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Loy, A.

Publications and source records attributed to Loy, A..

At least 19 recordsLinked to original sources

Reversible fixation of microbial cells for targeted genomics

Phylogeny- or activity-based fluorescent labelling of microorganisms coupled with fluorescence activated cell sorting (FACS) is a powerful approach to rapidly isolate cells of interest from complex communities for targeted genomics. However, the method has not been widely adopted because standard paraformaldehyde or ethanol fixation procedures hamper nucleic acid recovery and/or long-term sample storage. Here, we present dithiobis(succinimidyl propionate) (DSP) as a reversible fixative for microbial cells that enables fluorescence imaging and DNA extraction and amplification for sequencing. DSP fixation is compatible with widely used fluorescence in situ hybridization (FISH) approaches and bioorthogonal non-canonical amino acid tagging, and can be applied to diverse sample types, where it consistently performed as well as paraformaldehyde. Furthermore, high-quality genomes were obtained from individual and multiple bacterial cells selectively extracted from complex samples using FISH-FACS. Thus, DSP is a dual-use fixative for microbiome imaging and sequencing, improving targeted microbial genomics.

microbiology↗

Kineochelins - a novel group of siderophores from an Antarctic bacterium

BackgroundThe global rise of antimicrobial resistance has intensified the search for new microbial metabolites from underexplored environments and taxonomic groups. Extreme and geographically isolated habitats, such as Antarctic terrestrial ecosystems, represent promising reservoirs of novel biosynthetic diversity, particularly among rare and difficult-to-cultivate actinomycetes, where chemical mediators are thought to play key roles in microbial persistence and interaction under resource-limited conditions. ResultsHere, we report the characterization of kineochelins, a previously undescribed group of siderophores produced by an Antarctic isolate, Actinokineospora sp. UV203 representing difficult to cultivate actinomycetes. Structural elucidation revealed a set of closely related congener molecules with a mixed-ligand architecture consistent with metal-chelating activity. Genome mining combined with transcriptomic analysis identified the involvement of a dedicated nonribosomal peptide synthetase-encoding biosynthetic gene cluster responsible for kineochelin production. Comparative genomic analyses showed that, although kineochelin biosynthetic genes share limited homology with those of known mixed-ligand siderophores, their biosynthetic pathways differ substantially in gene content and organization, indicating a distinct evolutionary lineage. Functional characterization of kineochelins demonstrated strong and selective iron chelation, with pronounced affinity for ferric and ferrous iron. Crude culture extracts inhibited the growth of bacterial strains isolated from the same Antarctic environment, suggesting that kineochelin-associated chemistry contributes to iron-mediated competitive interactions within native microbial communities. In addition, kineochelin-enriched fractions exhibited selective inhibitory activity against the opportunistic yeast pathogen Nakaseomyces glabratus and a clinical isolate of Saccharomyces cerevisiae associated with invasive infection. ConclusionsTogether, these findings expand the known chemical and biosynthetic diversity of the genus Actinokineospora and demonstrate that Antarctic rare actinomycetes are a valuable source of novel natural products with potential relevance for microbial ecology and biotechnology. The ecological activities of kineochelins highlight the role of iron acquisition in shaping microbial interactions in extreme environments and underscore the biotechnological potential of metabolites derived from underexplored polar microorganisms.

microbiology↗

Methanobrevibacter smithii associates with colorectal cancer through trophic control of the cancer bacteriome

The human gut is colonized by trillions of microbes that influence the health of their human host. Whereas many bacterial species have now been linked to a variety of different diseases, the involvement of Archaea in human disease remains elusive. Here we searched for gut archaeal signatures of disease by screening 19 cross-sectional clinical studies comprising more than 1,800 individuals. We found that associations between Archaea and medical disorders are common but highly variable and are dominated by a significant increase of Methanobrevibacter smithii in colorectal cancer (CRC) patients. Metabolic modelling and in vitro co-culture identified distinct mutualistic interactions of M. smithii with CRC-causing bacteria such as Fusobacterium nucleatum, including metabolic enhancement. Metabolomics further revealed archaeal-derived compounds with tumor-modulating properties. This provides the first mechanistic link between human gut archaeome and CRC and highlights its role in modulating health in humans through trophic control of the resident bacteriome.

microbiology↗

Extensive richness and novel taxa of sulfoquinovose-degrading bacteria in the cow rumen

Sulfoquinovose (SQ), a sulfonated sugar derived from the thylakoid membrane lipid sulfoquinovosyl diacylglycerol (SQDG), is abundant in photosynthetic organisms and plays a key role in global sulfur cycling. Its degradation in nature is mediated by specialized bacteria, many of which rely on the enzyme sulfoquinovosidase (YihQ) to release SQ from SQDG. Despite its ecological importance, the diversity and functional roles of SQ-degrading microorganisms remain poorly characterized in natural environments. Here, we developed a yihQ-targeted amplicon sequencing approach to investigate the richness and distribution of SQ-degrading bacteria across selected environments, including marine sediments and the mammalian gut. We revealed particularly high richness of yihQ-containing microorganisms in cow rumen, far exceeding that observed in human and mouse gut microbiomes, suggesting an important role of SQ metabolism in ruminant digestion. Anaerobic microcosm experiments with SQ-amended rumen fluid revealed cooperative microbial degradation of SQ to sulfide via isethionate cross-feeding. Amplicon sequencing and genome-resolved metagenomics identified novel uncultured SQ-degrading taxa, including members of Caproiciproducens (Acutalibacteraceae), Limivicinus (Oscillospiraceae), and Sphaerochaetaceae, which encode the sulfo-transketolase pathway, along with Mailhella (Desulfovibrionaceae), a likely isethionate-respiring bacterium. This study presents the first functional gene-based assay for tracking environmental yihQ diversity, highlights SQ degradation as a central metabolic process in the cow rumen, describes novel SQ-metabolizing bacteria, and advances understanding of sulfur physiology in complex microbial communities.

microbiology↗

Evolutionary conservation of midline repulsive signaling by Robo family receptors inflies and mice

The Roundabout (Robo) family is an evolutionarily conserved group of axon guidance receptors that regulate midline crossing in a wide range of animal groups by signaling midline repulsion in response to Slit ligands. However, it is not known whether Robo receptors from different species signal midline repulsion via equivalent mechanisms. To examine the evolutionary conservation of midline repulsive signaling, here we express Robo family proteins from mouse in neurons of the fruit fly, Drosophila melanogaster. We show that Robo proteins which normally function in canonical Slit-dependent midline repulsion in the mouse (mRobo1 and mRobo2) can also repel Drosophila axons from the midline in the fly embryonic ventral nerve cord, and can partially rescue the ectopic midline crossing defects caused by loss of Drosophila robo1, though less efficiently as Drosophila Robo1 itself. In contrast, mouse Robo3 isoforms (mRobo3.1 and mRobo3.2) which do not normally respond to Slit have no detectable effect on axon guidance when expressed in fly embryos. We further show that the differences in midline repulsive signaling effectiveness between fly and mouse Robos is not due to a simple difference in Slit affinity conferred by the Slit-binding Ig1 domain. Together, our results support the idea that the core signaling mechanisms employed by Robo family receptors are conserved across bilaterians, though some degree of evolutionary divergence has decreased the ability of receptors from different bilaterian clades to directly substitute for one another.

developmental biology↗

Associations between gut microbiota and personality traits: insights from a captive common marmoset (Callithrix jacchus) colony

Recent studies have suggested the link between inter-individual behavioural variation (i.e., animal personality) and gut microbiota. Non-human primates living under controlled conditions are valuable models to investigate diet-independent microbiome-host interactions. In this study, we investigated links between specific gut microbiota members and personality traits, as well as group membership, sex, age class, breeding status and relatedness of 26 captive common marmosets (Callithrix jacchus), maintained under the same diet and housing conditions. Personality was assessed using an established testing battery in repeated tests. Then, we collected a total of 225 fecal samples during the summers of 2017 and 2019 from five marmoset social groups for 16S rRNA gene amplicon sequencing. Within-individual microbiota variance was smaller than that between group members. Group members also exhibited more similar gut microbiota than individuals from different groups in each sampling year. Beta diversity of the gut microbiota was linked with personality traits, age class, sex, and breeding status, but not with genetic relatedness. We identified specific bacterial taxa associated with personality traits. In particular, members of the sulfite-reducing genera Desulfovibrio were enriched in more avoidant marmosets. Amplicon sequencing of the dissimilatory sulfite reductase gene dsrB confirmed this pattern, yet additionally revealed an unknown uncultured bacterium that was the predominant sulfite-reducing bacterium in the fecal samples and was linked to more explorative individuals. These findings highlight specific association patterns between selected microbial taxa and personality traits in captive common marmosets. ImportanceThis study provides valuable insights into the intricate relationship between gut microbiota and host personality traits, using captive common marmosets as a model. By controlling for diet and housing conditions, it probes key host factors such as personality, age, sex, and social group membership, offering a robust framework for understanding microbiome-host interactions. The discovery of specific microbial taxa associated with personality traits, particularly the enrichment of sulfite-reducing genera in more avoidant individuals, underscores the potential role of the gut microbiome in shaping or reflecting personality. These findings advance our understanding of microbiome-host dynamics and pave the way for future research on the mechanistic links between behavior and gut microbiota in other animal models and across broader ecological contexts.

microbiology↗

Sulfoquinovose is differently degraded by the mouse and human gut microbiota and not metabolized by the host

BackgroundSulfoquinovose (SQ) is a green-diet-derived sulfonated glucose and a selective substrate for few human gut bacteria. Complete anaerobic SQ degradation via interspecies metabolite transfer to sulfonate-respiring bacteria produces hydrogen sulfide, which has dose- and context-dependent health effects. Here, we studied potential SQ degradation by the mammalian host and the impact of SQ supplementation on human and murine gut microbiota diversity and metabolism. Results13CO2 breath tests with germ-free C57BL/6 mice gavaged with 13C-SQ were negative. Also, SQ was not degraded by human intestinal cells in vitro, indicating that SQ is not directly metabolized by mice and humans. Addition of increasing SQ concentrations to human fecal microcosms revealed dose-dependent responses of the microbiota and corroborated the relevance of Agathobacter rectalis and Bilophila wadsworthia in cooperative degradation of SQ to hydrogen sulfide via interspecies transfer of 2,3-dihydroxy-1-propanesulfonate (DHPS). Similar to the human gut microbiome, the genetic capacity for SQ or DHPS degradation is sparsely distributed among bacterial species in the mouse gut. Escherichia coli and Enterocloster clostridioformis were identified as primary SQ degraders in the mouse gut. SQ and DHPS supplementation experiments with conventional laboratory mice and their intestinal contents showed that SQ was incompletely catabolized to DHPS. Although some E. clostridioformis genomes encode an extended sulfoglycolytic pathway for both SQ and DHPS fermentation, SQ was only degraded to DHPS by a mouse-derived E. clostridioformis strain. ConclusionsOur findings suggest that SQ is solely a nutrient for the gut microbiota and not for mice and humans, emphasizing its potential as a prebiotic. SQ degradation by the microbiota of conventional laboratory mice differs from the human gut microbiota by absence of DHPS degradation activity. Hence, the microbiota of conventional laboratory mice does not fully represent the SQ metabolism in humans, indicating the need for alternative model systems to assess the impact of SQ on human health. This study advances our understanding of how individual dietary compounds shape the microbial community structure and metabolism in the gut and thereby potentially influence host health.

microbiology↗

DeepRod: A human-in-the-loop system for automatic rodent behavior analysis

We present a human-in-the-loop system for efficient rodent behavior analysis in drug development. Addressing the time-consuming and labor-intensive nature of manual behavior categorization, this UX-optimized platform integrates AI for complex behavior prediction and active learning to identify rare events. The proposed solution leverages a cloud-native data processing pipeline, AI-based novelty behavior recognition and multi-class classification, demonstrating significant improvements in behavior labeling and discovery.

animal behavior and cognition↗

Global diversity and inferred ecophysiology of microorganisms with the potential for dissimilatory sulfate/sulfite reduction

Sulfate/sulfite-reducing microorganisms (SRM) are ubiquitous in nature, driving the global sulfur cycle. A hallmark of SRM is the dissimilatory sulfite reductase encoded by the paralogous genes dsrAB. Based on analysis of 950 mainly metagenome-derived dsrAB-encoding genomes, we redefine the global diversity of microorganisms with the potential for dissimilatory sulfate/sulfite reduction and uncover genetic repertoires that challenge earlier generalizations regarding their mode of energy metabolism. We show: (i) 19 out of 23 bacterial and 2 out of 4 archaeal phyla harbor uncharacterized SRM, (ii) four phyla including the Desulfobacterota harbor microorganisms with the genetic potential to switch between sulfate/sulfite reduction and sulfur oxidation, and (iii) the combination as well as presence/absence of different dsrAB-types, dsrL-types and dsrD provides guidance on the inferred direction of dissimilatory sulfur metabolism. We further provide an updated dsrAB database including >60% taxonomically resolved, uncultured family-level lineages and recommendations on existing dsrAB primers for environmental surveys. Our work summarizes insights into the inferred ecophysiology of newly discovered SRM, puts SRM diversity into context of the major recent changes in bacterial and archaeal taxonomy, and provides an up-to-date framework to study SRM in a global context. One sentence summarySulfate/sulfite reducing microorganisms are shaping Earths interconnected sulfur and carbon cycles since the Archaean: this legacy unfolds in 27 archaeal and bacterial phyla encountered in diverse marine, terrestrial, and deep-subsurface environments.

microbiology↗

A novel taurine-respiring murine gut bacterium contributes to colonization resistance against enteropathogens

Taurine-respiring gut bacteria produce H2S with ambivalent impact on host health. We report the isolation and genomic-ecophysiological characterization of the first taurine-respiring mouse gut bacterium. Taurinivorans muris represents a new widespread species with protective capacity against pathogens and differs from the human gut sulfidogen Bilophila wadsworthia in its sulfur metabolism and host distribution. Despite alternative physiologies, taurine respiration was the main in vivo lifestyle of T. muris independent of mouse diet and genotype. In gnotobiotic mice, T. muris selectively enhanced the activity of a sulfur metabolism gene-encoding prophage and provided slightly increased colonization resistance against Salmonella Typhimurium, which showed reduced expression of galactonate catabolism genes. We identified T. muris as the dominant sulfidogen of a mouse microbiota that conferred H2S-mediated protection against Klebsiella pneumoniae in a previous study. Together, we revealed the realized physiological niche of a key murine gut sulfidogen and its impact on pathogen and phage gene expression. One sentence summaryOur work identified and characterized a new core member of the murine gut microbiota, revealed sulfidogenic taurine respiration as its predominant in vivo lifestyle, and emphasizes its protective function in pathogen colonization.

microbiology↗

Novel taxa of Acidobacteriota involved in seafloor sulfur cycling

Acidobacteriota are widespread and often abundant in marine sediments, yet their metabolic and ecological properties are poorly understood. Here, we examined metabolisms and distributions of Acidobacteriota in marine sediments of Svalbard by functional predictions from metagenome-assembled genomes (MAGs), amplicon sequencing of 16S rRNA and dissimilatory sulfite reductase (dsrB) genes and transcripts, and gene expression analyses of tetrathionate-amended microcosms. Acidobacteriota were the second most abundant dsrB-harboring (averaging 13%) phylum after Desulfobacterota in Svalbard sediments, and represented 4% of dsrB transcripts on average. We propose two new Acidobacteriota genera, Candidatus Sulfomarinibacter (class Thermoanaerobaculia, sub-division 23) and Ca. Polarisedimenticola ( sub-division 22), with distinct genetic properties that may explain their distributions in biogeochemically distinct fjord sediments. Ca. Sulfomarinibacter encodes flexible respiratory routes, with potential for oxygen, nitrous oxide, metal-oxide, tetrathionate, sulfur and sulfite/sulfate respiration, and possibly sulfur disproportionation. Potential nutrients and energy include cellulose, proteins, cyanophycin, hydrogen and acetate. A Ca. Polarisedimenticola MAG encodes enzymes to degrade proteins, and to reduce oxygen, nitrate, sulfur/polysulfide and metal-oxides. 16S rRNA gene and transcript profiling showed Ca. Sulfomarinibacter members were relatively abundant and transcriptionally active in sulfidic fjord sediments, while Ca. Polarisedimenticola members were more relatively abundant in metal-rich fjord sediments. Overall, we reveal various physiological features of uncultured marine Acidobacteriota that indicate fundamental roles in seafloor biogeochemical cycling.

microbiology↗

Woeseiales transcriptional response in Arctic fjord surface sediment

Distinct lineages of Gammaproteobacteria clade Woeseiales are globally-distributed in marine sediments, based on metagenomic and 16S rRNA gene analysis. Yet little is known about why they are dominant or their ecological role in Arctic fjord sediments, where glacial retreat is rapidly imposing change. This study combined 16S rRNA gene analysis, metagenome-assembled genomes (MAGs), and genome-resolved metatranscriptomics uncovered the in situ abundance and transcriptional activity of Woeseiales with burial in four shallow sediment sites of Kongsfjorden and Van Keulenfjorden of Svalbard (79{degrees}N). We present five novel Woeseiales MAGs and show transcriptional evidence for metabolic plasticity during burial, including sulfur oxidation with reverse dissimilatory sulfite reductase (dsrAB) down to 4 cm depth and nitrite reduction down to 6 cm depth. A single stress protein, spore protein SP21 (hspA), had a tenfold higher mRNA abundance than any other transcript, and was a hundredfold higher on average than other transcripts. At three out of the four sites, SP21 transcript abundance increased with depth, while total mRNA abundance and richness decreased, indicating a shift in investment from metabolism and other cellular processes to build-up of spore protein SP21. The SP21 gene in MAGs was often flanked by genes involved in membrane-associated stress response. The ability of Woeseiales to shift from sulfur oxidation to nitrite reduction with burial into marine sediments with decreasing access to overlying oxic bottom waters, as well as enter into a dormant state dominated by SP21, may account for its ubiquity and high abundance in marine sediments worldwide, including those of the rapidly shifting Arctic.

microbiology↗

Anaerobic microbial degradation of protein and lipid macromolecules in subarctic marine sediment

Microorganisms in marine sediments play major roles in marine biogeochemical cycles by mineralizing substantial quantities of organic matter from decaying cells. Proteins and lipids are abundant components of necromass, yet microorganisms that degrade them remain understudied. Here, we revealed identities, trophic interactions and genomic features of microorganisms that degraded 13C-labelled proteins and lipids in cold anoxic microcosms with sulfidic subarctic marine sediment. Supplemented proteins and lipids were rapidly fermented to various volatile fatty acids within five days. DNA-stable isotope probing (SIP) suggested Psychrilyobacter atlanticus was an important primary degrader of proteins, and Psychromonas members were important primary degraders of both proteins and lipids. Closely related Psychromonas populations, as represented by distinct 16S rRNA gene variants, differentially utilized either proteins or lipids. DNA-SIP also showed 13C-labeling of various Deltaproteobacteria within ten days, indicating trophic transfer of carbon to putative sulfate-reducers. Metagenome-assembled genomes revealed the primary hydrolyzers encoded secreted peptidases or lipases, and enzymes for catabolism of protein or lipid degradation products. Psychromonas were prevalent in diverse marine sediments, suggesting they are important players in organic carbon processing in situ. Together, this study provides an improved understanding of the metabolic processes and functional partitioning of necromass macromolecules among microorganisms in the seafloor.

microbiology↗

Glacial runoff promotes deep burial of sulfur cycling-associated microorganisms in marine sediments

Marine fjords with active glacier outlets are hot spots for organic matter burial in the sediments and subsequent microbial mineralization, and will be increasingly important as climate warming causes more rapid glacial melt. Here, we investigated controls on microbial community assembly in sub-arctic glacier-influenced (GI) and non-glacier-influenced (NGI) marine sediments in the Godth[a]bsfjord region, south-western Greenland. We used a correlative approach integrating 16S rRNA gene and dissimilatory sulfite reductase (dsrB) amplicon sequence data over six meters of depth with biogeochemistry, sulfur-cycling activities, and sediment ages. GI sediments were characterized by comparably high sedimentation rates and had young sediment ages of <500 years even at 6 m sediment depth. In contrast, NGI stations reached ages of approximately 10,000 years at these depths. Sediment age-depth relationships, sulfate reduction rates, and C/N ratios were strongly correlated with differences in microbial community composition between GI and NGI sediments, indicating that age and diagenetic state were key drivers of microbial community assembly in subsurface sediments. Similar bacterial and archaeal communities were present in the surface sediments of all stations, whereas only in GI sediments were many surface taxa also abundant through the whole sediment core. The relative abundance of these taxa, including diverse Desulfobacteraceae members, correlated positively with sulfate reduction rates, indicating their active contributions to sulfur-cycling processes. In contrast, other surface community members, such as Desulfatiglans, Atribacteria and Chloroflexi, survived the slow sediment burial at NGI stations and dominated in the deepest sediment layers. These taxa are typical for the energy-limited marine deep biosphere and their relative abundances correlated positively with sediment age. In conclusion, our data suggests that high rates of sediment accumulation caused by glacier runoff and associated changes in biogeochemistry, promote persistence of sulfur-cycling activity and burial of a larger fraction of the surface microbial community into the deep subsurface.\n\nContribution to the Field StatementIn most coastal marine sediments organic matter turnover and total energy flux are highest at the surface and decrease significantly with increasing sediment depth, causing depth-dependent changes in the microbial community composition. Glacial runoff in arctic and subarctic fjords alters the composition of the microbial community at the surface, mainly due to different availabilities of organic matter and metals. Here we show that glacial runoff also modifies microbial community assembly with sediment depth. Sediment age was a key driver of microbial community composition in six-meter-long marine sediment cores from the Godth[a]bsfjord region, south-western Greenland. High sedimentation rates at glacier-influenced sediment stations enabled a complex community of sulfur-cycling-associated microorganisms to continuously thrive at high relative abundances from the surface into the sediment subsurface. These communities consisted of putative fermenters, sulfate reducers and sulfur oxidizers, which likely depended on high metal concentrations in the relatively young, glacier-influenced sediments. In non-glacier-influenced sediments with lower sedimentation rates, these sulfur-cycling-associated microorganisms were only present near the surface. With increasing sediment depth these surface microorganisms were largely replaced by other surface microorganisms that positively correlated with sediment age and belong to known taxa of the energy-limited, marine deep biosphere.

microbiology↗

DNA-foraging bacteria in the seafloor

Extracellular DNA is a major macromolecule in global element cycles, and is a particularly crucial phosphorus as well as nitrogen and carbon source for microorganisms in the seafloor. Nevertheless, the identities, ecophysiology and genetic features of key DNA-foraging microorganisms in marine sediments are completely unknown. Here we combined microcosm experiments, stable isotope probing and genome-centric metagenomics to study microbial catabolism of DNA and its sub-components in anoxic marine sediments. 13C-DNA added to sediment microcosms was degraded within ten days and mineralised to 13CO2. Stable isotope probing showed that diverse Candidatus Izemoplasma, Lutibacter, Shewanella, Fusibacteraceae and Nitrincolaceae incorporated DNA-derived 13C-carbon. Genomes representative of the 13C-labelled taxa were recovered and all encoded enzymatic repertoires for catabolism of DNA. Comparative genomics indicated that DNA can be digested by diverse members of the order Candidatus Izemoplasmatales (former Tenericutes), which appear to be specialised DNA-degraders that encode multiple extracellular nucleases. Fusibacteraceae lacked genes for extracellular nucleases but utilised various individual purine- and pyrimidine-based molecules, suggesting they cheated on liberated sub-components of DNA. Close relatives of the DNA-degrading taxa are globally distributed in marine sediments, suggesting that these poorly understood taxa contribute widely to the key ecosystem function of degrading and recycling DNA in the seabed.

microbiology↗

Diversity decoupled from sulfur isotope fractionation in a sulfate reducing microbial community

The extent of fractionation of sulfur isotopes by sulfate reducing microbes is dictated by genomic and environmental factors. A greater understanding of species-specific fractionations may better inform interpretation of sulfur isotopes preserved in the rock record. To examine whether gene diversity influences net isotopic fractionation in situ, we assessed environmental chemistry, sulfate reduction rates, diversity of putative sulfur metabolizing organisms by 16S rRNA and dissimilatory sulfite reductase (dsrB) gene amplicon sequencing, and net fractionation of sulfur isotopes along a sediment transect of a hypersaline Arctic spring. In situ sulfate reduction rates yielded minimum cell-specific sulfate reduction rates <0.3 x 10-15 moles cell-1 day-1. Neither 16S rRNA nor dsrB diversity indices correlated with relatively constant (38 to 45{per thousand}) net isotope fractionation ({varepsilon}34Ssulfide-sulfate). Measured {varepsilon}34S values could be reproduced in a mechanistic fractionation model if 1-2% of the microbial community (10-60% of Deltaproteobacteria) were engaged in sulfate respiration, indicating heterogeneous respiratory activity within sulfate-metabolizing populations. This model indicated enzymatic kinetic diversity of Apr was more likely to correlate with sulfur fractionation than DsrB. We propose that, above a threshold alpha diversity value, the influence of the specific composition of the microbial community responsible for generating an isotope signal is overprinted by the control exerted by environmental variables on microbial physiology.\n\nSubject categoriesO_LIIntegrated genomics and post-genomics approaches in microbial ecology\nC_LIO_LIMicrobial ecology and functional diversity of natural habitats\nC_LI

microbiology↗

Growth arrest in the active rare biosphere

Microbial diversity in the environment is mainly concealed within the rare biosphere, which is arbitrarily defined as all species with <0.1% relative abundance. While dormancy explains a low-abundance state very well, the cellular mechanisms leading to rare but active microorganisms are not clear. We used environmental systems biology to genomically and metabolically characterize a cosmopolitan sulfate reducer that is of low abundance but highly active in peat soil, where it contributes to counterbalance methane emissions. We obtained a 98%-complete genome of this low-abundance species, Candidatus Desulfosporosinus infrequens, by metagenomics. To test for environmentally relevant metabolic activity of Ca. D. infrequens, anoxic peat soil microcosms were incubated under diverse in situ-like conditions for 36 days and analyzed by metatranscriptomics. Compared to the no-substrate control, transcriptional activity of Ca. D. infrequens increased 56- to 188-fold in incubations with sulfate and acetate, propionate, lactate, or butyrate, revealing a versatile substrate use. Cellular activation was due to a significant overexpression of genes encoding ribosomal proteins, dissimilatory sulfate reduction, and carbon-degradation pathways, but not of genes encoding DNA or cell replication. We show for the first time that a rare biosphere member transcribes metabolic pathways relevant for carbon and sulfur cycling over prolonged time periods while being growth-arrested in its lag phase.\n\nSignificanceThe microbial rare biosphere represents the largest pool of biodiversity on Earth and constitutes, in sum of all its members, a considerable part of a habitats biomass. Dormancy or starvation are typically used to explain a low-abundance state. We show that low-abundance microorganisms can be highly metabolically active while being growth-arrested over prolonged time periods. We show that this is true for microbial keystone species, such as a cosmopolitan but low-abundance sulfate reducer in wetlands that is involved in counterbalancing greenhouse gas emission. Our results challenge the central dogmas \"metabolic activity translates directly into growth\" as well as \"low abundance equals little ecosystem impact\" and provide an important step forward in understanding rare biosphere members relevant for ecosystem functions.

microbiology↗

Peatland Acidobacteria with a dissimilatory sulfur metabolism

Sulfur-cycling microorganisms impact organic matter decomposition in wetlands and consequently greenhouse gas emissions from these globally relevant environments. However,their identities and physiological properties are largely unknown. By applying a functional metagenomics approach to an acidic peatland, we recovered draft genomes of seven novel Acidobacteria species with the potential for dissimilatory sulfite (dsrAB, dsrC, dsrD, dsrN, dsrT, dsrMKJOP) or sulfate respiration (sat, aprBA, qmoABC plus dsr genes). Surprisingly, the genomes also encoded dsrL, a unique gene of the sulfur oxidation pathway. Metatranscriptome analysis demonstrated expression of acidobacterial sulfur-metabolism genes in native peat soil and their upregulation in diverse anoxic microcosms. This indicated an active sulfate respiration pathway, which, however, could also operate in reverse for sulfur oxidation as recently shown for other microorganisms. Acidobacteria that only harbored genes for sulfite reduction additionally encoded enzymes that liberate sulfite from organosulfonates, which suggested organic sulfur compounds as complementary energy sources. Further metabolic potentials included polysaccharide hydrolysis and sugar utilization, aerobic respiration, several fermentative capabilities, and hydrogen oxidation. Our findings extend both, the known physiological and genetic properties of Acidobacteria and the known taxonomic diversity of microorganisms with a DsrAB-based sulfur metabolism, and highlight new fundamental niches for facultative anaerobic Acidobacteria in wetlands based on exploitation of inorganic and organic sulfur molecules for energy conservation.

microbiology↗