Summary
We used paddy soil slurries amended with rice straw to identify the microbial populations involved in the methanogenic breakdown of plant polymers. Rice straw greatly stimulated microbial ...activity over the 28‐day incubation period. On day 7, the transient peak concentration of acetate (24 mM) coincided with the onset of increased methane production. Microbial 16S rRNA transcript numbers increased by one to two orders of magnitude, but not the 16S rRNA gene copy numbers. Using metatranscriptomic rRNA, Clostridiaceae, Lachnospiraceae, Ruminococcaceae, Veillonellaceae and Pseudomonadaceae were identified to be the most abundant and the most dynamic bacterial groups. Changes in methanogen rRNA and mRNA abundances corresponded well with methanogenic activity. Acetate determined the abundance ratio between Methanosarcinaceae and Methanosaetaceae. Methanocellaceae dominated hydrogenotrophic methanogenesis. Transcript levels of mRNA families involved in plant polymer breakdown increased slightly with time. Glycosyl hydrolase (GH) transcripts involved in cellulose and chitin breakdown were predominantly expressed by the Firmicutes, whereas those involved in hemicellulose breakdown exhibited more diverse taxonomic sources, including Acidobacteria, Bacteriodetes and Chloroflexi. Taken together, we observed strong population dynamics and the expression of taxonomically diverse GH families, suggesting that not only Firmicutes, but also less abundant groups play a major functional role in the decomposition of rice straw.
Drainage is an important mitigation strategy to reduce methane emission from rice paddies. Here, we investigated how drainage shapes structure and functioning of the paddy soil microbial community. ...Soil microcosms were pre-incubated for 28 days under flooded conditions followed by nine days' drainage. Upon sampling, metatranscriptome libraries were generated from flooded and drained soils. With drainage, oxygen concentration increased from suboxic (1.6 μmol/l) to near-atmospheric (240 μmol/l) levels. Concurrently, water potential decreased to −0.87 MPa (corresponding to 11% soil moisture content). Drainage did not affect the absolute (RT-qPCR) SSU rRNA abundance of Bacteria and Archaea, but changed significantly their community composition. Firmicutes (Clostridiaceae, Ruminococcaceae, and Lachnospiraceae) decreased in relative abundance, while Actinobacteria (Nocardioidaceae) and Proteobacteria (Comamonadaceae) increased. These taxon-specific dynamics were observed on rRNA and mRNA levels. Methanogen SSU rRNA was stable, but methanogen mRNA significantly decreased. This coincided with complete inhibition of the methane production potential in drained soil. Among Eukarya, protists and Amoebozoa thrived in flooded soil, while Fungi proliferated with drainage. In particular, Pezizomycotina (Ascomycota) and Agaricomycotina (Basidiomycota) were the most abundant fungal groups in dry soil. Taking community-wide mRNA expression as a proxy, the overall microbial activity was not severely affected by drainage. The proportion of mRNA in total RNA increased from 1.7% to 2%. In particular, the abundance of mRNA related to transcription and translation significantly increased. Correspondingly, the bacterial SSU rRNA transcript/gene ratio increased 12-fold with drainage, suggesting the development of a metabolically highly active microbial community well adapted to oxic and dry soil conditions. This community showed an increased transcription of genes involved in the degradation of lignin, peptidoglycan, and storage molecules such as glycogen. Under flooded conditions, the microbial community expressed a higher level of glycoside hydrolase transcripts involved in cellulose and chitin degradation.
•Among Bacteria, drainage promoted enrichment of Proteobacteria and Actinobacteria.•Among Eukarya, drainage induced strong proliferation of the Ascomycota (fungi).•The newly arriving microbial community exhibited high transcriptional activity.•Methanogen abundance was stable on SSU rRNA level but not on mRNA level.•mRNA turnover was a greater proxy for community change than rRNA dynamics.
Despite the widely observed predominance of
. Patescibacteria in subsurface communities, their input source and ecophysiology are poorly understood. Here we study mechanisms of the formation of a ...groundwater microbiome and the subsequent differentiation of
. Patescibacteria. In the Hainich Critical Zone Exploratory, Germany, we trace the input of microorganisms from forested soils of preferential recharge areas through fractured aquifers along a 5.4 km hillslope well transect.
. Patescibacteria were preferentially mobilized from soils and constituted 66% of species-level OTUs shared between seepage and shallow groundwater. These OTUs, mostly related to
. Kaiserbacteraceae,
. Nomurabacteraceae, and unclassified UBA9983 at the family level, represented a relative abundance of 71.4% of the
. Patescibacteria community at the shallowest groundwater well, and still 44.4% at the end of the transect. Several
. Patescibacteria subclass-level groups exhibited preferences for different conditions in the two aquifer assemblages investigated:
. Kaiserbacteraceae surprisingly showed positive correlations with oxygen concentrations, while
. Nomurabacteraceae were negatively correlated. Co-occurrence network analysis revealed a central role of
. Patescibacteria in the groundwater microbial communities and pointed to potential associations with specific organisms, including abundant autotrophic taxa involved in nitrogen, sulfur and iron cycling. Strong associations among
. Patescibacteria themselves further suggested that for many groups within this phylum, distribution was mainly driven by conditions commonly supporting a fermentative life style without direct dependence on specific hosts. We propose that import from soil, and community differentiation driven by hydrochemical conditions, including the availability of organic resources and potential hosts, determine the success of
. Patescibacteria in groundwater environments.
Summary
Subsurface ecosystems like groundwater harbour diverse microbial communities, including small‐sized, putatively symbiotic organisms of the Candidate Phyla Radiation, yet little is known about ...their ecological preferences and potential microbial partners. Here, we investigated a member of the superphylum Microgenomates (Cand. Roizmanbacterium ADI133) from oligotrophic groundwater using mini‐metagenomics and monitored its spatio‐temporal distribution using 16S rRNA gene analyses. A Roizmanbacteria‐specific quantitative PCR assay allowed us to track its abundance over the course of 1 year within eight groundwater wells along a 5.4 km hillslope transect, where Roizmanbacteria reached maximum relative abundances of 2.3%. In‐depth genomic analyses suggested that Cand. Roizmanbacterium ADI133 is a lactic acid fermenter, potentially able to utilize a range of complex carbon substrates, including cellulose. We hypothesize that it attaches to host cells using a trimeric autotransporter adhesin and inhibits their cell wall biosynthesis using a toxin–antitoxin system. Network analyses based on correlating Cand. Roizmanbacterium ADI133 abundances with amplicon sequencing‐derived microbial community profiles suggested one potential host organism, classified as a member of the class Thermodesulfovibrionia (Nitrospirae). By providing lactate as an electron donor Cand. Roizmanbacterium ADI133 potentially mediates the transfer of carbon to other microorganisms and thereby is an important connector in the microbial community.
The accessibility of iron (Fe) species for microbial processes is dependent on solubility and redox state, which are influenced by complexation with dissolved organic matter (DOM) and ...water-extractable organic matter (WEOM). We evaluated the complexation of these pools of organic matter to soluble Fe(II) and Fe(III) in the slightly acidic Schlöppnerbrunnen fen and subsequent effects on Fe(II) oxidation and Fe(III) reduction. We found the majority of soluble Fe(II) and Fe(III) is complexed to DOM. High-resolution mass spectrometry identified potential complexing partners in peat-derived water extracts (PWE), including compound classes known to function as ligands or electron shuttles, like tannins and sulfur-containing compounds. Furthermore, we observed clear differences in the stability of Fe(II)- and Fe(III)-DOM, with more labile complexes dominating the upper, oxic layers (0–10 cm) and more stable complexes in lower, anoxic layers (15–30 cm). Metal isotope-coded profiling identified a single potential chemical formula (C42H57O13N9Fe2) associated with a stable Fe-DOM complex. Fe(III) reduction and Fe(II) oxidation incubations with Geobacter sulfurreducens PCA and Shewanella oneidensis MR-1 or Sideroxydans CL-21, respectively, were used to determine the influence of Fe-DOM complexes on Fe cycling rates. The addition of PWE led to a 2.3-fold increase in Fe(III) reduction rates and 0.5-fold increase in Fe(II) oxidation rates, indicating Fe-DOM complexes greatly influence microbial Fe cycling by potentially serving as electron shuttles. Molecular analyses revealed Fe(III)-reducing and Fe(II)-oxidizing bacteria co-exist across all depths, in approximately equal proportions (representing 0.1–1.0% of the total microbial community), despite observed changes in redox potential. The activity of Fe(III)-reducing bacteria might explain the presence of the detected Fe(II) stabilized via complexation with DOM even under oxic conditions in upper peat layers. Therefore, these Fe(II)-DOM complexes can be recycled by microaerophilic Fe(II)-oxidizers. Taken together, these results suggest Fe-DOM complexation in the fen accelerates microbial-mediated redox processes across the entire redox continuum.
Display omitted
•This field study of an Fe-rich peatland underlies the importance of Fe species determination.•The majority of Fe is complexed by DOM and keeps Fe(II) and Fe(III) in solution.•DOM stabilizes Fe(II) in oxic soil layers and contributes to the redox equilibria.•Fe-DOM-complexes enhance microbially-mediated Fe cycling.•Fe(II) and Fe(III) across all depths allows co-existence of Fe-cycling microorganisms.
Northern peatlands play a crucial role in the global carbon balance, serving as a persistent sink for atmospheric CO2 and a global carbon store. Their most extensive type, Sphagnum‐dominated acidic ...peatlands, is inhabited by microorganisms with poorly understood degradation capabilities. Here, we applied a combination of barcoded pyrosequencing of SSU rRNA genes and Illumina RNA‐Seq of total RNA (metatranscriptomics) to identify microbial populations and enzymes involved in degrading the major components of Sphagnum‐derived litter and exoskeletons of peat‐inhabiting arthropods: cellulose, xylan, pectin and chitin. Biopolymer addition to peat induced a threefold to fivefold increase in bacterial cell numbers. Functional community profiles of assembled mRNA differed between experimental treatments. In particular, pectin and xylan triggered increased transcript abundance of genes involved in energy metabolism and central carbon metabolism, such as glycolysis and TCA cycle. Concurrently, the substrate‐induced activity of bacteria on these two biopolymers stimulated grazing of peat‐inhabiting protozoa. Alveolata (ciliates) was the most responsive protozoa group as confirmed by analysis of both SSU rRNA genes and SSU rRNA. A stimulation of alphaproteobacterial methanotrophs on pectin was consistently shown by rRNA and mRNA data. Most likely, their significant enrichment was due to the utilization of methanol released during the degradation of pectin. Analysis of SSU rRNA and total mRNA revealed a specific response of Acidobacteria and Actinobacteria to chitin and pectin, respectively. Relatives of Telmatobacter bradus were most responsive among the Acidobacteria, while the actinobacterial response was primarily affiliated with Frankiales and Propionibacteriales. The expression of a wide repertoire of carbohydrate‐active enzymes (CAZymes) corresponded well to the detection of a highly diverse peat‐inhabiting microbial community, which is dominated by yet uncultivated bacteria.
Acid mine drainage (AMD) and mine tailing environments are well-characterized ecosystems known to be dominated by organisms involved in iron- and sulfur-cycling. Here we examined the microbiology of ...industrial soft coal slags that originate from alum leaching, an ecosystem distantly related to AMD environments. Our study involved geochemical analyses, bacterial community profiling, and shotgun metagenomics. The slags still contained high amounts of alum constituents (aluminum, sulfur), which mediated direct and indirect effects on bacterial community structure. Bacterial groups typically found in AMD systems and mine tailings were not present. Instead, the soft coal slags were dominated by uncharacterized groups of Acidobacteria (DA052 subdivision 2, KF-JG30-18 subdivision 13), Actinobacteria (TM214), Alphaproteobacteria (DA111), and Chloroflexi (JG37-AG-4), which have previously been detected primarily in peatlands and uranium waste piles. Shotgun metagenomics allowed us to reconstruct 13 high-quality Acidobacteria draft genomes, of which two genomes could be directly linked to dominating groups (DA052, KF-JG30-18) by recovered 16S rRNA gene sequences. Comparative genomics revealed broad carbon utilization capabilities for these two groups of elusive Acidobacteria, including polysaccharide breakdown (cellulose, xylan) and the competence to metabolize C1 compounds (ribulose monophosphate pathway) and lignin derivatives (dye-decolorizing peroxidases). Equipped with a broad range of efflux systems for metal cations and xenobiotics, DA052 and KF-JG30-18 may have a competitive advantage over other bacterial groups in this unique habitat.
The formation of Fe(III) oxides in natural environments occurs in the presence of natural organic matter (OM), resulting in the formation of OM–mineral complexes that form through adsorption or ...coprecipitation processes. Thus, microbial Fe(III) reduction in natural environments most often occurs in the presence of OM–mineral complexes rather than pure Fe(III) minerals. This study investigated to what extent does the content of adsorbed or coprecipitated OM on ferrihydrite influence the rate of Fe(III) reduction by Shewanella oneidensis MR-1, a model Fe(III)-reducing microorganism, in comparison to a microbial consortium extracted from the acidic, Fe-rich Schlöppnerbrunnen fen. We found that increased OM content led to increased rates of microbial Fe(III) reduction by S. oneidensis MR-1 in contrast to earlier findings with the model organism Geobacter bremensis. Ferrihydrite–OM coprecipitates were reduced slightly faster than ferrihydrites with adsorbed OM. Surprisingly, the complex microbial consortia stimulated by a mixture of electrons donors (lactate, acetate, and glucose) mimics S. oneidensis under the same experimental Fe(III)-reducing conditions suggesting similar mechanisms of electron transfer whether or not the OM is adsorbed or coprecipitated to the mineral surfaces. We also followed potential shifts of the microbial community during the incubation via 16S rRNA gene sequence analyses to determine variations due to the presence of adsorbed or coprecipitated OM–ferrihydrite complexes in contrast to pure ferrihydrite. Community profile analyses showed no enrichment of typical model Fe(III)-reducing bacteria, such as Shewanella or Geobacter sp., but an enrichment of fermenters (e.g., Enterobacteria) during pure ferrihydrite incubations which are known to use Fe(III) as an electron sink. Instead, OM–mineral complexes favored the enrichment of microbes including Desulfobacteria and Pelosinus sp., both of which can utilize lactate and acetate as an electron donor under Fe(III)-reducing conditions. In summary, this study shows that increasing concentrations of OM in OM–mineral complexes determines microbial Fe(III) reduction rates and shapes the microbial community structure involved in the reductive dissolution of ferrihydrite. Similarities observed between the complex Fe(III)-reducing microbial consortia and the model Fe(III)-reducer S. oneidensis MR-1 suggest electron-shuttling mechanisms dominate in OM-rich environments, including soils, sediments, and fens, where natural OM interacts with Fe(III) oxides during mineral formation.
Near-surface groundwaters are prone to receive (in)organic matter input from their recharge areas and are known to harbor autotrophic microbial communities linked to nitrogen and sulfur metabolism. ...Here, we use multi-omic profiling to gain holistic insights into the turnover of inorganic nitrogen compounds, carbon fixation processes, and organic matter processing in groundwater. We sampled microbial biomass from two superimposed aquifers via monitoring wells that follow groundwater flow from its recharge area through differences in hydrogeochemical settings and land use. Functional profiling revealed that groundwater microbiomes are mainly driven by nitrogen (nitrification, denitrification, and ammonium oxidation anammox) and to a lesser extent sulfur cycling (sulfur oxidation and sulfate reduction), depending on local hydrochemical differences. Surprisingly, the differentiation potential of the groundwater microbiome surpasses that of hydrochemistry for individual monitoring wells. Being dominated by a few phyla (
,
,
, and
), the taxonomic profiling of groundwater metagenomes and metatranscriptomes revealed pronounced differences between merely present microbiome members and those actively participating in community gene expression and biogeochemical cycling. Unexpectedly, we observed a constitutive expression of carbohydrate-active enzymes encoded by different microbiome members, along with the groundwater flow path. The turnover of organic carbon apparently complements for lithoautotrophic carbon assimilation pathways mainly used by the groundwater microbiome depending on the availability of oxygen and inorganic electron donors, like ammonium.
Groundwater is a key resource for drinking water production and irrigation. The interplay between geological setting, hydrochemistry, carbon storage, and groundwater microbiome ecosystem functioning is crucial for our understanding of these important ecosystem services. We targeted the encoded and expressed metabolic potential of groundwater microbiomes along an aquifer transect that diversifies in terms of hydrochemistry and land use. Our results showed that the groundwater microbiome has a higher spatial differentiation potential than does hydrochemistry.
A link between microbial life history strategies and soil organic carbon storage in agroecosystems is presumed, but largely unexplored at the gene level. We aimed to elucidate whether and how ...differential organic material amendments (manure versus peat-vermiculite) affect, relative to sole chemical fertilizer application, the link between microbial life history strategies and soil organic carbon storage in a wheat-maize rotation field experiment. To achieve this goal, we combined bacterial 16S rRNA gene and fungal ITS amplicon sequencing, metagenomics and the assembly of genomes. Fertilizer treatments had a significantly greater effect on microbial community composition than aggregate size, with soil available phosphorus and potassium being the most important community-shaping factors. Limitation in labile carbon was linked to a K-selected oligotrophic life history strategy (Gemmatimonadetes, Acidobacteria) under sole chemical fertilizer application; defined by a significant enrichment of genes involved in resource acquisition, polymer hydrolysis, and competition. By contrast, excess of labile carbon promoted an r-selected copiotrophic life history strategy (Cytophagales, Bacillales, Mortierellomycota) under manure treatment; defined by a significant enrichment of genes involved in cellular growth. A distinct life history strategy was not observed under peat-vermiculite treatment, but rather a mix of both K-selected (Acidobacteria) and r-selected (Actinobacteria, Mortierellomycota) microorganisms. Compared to sole chemical fertilizer application, soil organic carbon storage efficiency was significantly increased by 26.5% and 50.0% under manure and peat-vermiculite treatments, respectively. Taken together, our results highlight the importance of organic material amendments, but in particular a one-time peat-vermiculite application, to promote soil organic carbon storage as a potential management strategy for sustainable agriculture.
Display omitted
•Organic material amendments significantly increased soil carbon storage efficiency.•Organic manure addition enriched for genes indicative of cellular growth strategies.•Chemical fertilizer enriched for genes involved in resource acquisition and competition.•Soil amended with peat-vermiculite was dominated by a mix of r- and K-selected microbes.•Gemmatimonadetes showed a negative correlation to soil carbon storage efficiency.
PDF
