Schleheck, David
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Anaerobic dissimilatory phosphite oxidation, an extremely efficient concept of microbial electron economy
Phosphite is a stable phosphorus compound that, together with phosphate, made up a substantial part of the total phosphorus content of the prebiotic Earth's crust. Oxidation of phosphite to phosphate releases electrons at an unusually low redox potential (−690 mV at pH 7.0). Numerous aerobic and anaerobic bacteria use phosphite as a phosphorus source and oxidise it to phosphate for synthesis of nucleotides and other phosphorus-containing cell constituents. Only two pure cultures of strictly anaerobic bacteria have been isolated so far that use phosphite as an electron donor in their energy metabolism, the Gram-positive Phosphitispora fastidiosa and the Gram-negative Desulfotignum phosphitoxidans. The key enzyme of this metabolism is an NAD+-dependent phosphite dehydrogenase enzyme that phosphorylates AMP to ADP. These phosphorylating phosphite dehydrogenases were found to be related to nucleoside diphosphate sugar epimerases. The produced NADH is channelled into autotrophic CO2 fixation via the Wood-Ljungdahl (CO-DH) pathway, thus allowing for nearly complete assimilation of the substrate electrons into bacterial biomass. This extremely efficient type of electron flow connects energy and carbon metabolism directly through NADH and might have been important in the early evolution of life when phosphite was easily available on Earth.
Postglacial evolution of Lake Constance: sedimentological and geochemical evidence from a deep-basin sediment core
The modern, over 250-m-deep basin of Lake Constance represents the underfilled northern part of an over 400-m-deep, glacially overdeepened trough, which reaches well into the Alps at its southern end. The overdeepening was formed by repeated glacial advance-retreat cycles of the Rhine Glacier throughout the Middle to Late Pleistocene. A seismic survey of Lake Constance revealed a Quaternary sediment fill of more than 150 m thickness representing at least the last glacial cycle. The stratified sedimentary fill consists at the base of ice-contact deposits on top of the molasse bedrock, overlain by glaciolacustrine to lacustrine sediments. During the successful field test of a newly developed, mid-size coring system ("HIPERCORIG"), the longest core (HIBO19) ever taken in Lake Constance was retrieved with an overall length of 24 m. The sediments recovered consist of a nearly continuous succession of lacustrine silts and sands including more than 12 m of Late Glacial sediment at the base. 14 lithotypes were identified through petrophysical and geochemical analyses. In combination with a 14C- and OSL-based age-depth model, the core was divided into three main chronostratigraphic units. The basal age of ~ 13.7 ka BP dates the base of the succession back to the Bølling-Allerød interstadial, with overlying strata representing a complete and thick Younger-Dryas to Holocene succession. The sediments offer a high-resolution insight into the evolution of paleo-Lake Constance from a cold, postglacial to a more productive and warmer Holocene lake. The Late Glacial succession is dominated by massive, m-thick sand beds reflecting episodic sedimentation pulses. They are most likely linked to a subaquatic channel system originating in the river Seefelder Aach, which is, despite the Holocene drape, still apparent in today’s lake bathymetry. The overlying Holocene succession reveals a prominent, several cm-thick, double-turbiditic event layer representing the most distal impact of the Flimser Bergsturz, the largest known rockslide of the Alps that occurred over 100 km upstream the river Rhine at ~ 9.5 ka BP. Furthermore, lithologic variations in the Holocene succession document the varying sediment loads of the river Rhine and the endogenic production representing a multitude of environmental changes.
Proteogenomic analysis of Georgfuchsia toluolica revealed unexpected concurrent aerobic and anaerobic toluene degradation
Denitrifying Betaproteobacteria play a key role in the anaerobic degradation of monoaromatic hydrocarbons. We performed a multi-omics study to better understand the metabolism of the representative organism Georgfuchsia toluolica strain G5G6 known as a strict anaerobe coupling toluene oxidation with dissimilatory nitrate and Fe(III) reduction. Despite the genomic potential for degradation of different carbon sources, we did not find sugar or organic acid transporters, in line with the inability of strain G5G6 to use these substrates. Using a proteomics analysis, we detected proteins of fumarate-dependent toluene activation, membrane-bound nitrate reductase, and key components of the metal-reducing (Mtr) pathway under both nitrate- and Fe(III)-reducing conditions. High abundance of the multiheme cytochrome MtrC implied that a porin-cytochrome complex was used for respiratory Fe(III) reduction. Remarkably, strain G5G6 contains a full set of genes for aerobic toluene degradation, and we detected enzymes of aerobic toluene degradation under both nitrate- and Fe(III)-reducing conditions. We further detected an ATP-dependent benzoyl-CoA reductase, reactive oxygen species detoxification proteins, and cytochrome c oxidase indicating a facultative anaerobic lifestyle of strain G5G6. Correspondingly, we found diffusion through the septa a substantial source of oxygen in the cultures enabling concurrent aerobic and anaerobic toluene degradation by strain G5G6.
Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut
Responses of the microbiota to diet are highly personalized but mechanistically not well understood because many metabolic capabilities and interactions of human gut microorganisms are unknown. Here we show that sulfoquinovose (SQ), a sulfonated monosaccharide omnipresent in green vegetables, is a selective yet relevant substrate for few but ubiquitous bacteria in the human gut. In human feces and in defined co-culture, Eubacterium rectale and Bilophila wadsworthia used recently identified pathways to cooperatively catabolize SQ with 2,3-dihydroxypropane-1-sulfonate as a transient intermediate to hydrogen sulfide (H2S), a key intestinal metabolite with disparate effects on host health. SQ-degradation capability is encoded in almost half of E. rectale genomes but otherwise sparsely distributed among microbial species in the human intestine. However, re-analysis of fecal metatranscriptome datasets of four human cohorts showed that SQ degradation (mostly from E. rectale and Faecalibacterium prausnitzii) and H2S production (mostly from B. wadsworthia) pathways were expressed abundantly across various health states, demonstrating that these microbial functions are core attributes of the human gut. The discovery of green-diet-derived SQ as an exclusive microbial nutrient and an additional source of H2S in the human gut highlights the role of individual dietary compounds and organosulfur metabolism on microbial activity and has implications for precision editing of the gut microbiota by dietary and prebiotic interventions.
Biodegradable Mineral Plastics
Mineral plastics are a promising class of bio-inspired materials that offer exceptional properties, like self-heal ability, stretchability in the hydrogel state, and high hardness, toughness, transparency, and non-flammability in the dry state along with reversible transformation into the hydrogel by addition of water. This enables easy reshape-ability and recycling like the solubility in mild acids to subsequently form mineral plastics again by base addition. However, current mineral plastics rely on petrochemistry, are hardly biodegradable, and thus persistent in nature. This work presents the next generation of mineral plastics, which are bio-based and biodegradable, making them a promising, new class of polymers for the development of environmentally friendly materials. Physically cross-linked (poly)glutamic-acid (PGlu)-based mineral plastics are synthesized using various alcohol-water mixtures, metal ion ratios and molecular weights. The rheological properties are easily adjusted using these parameters. The general procedure involves addition of equimolar solution of CaCl2 to PGlu in equal volumes followed by addition of iPrOH (iPrOH:H2O = 1:1) under vigorous stirring conditions. The ready biodegradability of PGlu/CaFe mineral plastic is confirmed in this study where the elements N, Ca, and Fe present in it tend to act as additional nutrients, supporting the growth of microorganisms and consequently, promoting the biodegradation process.
Vegetation changes over the last centuries in the Lower Lake Constance region reconstructed from sediment‐core environmental DNA
Many European lake ecosystems, including their respective catchment areas, underwent anthropogenic environmental changes over the last centuries. This has resulted in changes in the aquatic and terrestrial vegetation, but historical records on the composition of the past vegetation on centennial scale are scarce. In this study, we examined changes in the terrestrial and aquatic plant communities in and around Lower Lake Constance using metabarcoding of sedimentary DNA (sedDNA) of three cores from different sub-basins covering the past, up to 300 years. We successfully identified an average of c. 3000 sequence variants (molecular operational taxonomic units -MOTUs) and obtained a taxonomically annotated dataset of 127 species, 104 genera, and 72 families. We could detect major changes in the terrestrial and aquatic vegetation of the Lower Lake Constance region by examining the cores. For example, alpha diversity decreased in the last c. 100 years, and this decrease was more pronounced in the terrestrial than in the aquatic plant community. Unlike the terrestrial plant community, the current aquatic plant-community composition partially resembles the community from before the 20th-century eutrophication phase of the lake. In addition to changes that can be attributed to anthropogenic impacts, we also captured the effect of DNA sedimentation on the terrestrial DNA diversity representation in sediments during periods of extensive flooding and potentially as a consequence of extremely cold winters. With sedDNA from Lower Lake Constance, we provide a new local dataset to investigate and extend the historical changes of different shoreline habitats and to identify characteristic and invasive plant species. Such highly resolved datasets spanning the past centuries can provide detailed information on human environmental history in densely populated regions that have undergone severe changes in the recent past.
Phosphitispora fastidiosa gen. nov. sp. nov., a new dissimilatory phosphite-oxidizing anaerobic bacterium isolated from anaerobic sewage sludge
A new strictly anaerobic bacterium, strain DYL19T, was enriched and isolated with phosphite as the sole electron donor and CO2 as a single carbon source and electron acceptor from anaerobic sewage sludge sampled at a sewage treatment plant in Constance, Germany. It is a Gram-positive, spore-forming, slightly curved, rod-shaped bacterium which oxidizes phosphite to phosphate while reducing CO2 to biomass and small amounts of acetate. Optimal growth is observed at 30 °C, pH 7.2, with a doubling time of 3 days. Beyond phosphite, no further inorganic or organic electron donor can be used, and no other electron acceptor than CO2 is reduced. Sulphate inhibits growth with phosphite and CO2. The G+C content is 45.95 mol%, and dimethylmenaquinone-7 is the only quinone detectable in the cells. On the basis of 16S rRNA gene sequence analysis and other chemotaxonomic properties, strain DYL19T is described as the type strain of a new genus and species, Phosphitispora fastidiosa gen. nov., sp. nov.
Biodegradable High‐Density Polyethylene‐like Material
We report a novel polyester material generated from readily available biobased 1,18-octadecanedicarboxylic acid and ethylene glycol possesses a polyethylene-like solid-state structure and also tensile properties similar to high density polyethylene (HDPE). Despite its crystallinity, high melting point (Tm=96 °C) and hydrophobic nature, polyester-2,18 is subject to rapid and complete hydrolytic degradation in in vitro assays with isolated naturally occurring enzymes. Under industrial composting conditions (ISO standard 14855-1) the material is biodegraded with mineralization above 95 % within two months. Reference studies with polyester-18,18 (Tm=99 °C) reveal a strong impact of the nature of the diol repeating unit on degradation rates, possibly related to the density of ester groups in the amorphous phase. Depolymerization by methanolysis indicates suitability for closed-loop recycling.
Bacterial microcompartments for isethionate desulfonation in the taurine-degrading human-gut bacterium Bilophila wadsworthia
Background
Bilophila wadsworthia, a strictly anaerobic, sulfite-reducing bacterium and common member of the human gut microbiota, has been associated with diseases such as appendicitis and colitis. It is specialized on organosulfonate respiration for energy conservation, i.e., utilization of dietary and host-derived organosulfonates, such as taurine (2-aminoethansulfonate), as sulfite donors for sulfite respiration, producing hydrogen sulfide (H2S), an important intestinal metabolite that may have beneficial as well as detrimental effects on the colonic environment. Its taurine desulfonation pathway involves the glycyl radical enzyme (GRE) isethionate sulfite-lyase (IslAB), which cleaves isethionate (2-hydroxyethanesulfonate) into acetaldehyde and sulfite.
Results
We demonstrate that taurine metabolism in B. wadsworthia 3.1.6 involves bacterial microcompartments (BMCs). First, we confirmed taurine-inducible production of BMCs by proteomic, transcriptomic and ultra-thin sectioning and electron-microscopical analyses. Then, we isolated BMCs from taurine-grown cells by density-gradient ultracentrifugation and analyzed their composition by proteomics as well as by enzyme assays, which suggested that the GRE IslAB and acetaldehyde dehydrogenase are located inside of the BMCs. Finally, we are discussing the recycling of cofactors in the IslAB-BMCs and a potential shuttling of electrons across the BMC shell by a potential iron-sulfur (FeS) cluster-containing shell protein identified by sequence analysis.
Conclusions
We characterized a novel subclass of BMCs and broadened the spectrum of reactions known to take place enclosed in BMCs, which is of biotechnological interest. We also provided more details on the energy metabolism of the opportunistic pathobiont B. wadsworthia and on microbial H2S production in the human gut.
Is Toxin-Producing Planktothrix sp. an Emerging Species in Lake Constance?
Recurring blooms of filamentous, red-pigmented and toxin-producing cyanobacteria Planktothrix rubescens have been reported in numerous deep and stratified prealpine lakes, with the exception of Lake Constance. In a 2019 and 2020 Lake Constance field campaign, we collected samples from a distinct red-pigmented biomass maximum below the chlorophyll-a maximum, which was determined using fluorescence probe measurements at depths between 18 and 20 m. Here, we report the characterization of these deep water red pigment maxima (DRM) as cyanobacterial blooms. Using 16S rRNA gene-amplicon sequencing, we found evidence that the blooms were, indeed, contributed by Planktothrix spp., although phycoerythrin-rich Synechococcus taxa constituted most of the biomass (>96% relative read abundance) of the cyanobacterial DRM community. Through UPLC–MS/MS, we also detected toxic microcystins (MCs) in the DRM in the individual sampling days at concentrations of ≤1.5 ng/L. Subsequently, we reevaluated the fluorescence probe measurements collected over the past decade and found that, in the summer, DRM have been present in Lake Constance, at least since 2009. Our study highlights the need for a continuous monitoring program also targeting the cyanobacterial DRM in Lake Constance, and for future studies on the competition of the different cyanobacterial taxa. Future studies will address the potential community composition changes in response to the climate change driven physiochemical and biological parameters of the lake.