental activity-based protein profiling (eABPP) as a novel proteomics-based approach bridging the gap between environmental genomics, correct function annotation and in situ enzyme activity. As a showcase, we report the successful identification of active thermostable serine hydrolases by combining genome-resolved metagenomics and mass spectrometry-based eABPP of natural microbial communities from two independent hot springs in Kamchatka, Russia. eABPP does not only advance current methodological approaches by providing evidence for enzyme and microbial activity in situ but also represents an alternative approach to sequence homology-guided biocatalyst discovery from environmental ecosystems.

biochemistry↗

bioRxiv2022

Heads in the clouds: marine viruses disperse bidirectionally along the natural water cycle

Marine viruses have thoroughly been studied in seawater, yet their dispersal from neuston ecosystems at the air-sea interface towards the atmosphere remains a knowledge gap. Here, we show that 6.2 % of the studied virus population were shared between air-sea interface ecosystems and rainwater. Virus enrichment in the 1-mm thin surface microlayer and sea foams happened selectively, and variant analysis proved virus transfer to aerosols and rain. Viruses detected in rain and aerosols showed a significantly higher percent G/C base content compared to marine viruses, and a genetically distinct rain virome supports that those viruses could inhabit higher air masses. CRISPR spacer matches of marine prokaryotes to "foreign" viruses from rainwater prove regular virus-host encounters at the air-sea interface. Our findings on aerosolization and long-range atmospheric dispersal implicate virus-mediated carbon turnover in remote areas, viral dispersal mechanisms relevant to human health, and involvement of viruses in atmospheric processes like ice-nucleation.

microbiology↗

bioRxiv2021

Label-free Raman microspectroscopy for identifying virocells

Raman microspectroscopy has been thoroughly used to assess growth dynamics and heterogeneity of prokaryotic cells. Yet, little is known about how the chemistry of individual cells changes during infection with lytic viruses, resulting in so-called virocells. Here, we investigate biochemical changes of bacterial and archaeal cells of three different species in laboratory cultures before and after addition of their respective viruses using single-cell Raman microspectroscopy. By applying multivariate statistics, we identified significant differences in the spectra of single cells and cells after addition of lytic phage (phi6) for Pseudomonas syringae. A general ratio of wavenumbers that contributed the greatest differences in the recorded spectra was defined as an indicator for virocells. Based on reference spectra, this difference is likely attributable to an increase in nucleic acid vs. protein ratio of virocells. This method proved also successful for identification of Bacillus subtilis cells infected with phi29 displaying a decrease in respective ratio but failed for archaeal virocells (Methanosarcina mazei with Methanosarcina Spherical Virus) due to autofluorescence. Multivariate and univariate analyses suggest that Raman spectral data of infected cells can also be used to explore the complex biology behind viral infections of bacteria. Using this method, we confirmed the previously described two-stage infection of P. syringaes phi6 and that infection of B. subtilis by phi29 results in a stress response within single cells. We conclude that Raman microspectroscopy is a promising tool for chemical identification of Gram-positive and Gram-negative virocells undergoing infection with lytic DNA or RNA viruses. ImportanceViruses are highly diverse biological entities shaping many ecosystems across Earth. Yet, understanding the infection of individual microbial cells and the related biochemical changes remains limited. Using Raman microspectroscopy in conjunction with univariate and unsupervised machine learning approaches, we established a marker for identification of infected Gram-positive and Gram-negative bacteria. This non-destructive, label-free analytical method at single-cell resolution paves the way for future studies geared towards analyzing complex biological changes of virus-infected cells in pure culture and natural ecosystems.

microbiology↗

bioRxiv2021

Virus-associated organosulfur metabolism in human and environmental systems

Viruses influence the fate of nutrients and human health by killing microorganisms and altering metabolic processes. Organosulfur metabolism and biologically-derived hydrogen sulfide play dynamic roles in manifestation of diseases, infrastructure degradation, and essential biological processes. While microbial organosulfur metabolism is well-studied, the role of viruses in organosulfur metabolism is unknown. Here we report the discovery of 39 gene families involved in organosulfur metabolism encoded by 3,749 viruses from diverse ecosystems, including human microbiomes. The viruses infect organisms from all three domains of life. Six gene families encode for enzymes that degrade organosulfur compounds into sulfide, while others manipulate organosulfur compounds and may influence sulfide production. We show that viral metabolic genes encode key enzymatic domains, are translated into protein, are maintained after recombination, and that sulfide provides a fitness advantage to viruses. Our results reveal viruses as drivers of organosulfur metabolism with important implications for human and environmental health.

microbiology↗

bioRxiv2020

Genome-informed microscopy reveals infections of uncultivated carbon-fixing archaea by lytic viruses in Earth's crust

The continental subsurface houses a major portion of lifes abundance and diversity, yet little is known about viruses infecting microbes that reside there. Here, we used a combination of metagenomics and genome-informed microscopy to show that highly abundant carbon-fixing organisms of the uncultivated genus Candidatus Altiarchaeum are frequent targets of previously unrecognized viruses in the deep subsurface. Analysis of CRISPR spacer matches displayed resistances of Ca. Altiarchaea against eight predicted viral clades, which showed genomic relatedness across continents but little similarity to previously identified viruses. Based on metagenomic information, we tagged and imaged a putatively viral genome rich in protospacers using fluorescence microscopy. Virus-targeted genomeFISH revealed a lytic lifestyle of the respective virus and challenges previous predictions that lysogeny prevails as the dominant viral lifestyle in the subsurface. CRISPR development over time and imaging of 18 samples from one subsurface ecosystem suggest a sophisticated interplay of viral diversification and adapting CRISPR-mediated resistances of Ca. Altiarchaeum. We conclude that infections of primary producers with lytic viruses followed by cell lysis potentially jump-start heterotrophic carbon cycling in these subsurface ecosystems.

microbiology↗

bioRxiv2020

uBin - a manual refining tool for metagenomic bins designed for educational purposes

Resolving bacterial and archaeal genomes from metagenomes has revolutionized our understanding of Earths biomes, yet producing high quality genomes from assembled fragments has been an ever-standing problem. While automated binning software and their combination produce prokaryotic bins in high-throughput, their manual refinement has been slow and sometimes difficult. Here, we present uBin, a GUI-based, standalone bin refiner that runs on all major operating platforms and was specifically designed for educational purposes. When applied to the public CAMI dataset, refinement of bins was able to improve 78.9% of bins by decreasing their contamination. We also applied the bin refiner as a standalone binner to public metagenomes from the International Space Station and demonstrate the recovery of near-complete genomes, whose replication indices indicate active proliferation of microbes in Earths lower orbit. uBin is an easy to install software for bin refinement, binning of simple metagenomes and communication of metagenomic results to other scientists and in classrooms. The software is open source and available under https://github.com/ProbstLab/uBin.

genomics↗