Biology subjects

Thamdrup, B.

Publications and source records attributed to Thamdrup, B..

10 recordsLinked to original sources

bioRxiv2025

Beyond magnetosomes: ubiquitous and diverse intracellular inclusions expand the role of magnetotactic bacteria in biogeochemical cycling

Magnetotactic bacteria (MTB) are capable of accumulating and storing intercellular pools containing phosphorus, sulfur, nitrogen and carbon. Yet, the metabolic pathways connected with their intracellular storage of polyphosphate, elemental sulfur, nitrate, and calcium carbonate, and the environmental influence on MTB inclusions and their quantitative contribution to sedimentary chemical budgets remain underexplored. Using a combination of chemical characterization, ultrastructural and compositional analyses, and phylogenetic and genomic insights into microbial assemblages, we investigated the influence of geochemical parameters on the diversity, ecophysiology, and distribution of MTB in freshwater and brackish sediments. Special focus is given to intracellular inclusions and their metabolic pathways to uncover functional traits and ecological roles in elemental cycling. Of the 118 examined MTB cells, polyphosphate granules (75%) and nitrate-containing vacuoles (67%) were the most common inclusions followed by sulfur globules (25%) and calcium carbonate granules (8%). The intracellular phosphorus, nitrogen, and sulfur stored in MTB cells were conservatively estimated to account for 0.60%, 0.91%, and 0.23% of the total sedimentary P, N, and S in the investigated freshwater sediments, respectively. The ubiquitous nature and important ecological role of MTB can be explained by their ability to sequester chemical elements into intracellular inclusions, giving them a metabolic advantage in dynamic chemically stratified environments. The extraordinary phylogenetic diversity of MTB, coupled with their capability to hyperaccumulate and store a wide range of elements and compounds, represents a significant resource for biotechnology innovation.

microbiology↗

bioRxiv2023

Differential contribution of nitrifying prokaryotes to nitrification in groundwater

The ecophysiology of complete ammonia-oxidizing bacteria (CMX) of the genus Nitrospira and their widespread occurrence in groundwater suggests that CMX bacteria have a competitive advantage over ammonia-oxidizing bacteria (AOB) and archaea (AOA) in these environments. However, the specific contribution of their activity to nitrification processes has remained unclear. We aimed to disentangle the contribution of CMX, AOA and AOB to nitrification and to identify the environmental drivers of their niche differentiation at different levels of ammonium and oxygen in oligotrophic carbonate rock aquifers. CMX amoA genes accounted on average for 16 to 75% of the total groundwater amoA genes detected. Nitrification rates were positively correlated to CMX clade A associated phylotypes and AOB affiliated with Nitrosomonas ureae. Short-term incubations amended with the nitrification inhibitors allylthiourea and chlorate suggested that AOB contributed a large fraction to overall ammonia oxidation, while metaproteomics analysis confirmed an active role of CMX in both ammonia and nitrite oxidation. Ecophysiological niche differentiation of CMX clades A and B, AOB and AOA was linked to their requirements for ammonium, oxygen tolerance, and metabolic versatility. Our results demonstrate that despite numerical predominance of CMX, the first step of nitrification in oligotrophic groundwater appears to be primarily governed by AOB. Higher growth yields at lower ammonia turnover rates and energy derived from nitrite oxidation most likely enable CMX to maintain consistently high populations.

microbiology↗

bioRxiv2022

Microbial and Viral Genome and Proteome Nitrogen Demand Varies Across Multiple Spatial Scales Within a Marine Oxygen Minimum Zone

Nutrient availability can significantly influence microbial genomic and proteomic streamlining, for example by selecting for lower nitrogen to carbon ratios. Oligotrophic open ocean microbes have streamlined genomic nitrogen requirements relative to their counterparts in nutrient-rich coastal waters. However, steep gradients in nutrient availability occur at meter- and even micron-level spatial scales. It is unclear if such gradients also structure genomic and proteomic stoichiometry. Focusing on the eastern tropical North Pacific oxygen minimum zone (OMZ), we use comparative metagenomics to examine how nitrogen availability shapes microbial and viral genome properties along the vertical gradient across the OMZ and between two size fractions distinguishing free-living versus particle-associated microbes. We find a substantial increase in nitrogen content of encoded proteins in particle-associated over free-living bacteria and archaea across nitrogen availability regimes over depth. Within each size-fraction, we find that bacterial and viral genomic nitrogen tends to increase with increasing nitrate concentrations with depth. In contrast to cellular genes, the nitrogen content of virus proteins does not differ between size fractions. We identified arginine as a key amino acid in modulating the C:N ratio of core genes for bacteria, archaea, and viruses. Functional analysis reveals that particle-associated bacterial metagenomes are enriched for genes involved in arginine metabolism and organic nitrogen compound catabolism. Our results are consistent with nitrogen streamlining in both cellular and viral genomes on spatial scales of meters to microns. These effects are similar in magnitude to those previously reported across scales of thousands of kilometers. IMPORTANCEThe genomes of marine microbes can be shaped by nutrient cycles, with ocean-scale gradients in nitrogen availability known to influence microbial amino acid usage. It is unclear, however, how genomic properties are shaped by nutrient changes over much smaller spatial scales, for example along the vertical transition into oxygen minimum zones (OMZs) or from the exterior to interior of detrital particles. Here, we measure protein nitrogen usage by marine bacteria, archaea, and viruses using metagenomes from the nitracline of the eastern tropical North Pacific OMZ including both particle-associated and non-associated biomass. Our results show higher genomic and proteomic nitrogen content in particle-associated microbes and at depths with higher nitrogen availability for cellular and viral genomes. This discovery suggests that stoichiometry influences microbial and viral evolution across multiple scales, including the micro- to millimeter scale associated with particle-associated versus free-living lifestyles.

microbiology↗

bioRxiv2021

Rates of primary production in groundwater rival those in oligotrophic marine systems

The terrestrial subsurface contains nearly all of Earths freshwater reserves1 and harbors upwards of 60% of our planets total prokaryotic biomass2,3. While genetic surveys suggest these organisms rely on in situ carbon fixation, rather than the translocation of photosynthetically derived organic carbon4-6, corroborating measurements of carbon fixation in the subsurface are absent. Using a novel ultra-low level 14C-labeling technique, we show that in situ carbon fixation rates in a carbonate aquifer reached 10% of the median rates measured in oligotrophic marine surface waters, and were up to six-fold greater than those observed in lower euphotic zone waters where deep chlorophyll levels peak. Empirical carbon fixation rates were substantiated by both nitrification and anammox rate data. Metagenomic analyses revealed a remarkable abundance of putative chemolithoautotrophic members of an uncharacterized order of Nitrospiria - the first representatives of this class expected to fix carbon via the Wood-Ljungdahl pathway. Based on these fixation rates, we extrapolate global primary production in carbonate groundwaters to be 0.11 Pg of carbon per year.

microbiology↗

bioRxiv2021

Oxygen production by an ammonia-oxidizing archaeon

Ammonia-oxidizing archaea (AOA) are one of the most abundant groups of microbes in the worlds oceans and are key players in the nitrogen cycle. Their energy metabolism, the oxidation of ammonia to nitrite, requires oxygen. Nevertheless, AOA are abundant in environments where oxygen is undetectable. In incubation experiments, where oxygen concentrations were resolved to the nanomolar range, we show that Nitrosopumilus maritimus produces oxygen (O2) and dinitrogen (N2). The pathway is not completely resolved, but it has nitric oxide as a key intermediate. Part of the oxygen produced is directly used for ammonia oxidation, while some accumulates in the surrounding environment. N. maritimus joins a small handful of organisms known to produce oxygen in the dark, and based on this ability, we re-evaluate their role in oxygen-depleted marine environments.

microbiology↗

bioRxiv2019

DNA and RNA-SIP reveal Nitrospira spp. as key drivers of nitrification in groundwater-fed biofilters

Nitrification, the oxidative process converting ammonia to nitrite and nitrate, is driven by microbes and plays a central role in the global nitrogen cycle. Our earlier metagenomics, amoA-amplicon, and amoA-qPCR based investigations of groundwater-fed biofilters indicated a consistently high abundance of comammox Nitrospira, and we hypothesized that these non-classical nitrifiers drive ammonia-N oxidation. Hence, we used DNA and RNA stable isotope probing (SIP) coupled with 16S rRNA amplicon sequencing to identify the active members in the biofilter community when subject to a continuous supply of NH4+ or NO2- in the presence of 13C-HCO3- (labelled) or 12C-HCO3- (unlabelled). Allylthiourea (ATU) and sodium chlorate were added to inhibit autotrophic ammonia- and nitrite-oxidizing bacteria, respectively. Our results confirmed that lineage II Nitrospira dominated ammonium oxidation in the biofilter community. A total of 78 (8 in RNA-SIP and 70 in DNA-SIP) and 96 (25 in RNA-SIP and 71 in DNA-SIP) Nitrospira phylotypes (at 99% 16S rRNA sequence similarity) were identified as complete ammonia- and nitrite-oxidizing, respectively. We also detected significant HCO3- uptake by Acidobacteria subgroup10, Pedomicrobium, Rhizobactera, and Acidovorax under conditions that favoured ammonium oxidation. Canonical Nitrospira alone drove nitrite oxidation in the biofilter community, and activity of archaeal ammonia oxidizing taxa was not detected in the SIP fractions. This study provides the first in-situ evidence of ammonia oxidation by comammox Nitrospira in an ecologically relevant complex microbiome.

physiology↗

bioRxiv2019

Baltic Methanosarcina and Clostridium compete for electrons from metallic iron

Microbial induced corrosion of steel structures, used for transport or storage of fuels, chemical weapons or waste radionuclides, is an environmental and economic threat. In non-sulfidic environments, the exact role of methanogens in steel corrosion is poorly understood. From the non-sulfidic, methanogenic sediments of the Baltic Sea corrosive communities were enriched using exclusively Fe0 as electron donor and CO2 as electron acceptor. Methane and acetate production were persistent for three years of successive transfers. Methanosarcina and Clostridium were attached to the Fe0, and dominated metagenome libraries. Since prior reports indicated Methanosarcina were merely commensals, consuming the acetate produced by acetogens, we investigated whether these methanogens were capable of Fe0 corrosion without bacterial partners (inhibited by an antibiotic cocktail). Unassisted, methanogens corroded Fe0 to Fe2+ at similar rates to the mixed community. Surprisingly, in the absence of competitive bacteria, Baltic-Methanosarcina produced six times more methane than they did in the mixed community. This signifies that Baltic-Methanosarcina achieved better corrosion alone, exclusive of an operative bacterial partner. Our results also show that together with acetogens, Methanosarcina interact competitively to retrieve electrons from Fe0 rather than as commensals as previously assumed.

microbiology↗

bioRxiv2018

Extracellular electron uptake by two Methanosarcina species

Direct electron uptake by prokaryotes is a recently described mechanism with a potential application for energy and CO2 storage into value added chemicals. Members of Methanosarcinales, an environmentally and biotechnologically relevant group of methanogens, were previously shown to retrieve electrons from an extracellular electrogenic partner performing Direct Interspecies Electron Transfer (DIET) and were therefore proposed to be electroactive. However, their intrinsic electroactivity has never been examined. In this study, we tested two methanogens belonging to the genus Methanosarcina, M. barkeri and M. horonobensis, regarding their ability to accept electrons directly from insoluble electron donors like other cells, conductive particles and electrodes. Both methanogens were able to retrieve electrons from Geobacter metallireducens via DIET. Furthermore, DIET was also stimulated upon addition of electrically conductive granular activated carbon (GAC) when each was co-cultured with G. metallireducens. However, when provided with a cathode poised at -400 mV (vs. SHE), only M. barkeri could perform electromethanogenesis. In contrast, the strict hydrogenotrophic methanogen, Methanobacterium formicicum, did not produce methane regardless of the type of insoluble electron donor provided (Geobacter cells, GAC or electrodes). A comparison of functional gene categories between the two Methanosarcina showed differences regarding energy metabolism, which could explain dissimilarities concerning electromethanogenesis at fixed potentials. We suggest that these dissimilarities are minimized in the presence of an electrogenic DIET partner (e.g. Geobacter), which can modulate its surface redox potentials by adjusting the expression of electroactive surface proteins.

microbiology↗

bioRxiv2018

Interspecies interactions mediated by conductive minerals in the sediments of the ferruginous Lake La Cruz, Spain

Lake La Cruz is considered a biogeochemical analogue to early Earth marine environments because its water column is depleted in sulfate, but rich in methane and iron, similar to conditions envisaged for much of the Precambrian. In this early Earth analogue environment, we show that conductive particles establish a tight metabolic coupling between electroactive microbial clades. We propose that mineral-based syntrophy is of potential relevance for the evolution of Earths earliest complex life forms. We show that the anoxic sediment of Lake La Cruz, which is rich in biogeochemically reactive iron minerals, harbors known electroactive species such as Geobacter and Methanothrix, in addition to other groups which have not been previously associated with an electroactive lifestyle. Slurry incubations on various substrates in the presence of conductive particles showed significant methanogenic activity, whereas incubations with non-conductive glass beads resulted in low methanogenic rates similar to slurries without added particles. In the absence of conductive particles, all tested substrates were metabolized to acetate, which accumulated to [~]10 mM. Similar to a previous study on iron-rich Baltic Sea sediments, we observed that conductive mineral additions to La Cruz slurries enabled acetate oxidation, thus preventing acetate accumulation. Acetate oxidation coupled to high methanogenic activity was only maintained in successive mud-free enrichments when these were amended with conductive minerals. In serial mud-free transfers, conductive particles conserved a consortium of Youngiibacter-Methanothrix, whereas Youngiibacter spp. died off in the absence of conductive particles. In contrast, mud-free enrichments without conductive particles ceased any metabolic activity during the second transfers. Syntrophic consortia from this early Earth analogue environment only survived in the presence of conductive particles. Mineral-mediated syntrophy could be one of the earliest evolutionary interspecies associations. Conductive minerals might have fueled metabolic exchange between cells via intercellular electron transfer prompting tight cell-to-cell associations and possibly eukaryogenesis.

microbiology↗

bioRxiv2017

Conductive particles enable syntrophic acetate oxidation between Geobacter and Methanosarcina from coastal sediments

Coastal sediments are rich in conductive minerals, which could impact microbial processes for which acetate is a central intermediate. In the methanogenic zone, acetate is consumed by methanogens and/or syntrophic acetate oxidizing (SAO) consortia. SAO consortia live under extreme thermodynamic pressure and their survival depends on successful partnership. Here we demonstrate that conductive minerals facilitate a SAO partnership between Geobacter and Methanosarcina from the coastal sediments of the Bothnian Bay, Baltic Sea. Bothnian methanogenic sediments showed a high apparent isotopic fractionation (c 1.07) characteristic of CO2-reductive methanogenesis. The native community was represented by electrogens such as Geobacter and methanogens like Methanosarcina. Upon the addition of conductive particles (activated carbon and magnetite) methanogenesis from acetate increased four fold. Geobacter (96% related to G. psychrophilus) and Methanosarcina (99% related to M. subterranea) dominated the conductive particle-spiked SAO communities. Using NanoSIMS we demonstrated that during SAO, Geobacter incorporated 82% of the labeled acetate as compared to only 18% by Methanosarcina. At the same time Geobacter converted 27% of the 13C-acetate to 13CO2 as detected by IRMS. Indigenous soluble shuttles were not involved in SAO, since spiking fresh cultures with spent-media filtrate had no effect on methanogenic rates. Our results demonstrate that Geobacter oxidizes acetate to CO2 while transferring electrons extracellularly via conductive particles to Methanosarcina, which utilizes them for CO2 reduction to methane. In natural environments, mediation of SAO by conductive particles between electrogens and methanogens could impact the iron and methane cycles.\n\nSignificanceAcetate oxidizing bacteria are known to thrive in mutualistic consortia in which H2 or formate is shuttled to a methane-producing Archaea partner. Here we discovered that they could instead transfer electrons via conductive minerals. Mineral-SAO (syntrophic acetate oxidation) could be a vital pathway for CO2-reductive methanogenesis in the environment, especially in sediments rich in conductive minerals. Mineral-SAO is therefore of potential importance for both iron and methane cycles in sediments and soils. Additionally, our observations imply that agricultural runoff or amendments with conductive chars could trigger a significant increase in methane emissions.

microbiology↗