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Hausmann, B.

Publications and source records attributed to Hausmann, B..

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↗

Symbiont diversity within Loripes orbiculatus and the case for multiple hosts

Seagrasses support immense biodiversity and are critical for maintaining coastal ecosystem health. These foundation species benefit from a three-way facultative relationship with one of the common inhabitants of seagrass meadows, lucinid bivalves, which host specific bacterial Ca. Thiodiazotropha symbionts. Relatives of the bivalve symbionts have been detected on seagrass roots raising the possibility that these symbionts may colonize both animals and plants; however, no study has yet compared bivalve- and seagrass-associated symbionts at the same site and time. Our combination of 16S rRNA amplicon and metagenome sequencing revealed a greater diversity than was previously observed within both lucinid bivalves and on seagrass roots from the Adriatic Sea. We show that two of the Ca. Thiodiazotropha ASVs found on seagrass roots are identical to those found in bivalve hosts at the same site. This suggests that symbiont sharing may occur in the seagrass habitat between these two species, which has important evolutionary and ecological implications for both hosts and symbionts, as well as thin response to climate change.

microbiology↗

Model substrate particles uncover dynamics of microbial communities associated with particulate organic matter decomposition in soil

Soil organic matter is the largest terrestrial reservoir of organic carbon. Its particulate fraction, particulate organic matter (POM), serves as a resource and surface for microbial colonization. Degradation of complex biopolymers like cellulose and chitin requires extracellular enzymes produced by phylogenetically diverse microbes. Despite their importance for carbon cycling, the structure and spatio-temporal dynamics of POM-associated microbial communities in soil and how specific substrates influence them remain poorly understood. This study investigated whether microbial communities associated with POM change in composition and richness over time and whether chitin and cellulose select for distinct fungal and bacterial taxa. We incubated self-manufactured, millimetre-sized model substrate particles containing chitin or cellulose in soil under laboratory and field conditions. We assessed particle-associated communities at multiple time points over a 50-day-long incubation in the lab and after 47 days in the field. Our results show that community structure and temporal dynamics of particle-associated microbial communities were substrate-specific. While microbial biomass increased on both particle types, chitin-associated microbial communities exhibited stronger temporal changes. Communities on chitin and cellulose particles were enriched in specific bacterial and fungal genera compared to communities in the surrounding soil. We demonstrate that microbial communities associated with model chitin particles underwent notable temporal changes, including decreased microbial richness and shifts in community composition over the incubation period. This study shows the potential of model particles to advance our understanding of particle- and substrate-associated microbial communities in soil.

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↗

Edited Filamin A in myeloid cells reduces intestinal inflammation and protects from colitis

Patho-mechanistic origins and disease dynamics of ulcerative colitis are still poorly understood. The actin-crosslinker Filamin A (FLNA) impacts cellular responses through interaction with cytosolic proteins. FLNA exists in two forms that differ only in one amino acid: genome-encoded FLNAQ and FLNAR - generated by post-transcriptional A-to-I editing. FLNA is edited in fibroblasts, smooth muscle- and endothelial cells in the colon. We identified the FLNA editing status as a key determinant of colitis severity. FLNA editing was highest in healthy colons and reduced during acute murine and human colitis. Mice that exclusively express edited FLNAR and do not downregulate editing upon challenge were highly resistant to DSS-induced colitis, whereas fully unedited FLNAQ animals developed severe inflammation. While the genetic induction of FLNA editing influenced transcriptional states of structural cells and the microbiome composition, we found that FLNAR exerts protection specifically via its influence on myeloid cells, which are not edited under physiological conditions. Introducing fixed, fully edited FLNAR did not hamper normal cell migration but reduced macrophage inflammation and rendered neutrophils less prone to NETosis. In conclusion, loss of FLNA editing correlates with colitis severity, and targeted FLNA editing of myeloid cells might serve as a novel therapeutic approach in intestinal inflammation. SummaryIn this study, Gawish et al. show that RNA editing of the actin cross-linker FLNA is similarly regulated in mice and humans and that the targeted induction of edited FLNAR in myeloid cells governs resistance to DSS-induced colitis, revealing its potential in IBD therapy.

molecular 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↗

Human-derived microRNA 21 regulates indole and L-tryptophan biosynthesis transcripts in a prominent gut symbiont

In the gut, microRNAs (miRNAs) produced by intestinal epithelial cells are secreted into the lumen and can shape the composition and function of the gut microbiome. Crosstalk between gut microbes and the host plays a key role in irritable bowel syndrome (IBS) and inflammatory bowel diseases, yet little is known about how the miRNA-gut microbiome axis contributes to the pathogenesis of these conditions. In this study, we aimed to explore the ability of miR-21, a miRNA that we found decreased in stool samples from IBS patients, to associate with and regulate gut microbiome function. Incubation of human faecal microbiota with miR-21 revealed a rapid association with microbial cells, reproducible across multiple donor samples. Fluorescence-activated cell sorting and sequencing of microbial cells incubated with fluorescently-labelled miR-21 identified organisms belonging to the genera Bacteroides, Limosilactobacillus, Ruminococcus, or Coprococcus which predominantly interacted with miR-21. Surprisingly, these and other genera also interacted with a miRNA scramble control, suggesting that physical interaction and/or uptake of these miRNAs by gut microbiota is not sequence-dependent. Nevertheless, transcriptomic analysis of the gut commensal Bacteroides thetaiotaomicron revealed a miRNA sequence-specific effect on bacterial transcript levels. Supplementation of miR-21, but not of small RNA controls resulted in significantly altered levels of many cellular transcripts and increased transcription of a biosynthetic operon for indole and L-tryptophan, metabolites known to regulate host inflammation and colonic motility. Our study identifies a novel putative miR-21-dependent pathway of regulation of intestinal function through the gut microbiome with implications for gastrointestinal conditions.

microbiology↗

Shewanella is a putative producer of polyunsaturated fatty acids in the gut soil of the composting earthworm Eisenia fetida

Withdrawal StatementThe authors have withdrawn this manuscript owing to a duplicate posting of manuscript number BIORXIV/2024/587473. Therefore, the authors do not wish this work to be cited as reference for the project. If you have any questions, please contact the corresponding author. The correct preprint can be found at doi.org/10.1101/2024.03.31.587473.

microbiology↗

Shewanella is a putative producer of polyunsaturated fatty acids in the gut soil of the composting earthworm Eisenia fetida

Polyunsaturated fatty acids (PUFAs) play a crucial role in aiding bacteria to adapt to extreme and stressful environments. While there is a well-established understanding of their production, accrual, and transfer within marine ecosystems, knowledge about terrestrial environments remains limited. Investigation of the intestinal microbiome of earthworms has illuminated the presence of PUFAs presumably of microbial origin, which contrasts with the surrounding soil. To comprehensively study this phenomenon, a multi-faceted approach was employed, combining fatty acid analysis with amplicon sequencing of the PfaA-KS domain of the anaerobic fatty acid synthase gene (pfa), as well as the 16S rRNA and 18S rRNA genes. This methodology was applied to scrutinize the gut microbiome of Eisenia fetida, its compost-based dietary source, and the resultant castings. This study unveiled a distinct gut soil ecosystem from input compost and output castings in fatty acid profile as well as type and abundance of organisms. 16S sequencing provided insights into the microbial composition, showing increased relative abundance of certain Pseudomonadota, including Shewanellaceae, and Planctomycetota, including Gemmataceae within the gut microbiome compared to input bulk soil compost, while Actinomycetota and Bacillota were relatively enriched compared to the casted feces. Sequencing of the PfaA-KS domain revealed ASVs belonging primarily to Shewanella. Intriguingly, the 20C PUFAs were identified only in gut-soil samples, though PfaA-KS sequence abundance was highest in output castings, indicating a unique metabolism occurring only in the gut. Overall, the results indicate that Shewanella can explain PUFA enrichment in the gut environment because of pfa gene presence detected via PfaA-KS sequence data. ImportancePrior research has demonstrated that earthworm microbiomes can potentially harbor PUFAs that are not found within their residing soil environment. Moreover, distinct indicator species have been pinpointed for various microbial genera in earthworm microbiomes. Nevertheless, none of these studies have integrated metataxonomic and fatty acid analysis to explore the origin of PUFA synthesis in any earthworm species, with the objective of identifying the specific organisms and locations responsible for this production. This study suggests that earthworms accumulate PUFAs produced from bacteria, especially Shewanella, activated through the gut ecosystem.

microbiology↗

Novel nitrifying symbiont lineages are vertically inherited and widespread in marine sponges

Ammonia-oxidising archaea and nitrite-oxidising bacteria are common members of marine sponge microbiomes. They derive energy for carbon fixation and growth from nitrification - the oxidation of ammonia to nitrite and further to nitrate - and are proposed to play essential roles in the carbon and nitrogen cycling of sponge holobionts. In this study, we characterise two novel nitrifying symbiont lineages, Ca. Nitrosokoinonia and Ca. Nitrosymbion in the marine sponge Coscinoderma matthewsi using a combination of molecular tools, single-cell imaging techniques, and physiological rate measurements. Both represent a new genus in the ammonia-oxidising archaeal class Nitrososphaeria and the nitrite-oxidising bacterial order Nitrospirales, respectively. Furthermore, we show that larvae of this viviparous sponge are densely colonised by representatives of Ca. Nitrosokoinonia and Ca. Nitrosymbion indicating vertical transmission. In adults, the representatives of both symbiont genera are located extracellularly in the mesohyl. Comparative metagenome analyses and physiological data suggest that ammonia-oxidising archaeal symbionts of the genus Ca. Nitrosokoinonia strongly rely on endogenously produced nitrogenous compounds (i.e., ammonium, urea, nitriles/cyanides, and creatinine) rather than on exogenous ammonium sources taken up by the sponge. Additionally, the nitrite-oxidising bacterial symbionts Ca. Nitrosymbion may reciprocally support the ammonia-oxidisers with ammonia via the utilisation of sponge-derived urea and cyanate. Interestingly, comparative analyses of published environmental 16S rRNA amplicon data revealed that Ca. Nitrosokoinonia and Ca. Nitrosymbion are widely distributed and predominantly associated with marine sponges and corals, suggesting a broad relevance of our findings.

microbiology↗

The Parkinson's drug entacapone disrupts gut microbiome homeostasis via iron sequestration

Increasing evidence shows that many human-targeted drugs alter the gut microbiome, leading to implications for host health. However, much less is known about the mechanisms by which drugs target the microbiome and how drugs affect microbial function. Here we combined quantitative microbiome profiling, long-read metagenomics, stable isotope probing and single cell chemical imaging to investigate the impact of two widely prescribed nervous system targeted drugs on the gut microbiome. Ex vivo supplementation of physiologically relevant concentrations of entacapone or loxapine succinate to faecal samples significantly impacted the abundance of up to one third of the microbial species present. Importantly, we demonstrate that the impact of these drugs on microbial metabolism is much more pronounced than their impact on abundances, with low concentrations of drugs reducing the activity, but not the abundance of key microbiome members like Bacteroides, Ruminococcus or Clostridium species. We further demonstrate that entacapone impacts the microbiome due to its ability to complex and deplete available iron, and that microbial growth can be rescued by replenishing levels of microbiota-accessible iron. Remarkably, entacapone-induced iron starvation selected for iron-scavenging organisms carrying antimicrobial resistance and virulence genes. Collectively, our study unveils the impact of two under-investigated drugs on whole microbiomes and identifies metal sequestration as a mechanism of drug-induced microbiome disturbance.

microbiology↗

Global abundance patterns, diversity, and ecology of Patescibacteria in wastewater treatment plants

BackgroundMicroorganisms are responsible for nutrient removal and resource recovery in wastewater treatment plants (WWTPs), and their diversity is often studied by 16S rRNA gene amplicon sequencing. However, this approach underestimates the abundance and diversity of Patescibacteria due to the low coverage of commonly used PCR primers for this highly divergent bacterial phylum. Therefore, our current understanding of the global diversity, distribution, and ecological role of Patescibacteria in WWTPs is very incomplete. This is particularly relevant as Patescibacteria are considered to be associated with microbial host cells and can therefore influence the abundance and temporal variability of other microbial groups that are important for WWTP functioning. ResultsHere, we evaluated the in silico coverage of widely used 16S rRNA gene-targeted primer pairs and redesigned a primer pair targeting the V4 region of bacterial and archaeal 16S rRNA genes to expand its coverage for Patescibacteria. We then experimentally evaluated and compared the performance of the original and modified V4-targeted primers on 565 WWTP samples from the MiDAS global sample collection. Using the modified primer pair, the percentage of ASVs classified as Patescibacteria increased from 5.9% to 23.8%, and the number of detected patescibacterial genera increased from 560 to 1,576, while the detected diversity of the remaining microbial community remained similar. Due to this significantly improved coverage of Patescibacteria, we identified 23 core genera of Patescibacteria in WWTPs and described the global distribution pattern of these unusual microbes in these systems. Finally, correlation network analysis revealed potential host organisms that might be associated with Patescibacteria in WWTPs. Interestingly, strong indications were found for an association between Patescibacteria of the Saccharimonadia and globally abundant polyphosphate-accumulating organisms of the genus Ca. Phosporibacter. ConclusionsOur study (i) provides an improved 16S rRNA gene V4 region-targeted amplicon primer pair inclusive of Patescibacteria with little impact on the detection of other taxa, (ii) reveals the diversity and distribution patterns of Patescibacteria in WWTPs on a global scale, and (iii) provides new insights into the ecological role and potential hosts of Patescibacteria in WWTPs.

ecology↗

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↗

Gut microbiome signatures of Yorkshire Terrier Enteropathy during disease and remission.

The role of the gut microbiome in developing Inflammatory Bowel Disease (IBD) in humans and dogs has received attention in recent years. Evidence suggests that IBD is associated with alterations in gut microbial composition, but further research is needed in veterinary medicine. The impact of IBD treatment on the gut microbiome needs to be better understood, especially in a breed-specific form of IBD in Yorkshire Terriers known as Yorkshire Terrier Enteropathy (YTE). This study aimed to investigate the difference in gut microbiome composition between YTE dogs during disease and remission and healthy Yorkshire Terriers. Our results showed a significant increase in specific taxa such as Clostridium sensu stricto 1, Escherichia-Shigella, and Streptococcus, and a decrease in Bacteroides, Prevotella, Alloprevotella, and Phascolarctobacterium in YTE dogs compared to healthy controls. No significant difference was found between the microbiome of dogs in remission and those with active disease, suggesting that the gut microbiome is affected beyond clinical recovery.

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↗

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↗

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↗