Publications by authors named "Alexander Loy"

98 Publications

Genomic insights into diverse bacterial taxa that degrade extracellular DNA in marine sediments.

Nat Microbiol 2021 Jun 14. Epub 2021 Jun 14.

Division of Microbial Ecology, Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria.

Extracellular DNA is a major macromolecule in global element cycles, and is a particularly crucial phosphorus, nitrogen and carbon source for microorganisms in the seafloor. Nevertheless, the identities, ecophysiology and genetic features of DNA-foraging microorganisms in marine sediments are largely unknown. Here, we combined microcosm experiments, DNA stable isotope probing (SIP), single-cell SIP using nano-scale secondary isotope mass spectrometry (NanoSIMS) and genome-centric metagenomics to study microbial catabolism of DNA and its subcomponents in marine sediments. C-DNA added to sediment microcosms was largely degraded within 10 d and mineralized to CO. SIP probing of DNA revealed diverse 'Candidatus Izemoplasma', Lutibacter, Shewanella and Fusibacteraceae incorporated DNA-derived C-carbon. NanoSIMS confirmed incorporation of C into individual bacterial cells of Fusibacteraceae sorted from microcosms. Genomes of the C-labelled taxa all encoded enzymatic repertoires for catabolism of DNA or subcomponents of DNA. Comparative genomics indicated that diverse 'Candidatus Izemoplasmatales' (former Tenericutes) are exceptional because they encode multiple (up to five) predicted extracellular nucleases and are probably specialized DNA-degraders. Analyses of additional sediment metagenomes revealed extracellular nuclease genes are prevalent among Bacteroidota at diverse sites. Together, our results reveal the identities and functional properties of microorganisms that may contribute to the key ecosystem function of degrading and recycling DNA in the seabed.
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http://dx.doi.org/10.1038/s41564-021-00917-9DOI Listing
June 2021

An Economical and Flexible Dual Barcoding, Two-Step PCR Approach for Highly Multiplexed Amplicon Sequencing.

Front Microbiol 2021 20;12:669776. Epub 2021 May 20.

Joint Microbiome Facility of the Medical University of Vienna and the University of Vienna, Vienna, Austria.

In microbiome research, phylogenetic and functional marker gene amplicon sequencing is the most commonly-used community profiling approach. Consequently, a plethora of protocols for the preparation and multiplexing of samples for amplicon sequencing have been developed. Here, we present two economical high-throughput gene amplification and sequencing workflows that are implemented as standard operating procedures at the Joint Microbiome Facility of the Medical University of Vienna and the University of Vienna. These workflows are based on a previously-published two-step PCR approach, but have been updated to either increase the accuracy of results, or alternatively to achieve orders of magnitude higher numbers of samples to be multiplexed in a single sequencing run. The high-accuracy workflow relies on unique dual sample barcoding. It allows the same level of sample multiplexing as the previously-published two-step PCR approach, but effectively eliminates residual read missasignments between samples (crosstalk) which are inherent to single barcoding approaches. The high-multiplexing workflow is based on combinatorial dual sample barcoding, which theoretically allows for multiplexing up to 299,756 amplicon libraries of the same target gene in a single massively-parallelized amplicon sequencing run. Both workflows presented here are highly economical, easy to implement, and can, without significant modifications or cost, be applied to any target gene of interest.
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http://dx.doi.org/10.3389/fmicb.2021.669776DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8173057PMC
May 2021

Novel taxa of Acidobacteriota implicated in seafloor sulfur cycling.

ISME J 2021 May 12. Epub 2021 May 12.

Division of Microbial Ecology, Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria.

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. Meta-analysis of dsrAB datasets also showed Acidobacteriota dsrAB sequences are prominent in marine sediments worldwide, averaging 15% of all sequences analysed, and represent most of the previously unclassified dsrAB in marine sediments. We propose two new Acidobacteriota genera, Candidatus Sulfomarinibacter (class Thermoanaerobaculia, "subdivision 23") and Ca. Polarisedimenticola ("subdivision 22"), with distinct genetic properties that may explain their distributions in biogeochemically distinct sediments. Ca. Sulfomarinibacter encode 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 various enzymes to degrade proteins, and to reduce oxygen, nitrate, sulfur/polysulfide and metal-oxides. 16S rRNA gene and transcript profiling of Svalbard sediments 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.
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http://dx.doi.org/10.1038/s41396-021-00992-0DOI Listing
May 2021

Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut.

ISME J 2021 Mar 31. Epub 2021 Mar 31.

Division of Microbial Ecology, Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria.

Responses of the microbiota to diet are highly personalized but mechanistically not well understood because many metabolic capabilities and interactions of human gut microorganisms are unknown. Here we show that sulfoquinovose (SQ), a sulfonated monosaccharide omnipresent in green vegetables, is a selective yet relevant substrate for few but ubiquitous bacteria in the human gut. In human feces and in defined co-culture, Eubacterium rectale and Bilophila wadsworthia used recently identified pathways to cooperatively catabolize SQ with 2,3-dihydroxypropane-1-sulfonate as a transient intermediate to hydrogen sulfide (HS), a key intestinal metabolite with disparate effects on host health. SQ-degradation capability is encoded in almost half of E. rectale genomes but otherwise sparsely distributed among microbial species in the human intestine. However, re-analysis of fecal metatranscriptome datasets of four human cohorts showed that SQ degradation (mostly from E. rectale and Faecalibacterium prausnitzii) and HS production (mostly from B. wadsworthia) pathways were expressed abundantly across various health states, demonstrating that these microbial functions are core attributes of the human gut. The discovery of green-diet-derived SQ as an exclusive microbial nutrient and an additional source of HS in the human gut highlights the role of individual dietary compounds and organosulfur metabolism on microbial activity and has implications for precision editing of the gut microbiota by dietary and prebiotic interventions.
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http://dx.doi.org/10.1038/s41396-021-00968-0DOI Listing
March 2021

Anaerobic bacterial degradation of protein and lipid macromolecules in subarctic marine sediment.

ISME J 2021 03 18;15(3):833-847. Epub 2020 Nov 18.

Division of Microbial Ecology, Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria.

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 the taxonomic identities of microorganisms that actively degrade them remain poorly resolved. Here, we revealed identities, trophic interactions, and genomic features of bacteria that degraded C-labeled proteins and lipids in cold anoxic microcosms containing sulfidic subarctic marine sediment. Supplemented proteins and lipids were rapidly fermented to various volatile fatty acids within 5 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 C-labeling of various Deltaproteobacteria within 10 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 species are prevalent in diverse marine sediments, suggesting they are important players in organic carbon processing in situ. Together, this study provides new insights into the identities, functions, and genomes of bacteria that actively degrade abundant necromass macromolecules in the seafloor.
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http://dx.doi.org/10.1038/s41396-020-00817-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8027456PMC
March 2021

Proposal to reclassify the proteobacterial classes and , and the phylum into four phyla reflecting major functional capabilities.

Int J Syst Evol Microbiol 2020 Nov 5;70(11):5972-6016. Epub 2020 Nov 5.

Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD, Australia.

The class comprises an ecologically and metabolically diverse group of bacteria best known for dissimilatory sulphate reduction and predatory behaviour. Although this lineage is the fourth described class of the phylum , it rarely affiliates with other proteobacterial classes and is frequently not recovered as a monophyletic unit in phylogenetic analyses. Indeed, one branch of the class encompassing like predators was recently reclassified into a separate proteobacterial class, the . Here we systematically explore the phylogeny of taxa currently assigned to these classes using 120 conserved single-copy marker genes as well as rRNA genes. The overwhelming majority of markers reject the inclusion of the classes and in the phylum . Instead, the great majority of currently recognized members of the class are better classified into four novel phylum-level lineages. We propose the names phyl. nov. and phyl. nov. for two of these phyla, based on the oldest validly published names in each lineage, and retain the placeholder name SAR324 for the third phylum pending formal description of type material. Members of the class represent a separate phylum for which we propose the name phyl. nov. based on priority in the literature and general recognition of the genus phyl. nov. includes the taxa previously classified in the phylum , and these reclassifications imply that the ability of sulphate reduction was vertically inherited in the rather than laterally acquired as previously inferred. Our analysis also indicates the independent acquisition of predatory behaviour in the phyla and , which is consistent with their distinct modes of action. This work represents a stable reclassification of one of the most taxonomically challenging areas of the bacterial tree and provides a robust framework for future ecological and systematic studies.
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http://dx.doi.org/10.1099/ijsem.0.004213DOI Listing
November 2020

Environmental and Intestinal Phylum Firmicutes Bacteria Metabolize the Plant Sugar Sulfoquinovose via a 6-Deoxy-6-sulfofructose Transaldolase Pathway.

iScience 2020 Aug 28;23(9):101510. Epub 2020 Aug 28.

Department of Biology, University of Konstanz, 78457 Konstanz, Germany; Konstanz Research School Chemical Biology (KoRS-CB), University of Konstanz, 78457 Konstanz, Germany. Electronic address:

Bacterial degradation of the sugar sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose) produced by plants, algae, and cyanobacteria, is an important component of the biogeochemical carbon and sulfur cycles. Here, we reveal a third biochemical pathway for primary SQ degradation in an aerobic Bacillus aryabhattai strain. An isomerase converts SQ to 6-deoxy-6-sulfofructose (SF). A novel transaldolase enzyme cleaves the SF to 3-sulfolactaldehyde (SLA), while the non-sulfonated C-(glycerone)-moiety is transferred to an acceptor molecule, glyceraldehyde phosphate (GAP), yielding fructose-6-phosphate (F6P). Intestinal anaerobic bacteria such as Enterococcus gilvus, Clostridium symbiosum, and Eubacterium rectale strains also express transaldolase pathway gene clusters during fermentative growth with SQ. The now three known biochemical strategies for SQ catabolism reflect adaptations to the aerobic or anaerobic lifestyle of the different bacteria. The occurrence of these pathways in intestinal (family) Enterobacteriaceae and (phylum) Firmicutes strains further highlights a potential importance of metabolism of green-diet SQ by gut microbial communities to, ultimately, hydrogen sulfide.
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http://dx.doi.org/10.1016/j.isci.2020.101510DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7491151PMC
August 2020

Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment.

PLoS One 2020 27;15(8):e0234839. Epub 2020 Aug 27.

Department of Microbiology, University of Tennessee, Knoxville, Tennessee, United States of America.

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°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.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0234839PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7451513PMC
October 2020

Microbiome definition re-visited: old concepts and new challenges.

Microbiome 2020 06 30;8(1):103. Epub 2020 Jun 30.

Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW, Australia.

The field of microbiome research has evolved rapidly over the past few decades and has become a topic of great scientific and public interest. As a result of this rapid growth in interest covering different fields, we are lacking a clear commonly agreed definition of the term "microbiome." Moreover, a consensus on best practices in microbiome research is missing. Recently, a panel of international experts discussed the current gaps in the frame of the European-funded MicrobiomeSupport project. The meeting brought together about 40 leaders from diverse microbiome areas, while more than a hundred experts from all over the world took part in an online survey accompanying the workshop. This article excerpts the outcomes of the workshop and the corresponding online survey embedded in a short historical introduction and future outlook. We propose a definition of microbiome based on the compact, clear, and comprehensive description of the term provided by Whipps et al. in 1988, amended with a set of novel recommendations considering the latest technological developments and research findings. We clearly separate the terms microbiome and microbiota and provide a comprehensive discussion considering the composition of microbiota, the heterogeneity and dynamics of microbiomes in time and space, the stability and resilience of microbial networks, the definition of core microbiomes, and functionally relevant keystone species as well as co-evolutionary principles of microbe-host and inter-species interactions within the microbiome. These broad definitions together with the suggested unifying concepts will help to improve standardization of microbiome studies in the future, and could be the starting point for an integrated assessment of data resulting in a more rapid transfer of knowledge from basic science into practice. Furthermore, microbiome standards are important for solving new challenges associated with anthropogenic-driven changes in the field of planetary health, for which the understanding of microbiomes might play a key role. Video Abstract.
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http://dx.doi.org/10.1186/s40168-020-00875-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7329523PMC
June 2020

Hair eruption initiates and commensal skin microbiota aggravate adverse events of anti-EGFR therapy.

Sci Transl Med 2019 12;11(522)

Institute of Cancer Research, Department of Medicine I, Medical University of Vienna and Comprehensive Cancer Center, Vienna 1090, Austria.

Epidermal growth factor receptor (EGFR)-targeted anticancer therapy induces stigmatizing skin toxicities affecting patients' quality of life and therapy adherence. The lack of mechanistic details underlying these adverse events hampers their management. We found that EGFR/ERK signaling is required in LRIG1-positive stem cells during de novo hair eruption to secure barrier integrity and prevent the invasion of commensal microbiota and inflammatory skin disease. EGFR-deficient epidermis is permissive for microbiota outgrowth and displays an atopic-like T2-dominated signature. The opening of the follicular ostia during hair eruption allows invasion of commensal microbiota into the hair follicle, initiating an additional T1 and T17 response culminating in chronic folliculitis. Restoration of epidermal ERK signaling via prophylactic FGF7 treatment or transgenic SOS expression rescues the barrier defect in the absence of EGFR, highlighting a therapeutic anchor point. These data reveal that commensal skin microbiota provoke atopic-like inflammatory skin diseases by invading into the follicular opening of erupting hair.
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http://dx.doi.org/10.1126/scitranslmed.aax2693DOI Listing
December 2019

Glacial Runoff Promotes Deep Burial of Sulfur Cycling-Associated Microorganisms in Marine Sediments.

Front Microbiol 2019 7;10:2558. Epub 2019 Nov 7.

Division of Microbial Ecology, Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria.

Marine fjords with active glacier outlets are hot spots for organic matter burial in the sediments and subsequent microbial mineralization. Here, we investigated controls on microbial community assembly in sub-arctic glacier-influenced (GI) and non-glacier-influenced (NGI) marine sediments in the Godthåbsfjord region, south-western Greenland. We used a correlative approach integrating 16S rRNA gene and dissimilatory sulfite reductase () 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 (SRR), 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 members, correlated positively with SRRs, indicating their active contributions to sulfur-cycling processes. In contrast, other surface community members, such as , , and , 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.
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http://dx.doi.org/10.3389/fmicb.2019.02558DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6853847PMC
November 2019

A fiber-deprived diet disturbs the fine-scale spatial architecture of the murine colon microbiome.

Nat Commun 2019 09 25;10(1):4366. Epub 2019 Sep 25.

Centre for Microbiology and Environmental Systems Science, Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria.

Compartmentalization of the gut microbiota is thought to be important to system function, but the extent of spatial organization in the gut ecosystem remains poorly understood. Here, we profile the murine colonic microbiota along longitudinal and lateral axes using laser capture microdissection. We found fine-scale spatial structuring of the microbiota marked by gradients in composition and diversity along the length of the colon. Privation of fiber reduces the diversity of the microbiota and disrupts longitudinal and lateral gradients in microbiota composition. Both mucus-adjacent and luminal communities are influenced by the absence of dietary fiber, with the loss of a characteristic distal colon microbiota and a reduction in the mucosa-adjacent community, concomitant with depletion of the mucus layer. These results indicate that diet has not only global but also local effects on the composition of the gut microbiota, which may affect function and resilience differently depending on location.
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http://dx.doi.org/10.1038/s41467-019-12413-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6761162PMC
September 2019

Draft Genome Sequence of Desulfosporosinus fructosivorans Strain 63.6F, Isolated from Marine Sediment in the Baltic Sea.

Microbiol Resour Announc 2019 Aug 1;8(31). Epub 2019 Aug 1.

Centre for Microbiology and Environmental Systems Science, Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Vienna, Austria.

strain 63.6F is a strictly anaerobic, spore-forming, sulfate-reducing bacterium isolated from marine sediment in the Baltic Sea. Here, we report the draft genome sequence of 63.6F.
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http://dx.doi.org/10.1128/MRA.00427-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6675983PMC
August 2019

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

Geobiology 2019 11 21;17(6):660-675. Epub 2019 Jul 21.

Department of Geological Sciences, University of Colorado, Boulder, CO, USA.

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 × 10 moles cell  day . Neither 16S rRNA nor dsrB diversity indices correlated with relatively constant (38‰-45‰) net isotope fractionation (ε S ). Measured ε S 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-reducing 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 Shannon diversity value of 0.8 for dsrB, 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.
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http://dx.doi.org/10.1111/gbi.12356DOI Listing
November 2019

Draft Genome Sequence of sp. Strain Sb-LF, Isolated from an Acidic Peatland in Germany.

Microbiol Resour Announc 2019 Jul 18;8(29). Epub 2019 Jul 18.

Centre for Microbiology and Environmental Systems Science, Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Vienna, Austria.

sp. strain Sb-LF was isolated from an acidic peatland in Bavaria, Germany. Here, we report the draft genome sequence of the sulfate-reducing and lactate-utilizing strain Sb-LF.
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http://dx.doi.org/10.1128/MRA.00428-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6639609PMC
July 2019

Mucispirillum schaedleri Antagonizes Salmonella Virulence to Protect Mice against Colitis.

Cell Host Microbe 2019 05 18;25(5):681-694.e8. Epub 2019 Apr 18.

Max-von-Pettenkofer Institute, LMU Munich, Pettenkoferstr. 9a, 80336 Munich, Germany; German Center for Infection Research (DZIF), partner site LMU Munich, 80336 Munich, Germany. Electronic address:

The microbiota and the gastrointestinal mucus layer play a pivotal role in protection against non-typhoidal Salmonella enterica serovar Typhimurium (S. Tm) colitis. Here, we analyzed the course of Salmonella colitis in mice lacking a functional mucus layer in the gut. Unexpectedly, in contrast to mucus-proficient littermates, genetically deficient mice were protected against Salmonella-induced gut inflammation in the streptomycin colitis model. This correlated with microbiota alterations and enrichment of the bacterial phylum Deferribacteres. Using gnotobiotic mice associated with defined bacterial consortia, we causally linked Mucispirillum schaedleri, currently the sole known representative of Deferribacteres present in the mammalian microbiota, to host protection against S. Tm colitis. Inhibition by M. schaedleri involves interference with S. Tm invasion gene expression, partly by competing for anaerobic electron acceptors. In conclusion, this study establishes M. schaedleri, a core member of the murine gut microbiota, as a key antagonist of S. Tm virulence in the gut.
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http://dx.doi.org/10.1016/j.chom.2019.03.004DOI Listing
May 2019

Historical Factors Associated With Past Environments Influence the Biogeography of Thermophilic Endospores in Arctic Marine Sediments.

Front Microbiol 2019 28;10:245. Epub 2019 Feb 28.

School of Civil Engineering and Geosciences, Newcastle University, Newcastle upon Tyne, United Kingdom.

Selection by the local, contemporary environment plays a prominent role in shaping the biogeography of microbes. However, the importance of historical factors in microbial biogeography is more debatable. Historical factors include past ecological and evolutionary circumstances that may have influenced present-day microbial diversity, such as dispersal and past environmental conditions. Diverse thermophilic sulfate-reducing are present as dormant endospores in marine sediments worldwide where temperatures are too low to support their growth. Therefore, they are dispersed to here from elsewhere, presumably a hot, anoxic habitat. While dispersal through ocean currents must influence their distribution in cold marine sediments, it is not clear whether even earlier historical factors, related to the source habitat where these organisms were once active, also have an effect. We investigated whether these historical factors may have influenced the diversity and distribution of thermophilic endospores by comparing their diversity in 10 Arctic fjord surface sediments. Although community composition varied spatially, clear biogeographic patterns were only evident at a high level of taxonomic resolution (>97% sequence similarity of the 16S rRNA gene) achieved with oligotyping. In particular, the diversity and distribution of oligotypes differed for the two most prominent OTUs (defined using a standard 97% similarity cutoff). One OTU was dominated by a single ubiquitous oligotype, while the other OTU consisted of ten more spatially localized oligotypes that decreased in compositional similarity with geographic distance. These patterns are consistent with differences in historical factors that occurred when and where the taxa were once active, prior to sporulation. Further, the influence of history on biogeographic patterns was only revealed by analyzing microdiversity within OTUs, suggesting that populations within standard OTU-level groupings do not necessarily share a common ecological and evolutionary history.
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http://dx.doi.org/10.3389/fmicb.2019.00245DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6403435PMC
February 2019

Long-Term Transcriptional Activity at Zero Growth of a Cosmopolitan Rare Biosphere Member.

mBio 2019 02 12;10(1). Epub 2019 Feb 12.

Department of Biology, University of Konstanz, Konstanz, Germany

Microbial diversity in the environment is mainly concealed within the rare biosphere (all species with <0.1% relative abundance). While dormancy explains a low-abundance state very well, the mechanisms leading to rare but active microorganisms remain elusive. We used environmental systems biology to genomically and transcriptionally characterize " Desulfosporosinus infrequens," a low-abundance sulfate-reducing microorganism cosmopolitan to freshwater wetlands, where it contributes to cryptic sulfur cycling. We obtained its near-complete genome by metagenomics of acidic peat soil. In addition, we analyzed anoxic peat soil incubated under -like conditions for 50 days by -targeted qPCR and metatranscriptomics. The population stayed at a constant low abundance under all incubation conditions, averaging 1.2 × 10 16S rRNA gene copies per cm³ soil. In contrast, transcriptional activity of " Desulfosporosinus infrequens" increased at day 36 by 56- to 188-fold when minor amendments of acetate, propionate, lactate, or butyrate were provided with sulfate, compared to the no-substrate-control. Overall transcriptional activity was driven by expression of genes encoding ribosomal proteins, energy metabolism, and stress response but not by expression of genes encoding cell growth-associated processes. Since our results did not support growth of these highly active microorganisms in terms of biomass increase or cell division, they had to invest their sole energy for maintenance, most likely counterbalancing acidic pH conditions. This finding explains how a rare biosphere member can contribute to a biogeochemically relevant process while remaining in a zero-growth state over a period of 50 days. The microbial rare biosphere represents the largest pool of biodiversity on Earth and constitutes, in sum of all its members, a considerable part of a habitat's biomass. Dormancy or starvation is typically used to explain the persistence of low-abundance microorganisms in the environment. We show that a low-abundance microorganism can be highly transcriptionally active while remaining in a zero-growth state for at least 7 weeks. Our results provide evidence that this zero growth at a high cellular activity state is driven by maintenance requirements. We show that this is true for a microbial keystone species, in particular a cosmopolitan but permanently low-abundance sulfate-reducing microorganism in wetlands that is involved in counterbalancing greenhouse gas emissions. In summary, our results provide an important step forward in understanding time-resolved activities of rare biosphere members relevant for ecosystem functions.
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http://dx.doi.org/10.1128/mBio.02189-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6372793PMC
February 2019

Bacterial interactions during sequential degradation of cyanobacterial necromass in a sulfidic arctic marine sediment.

Environ Microbiol 2018 08 3;20(8):2927-2940. Epub 2018 Sep 3.

Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network Chemistry meets Microbiology, University of Vienna, Vienna, Austria.

Seafloor microorganisms impact global carbon cycling by mineralizing vast quantities of organic matter (OM) from pelagic primary production, which is predicted to increase in the Arctic because of diminishing sea ice cover. We studied microbial interspecies-carbon-flow during anaerobic OM degradation in arctic marine sediment using stable isotope probing. We supplemented sediment incubations with C-labeled cyanobacterial necromass (spirulina), mimicking fresh OM input, or acetate, an important OM degradation intermediate and monitored sulfate reduction rates and concentrations of volatile fatty acids (VFAs) during substrate degradation. Sequential 16S rRNA gene and transcript amplicon sequencing and fluorescence in situ hybridization combined with Raman microspectroscopy revealed that only few bacterial species were the main degraders of C-spirulina necromass. Psychrilyobacter, Psychromonas, Marinifilum, Colwellia, Marinilabiaceae and Clostridiales species were likely involved in the primary hydrolysis and fermentation of spirulina. VFAs, mainly acetate, produced from spirulina degradation were mineralized by sulfate-reducing bacteria and an Arcobacter species. Cellular activity of Desulfobacteraceae and Desulfobulbaceae species during acetoclastic sulfate reduction was largely decoupled from relative 16S rRNA gene abundance shifts. Our findings provide new insights into the identities and physiological constraints that determine the population dynamics of key microorganisms during complex OM degradation in arctic marine sediments.© 2018 Society for Applied Microbiology and John Wiley & Sons Ltd.
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http://dx.doi.org/10.1111/1462-2920.14297DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6175234PMC
August 2018

Stable-Isotope Probing of Human and Animal Microbiome Function.

Trends Microbiol 2018 12 9;26(12):999-1007. Epub 2018 Jul 9.

Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network Chemistry Meets Microbiology, University of Vienna, Althanstrasse 14, Vienna, Austria.

Humans and animals host diverse communities of microorganisms important to their physiology and health. Despite extensive sequencing-based characterization of host-associated microbiomes, there remains a dramatic lack of understanding of microbial functions. Stable-isotope probing (SIP) is a powerful strategy to elucidate the ecophysiology of microorganisms in complex host-associated microbiotas. Here, we suggest that SIP methodologies should be more frequently exploited as part of a holistic functional microbiomics approach. We provide examples of how SIP has been used to study host-associated microbes in vivo and ex vivo. We highlight recent developments in SIP technologies and discuss future directions that will facilitate deeper insights into the function of human and animal microbiomes.
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http://dx.doi.org/10.1016/j.tim.2018.06.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6249988PMC
December 2018

Peatland Acidobacteria with a dissimilatory sulfur metabolism.

ISME J 2018 06 23;12(7):1729-1742. Epub 2018 Feb 23.

Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network Chemistry meets Microbiology, University of Vienna, Vienna, Austria.

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, which so far was only found in sulfur-oxidizing microorganisms. 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, might also operate in reverse for dissimilatory sulfur oxidation or disproportionation as proposed for the sulfur-oxidizing Desulfurivibrio alkaliphilus. 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.
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http://dx.doi.org/10.1038/s41396-018-0077-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6018796PMC
June 2018

Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle.

ISME J 2018 06 21;12(7):1715-1728. Epub 2018 Feb 21.

Department of Earth and Planetary Science, Berkeley, CA, USA.

A critical step in the biogeochemical cycle of sulfur on Earth is microbial sulfate reduction, yet organisms from relatively few lineages have been implicated in this process. Previous studies using functional marker genes have detected abundant, novel dissimilatory sulfite reductases (DsrAB) that could confer the capacity for microbial sulfite/sulfate reduction but were not affiliated with known organisms. Thus, the identity of a significant fraction of sulfate/sulfite-reducing microbes has remained elusive. Here we report the discovery of the capacity for sulfate/sulfite reduction in the genomes of organisms from 13 bacterial and archaeal phyla, thereby more than doubling the number of microbial phyla associated with this process. Eight of the 13 newly identified groups are candidate phyla that lack isolated representatives, a finding only possible given genomes from metagenomes. Organisms from Verrucomicrobia and two candidate phyla, Candidatus Rokubacteria and Candidatus Hydrothermarchaeota, contain some of the earliest evolved dsrAB genes. The capacity for sulfite reduction has been laterally transferred in multiple events within some phyla, and a key gene potentially capable of modulating sulfur metabolism in associated cells has been acquired by putatively symbiotic bacteria. We conclude that current functional predictions based on phylogeny significantly underestimate the extent of sulfate/sulfite reduction across Earth's ecosystems. Understanding the prevalence of this capacity is integral to interpreting the carbon cycle because sulfate reduction is often coupled to turnover of buried organic carbon. Our findings expand the diversity of microbial groups associated with sulfur transformations in the environment and motivate revision of biogeochemical process models based on microbial community composition.
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http://dx.doi.org/10.1038/s41396-018-0078-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6018805PMC
June 2018

Draft Genome Sequence of 26-4b1, an Acidotolerant Peatland Alphaproteobacterium Potentially Involved in Sulfur Cycling.

Genome Announc 2018 Jan 25;6(4). Epub 2018 Jan 25.

Research Network Chemistry meets Microbiology, Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria.

The facultative anaerobic chemoorganoheterotrophic alphaproteobacterium 26-4b1 was isolated from a Siberian peatland. We report here a 6.20-Mbp near-complete high-quality draft genome sequence of that reveals expected and novel metabolic potential for the genus , including genes for sulfur oxidation.
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http://dx.doi.org/10.1128/genomeA.01524-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5786683PMC
January 2018

Ammonia-oxidising archaea living at low pH: Insights from comparative genomics.

Environ Microbiol 2017 Dec 4;19(12):4939-4952. Epub 2017 Dec 4.

School of Biological Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen, AB24 3UU, UK.

Obligate acidophilic members of the thaumarchaeotal genus Candidatus Nitrosotalea play an important role in nitrification in acidic soils, but their evolutionary and physiological adaptations to acidic environments are still poorly understood, with only a single member of this genus (Ca. N. devanaterra) having its genome sequenced. In this study, we sequenced the genomes of two additional cultured Ca. Nitrosotalea strains, extracted an almost complete Ca. Nitrosotalea metagenome-assembled genome from an acidic fen, and performed comparative genomics of the four Ca. Nitrosotalea genomes with 19 other archaeal ammonia oxidiser genomes. Average nucleotide and amino acid identities revealed that the four Ca. Nitrosotalea strains represent separate species within the genus. The four Ca. Nitrosotalea genomes contained a core set of 103 orthologous gene families absent from all other ammonia-oxidizing archaea and, for most of these gene families, expression could be demonstrated in laboratory culture or the environment via proteomic or metatranscriptomic analyses respectively. Phylogenetic analyses indicated that four of these core gene families were acquired by the Ca. Nitrosotalea common ancestor via horizontal gene transfer from acidophilic representatives of Euryarchaeota. We hypothesize that gene exchange with these acidophiles contributed to the competitive success of the Ca. Nitrosotalea lineage in acidic environments.
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http://dx.doi.org/10.1111/1462-2920.13971DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5767755PMC
December 2017

Depth Distribution and Assembly of Sulfate-Reducing Microbial Communities in Marine Sediments of Aarhus Bay.

Appl Environ Microbiol 2017 Dec 16;83(23). Epub 2017 Nov 16.

Center for Geomicrobiology, Section for Microbiology, Department of Bioscience, Aarhus University, Aarhus, Denmark

Most sulfate-reducing microorganisms (SRMs) present in subsurface marine sediments belong to uncultured groups only distantly related to known SRMs, and it remains unclear how changing geochemical zones and sediment depth influence their community structure. We mapped the community composition and abundance of SRMs by amplicon sequencing and quantifying the gene, which encodes dissimilatory sulfite reductase subunit beta, in sediment samples covering different vertical geochemical zones ranging from the surface sediment to the deep sulfate-depleted subsurface at four locations in Aarhus Bay, Denmark. SRMs were present in all geochemical zones, including sulfate-depleted methanogenic sediment. The biggest shift in SRM community composition and abundance occurred across the transition from bioturbated surface sediments to nonbioturbated sediments below, where redox fluctuations and the input of fresh organic matter due to macrofaunal activity are absent. SRM abundance correlated with sulfate reduction rates determined for the same sediments. Sulfate availability showed a weaker correlation with SRM abundances and no significant correlation with the composition of the SRM community. The overall SRM species diversity decreased with depth, yet we identified a subset of highly abundant community members that persists across all vertical geochemical zones of all stations. We conclude that subsurface SRM communities assemble by the persistence of members of the surface community and that the transition from the bioturbated surface sediment to the unmixed sediment below is a main site of assembly of the subsurface SRM community. Sulfate-reducing microorganisms (SRMs) are key players in the marine carbon and sulfur cycles, especially in coastal sediments, yet little is understood about the environmental factors controlling their depth distribution. Our results suggest that macrofaunal activity is a key driver of SRM abundance and community structure in marine sediments and that a small subset of SRM species of high relative abundance in the subsurface SRM community persists from the sulfate-rich surface sediment to sulfate-depleted methanogenic subsurface sediment. More generally, we conclude that SRM communities inhabiting the subsurface seabed assemble by the selective survival of members of the surface community.
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http://dx.doi.org/10.1128/AEM.01547-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5691419PMC
December 2017

Bottled aqua incognita: microbiota assembly and dissolved organic matter diversity in natural mineral waters.

Microbiome 2017 09 22;5(1):126. Epub 2017 Sep 22.

Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, Research Network Chemistry meets Microbiology, University of Vienna, Althanstrasse 14, A-1090, Vienna, Austria.

Background: Non-carbonated natural mineral waters contain microorganisms that regularly grow after bottling despite low concentrations of dissolved organic matter (DOM). Yet, the compositions of bottled water microbiota and organic substrates that fuel microbial activity, and how both change after bottling, are still largely unknown.

Results: We performed a multifaceted analysis of microbiota and DOM diversity in 12 natural mineral waters from six European countries. 16S rRNA gene-based analyses showed that less than 10 species-level operational taxonomic units (OTUs) dominated the bacterial communities in the water phase and associated with the bottle wall after a short phase of post-bottling growth. Members of the betaproteobacterial genera Curvibacter, Aquabacterium, and Polaromonas (Comamonadaceae) grew in most waters and represent ubiquitous, mesophilic, heterotrophic aerobes in bottled waters. Ultrahigh-resolution mass spectrometry of DOM in bottled waters and their corresponding source waters identified thousands of molecular formulae characteristic of mostly refractory, soil-derived DOM.

Conclusions: The bottle environment, including source water physicochemistry, selected for growth of a similar low-diversity microbiota across various bottled waters. Relative abundance changes of hundreds of multi-carbon molecules were related to growth of less than ten abundant OTUs. We thus speculate that individual bacteria cope with oligotrophic conditions by simultaneously consuming diverse DOM molecules.
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http://dx.doi.org/10.1186/s40168-017-0344-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5610417PMC
September 2017

HuR Small-Molecule Inhibitor Elicits Differential Effects in Adenomatosis Polyposis and Colorectal Carcinogenesis.

Cancer Res 2017 05 20;77(9):2424-2438. Epub 2017 Feb 20.

Christian Doppler Laboratory for Molecular Cancer Chemoprevention, Division of Gastroenterology and Hepatology, Department of Medicine 3, Medical University of Vienna, Vienna, Austria.

HuR is an RNA-binding protein implicated in immune homeostasis and various cancers, including colorectal cancer. HuR binding to AU-rich elements within the 3' untranslated region of mRNAs encoding oncogenes, growth factors, and various cytokines leads message stability and translation. In this study, we evaluated HuR as a small-molecule target for preventing colorectal cancer in high-risk groups such as those with familial adenomatosis polyposis (FAP) or inflammatory bowel disease (IBD). In human specimens, levels of cytoplasmic HuR were increased in colonic epithelial cells from patients with IBD, IBD-cancer, FAP-adenoma, and colorectal cancer, but not in patients with IBD-dysplasia. Intraperitoneal injection of the HuR small-molecule inhibitor MS-444 in AOM/DSS mice, a model of IBD and inflammatory colon cancer, augmented DSS-induced weight loss and increased tumor multiplicity, size, and invasiveness. MS-444 treatment also abrogated tumor cell apoptosis and depleted tumor-associated eosinophils, accompanied by a decrease in IL18 and eotaxin-1. In contrast, HuR inhibition in APC mice, a model of FAP and colon cancer, diminished the number of small intestinal tumors generated. In this setting, fecal microbiota, evaluated by 16S rRNA gene amplicon sequencing, shifted to a state of reduced bacterial diversity, with an increased representation of , and Taken together, our results indicate that HuR activation is an early event in FAP-adenoma but is not present in IBD-dysplasia. Furthermore, our results offer a preclinical proof of concept for HuR inhibition as an effective means of FAP chemoprevention, with caution advised in the setting of IBD. .
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http://dx.doi.org/10.1158/0008-5472.CAN-15-1726DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5826591PMC
May 2017

The life sulfuric: microbial ecology of sulfur cycling in marine sediments.

Environ Microbiol Rep 2017 08 5;9(4):323-344. Epub 2017 May 5.

Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, Research Network "Chemistry meets Microbiology", University of Vienna, Althanstrasse 14, Vienna, A-1090, Austria.

Almost the entire seafloor is covered with sediments that can be more than 10 000 m thick and represent a vast microbial ecosystem that is a major component of Earth's element and energy cycles. Notably, a significant proportion of microbial life in marine sediments can exploit energy conserved during transformations of sulfur compounds among different redox states. Sulfur cycling, which is primarily driven by sulfate reduction, is tightly interwoven with other important element cycles (carbon, nitrogen, iron, manganese) and therefore has profound implications for both cellular- and ecosystem-level processes. Sulfur-transforming microorganisms have evolved diverse genetic, metabolic, and in some cases, peculiar phenotypic features to fill an array of ecological niches in marine sediments. Here, we review recent and selected findings on the microbial guilds that are involved in the transformation of different sulfur compounds in marine sediments and emphasise how these are interlinked and have a major influence on ecology and biogeochemistry in the seafloor. Extraordinary discoveries have increased our knowledge on microbial sulfur cycling, mainly in sulfate-rich surface sediments, yet many questions remain regarding how sulfur redox processes may sustain the deep-subsurface biosphere and the impact of organic sulfur compounds on the marine sulfur cycle.
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http://dx.doi.org/10.1111/1758-2229.12538DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5573963PMC
August 2017

Lifestyle and Horizontal Gene Transfer-Mediated Evolution of , a Core Member of the Murine Gut Microbiota.

mSystems 2017 Jan-Feb;2(1). Epub 2017 Jan 31.

Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, University of Vienna, Austria.

is an abundant inhabitant of the intestinal mucus layer of rodents and other animals and has been suggested to be a pathobiont, a commensal that plays a role in disease. In order to gain insights into its lifestyle, we analyzed the genome and transcriptome of ASF 457 and performed physiological experiments to test traits predicted by its genome. Although described as a mucus inhabitant, has limited capacity for degrading host-derived mucosal glycans and other complex polysaccharides. Additionally, reduces nitrate and expresses systems for scavenging oxygen and reactive oxygen species , which may account for its localization close to the mucosal tissue and expansion during inflammation. Also of note, harbors a type VI secretion system and putative effector proteins and can modify gene expression in mucosal tissue, suggesting intimate interactions with its host and a possible role in inflammation. The genome has been shaped by extensive horizontal gene transfer, primarily from intestinal - and , indicating that horizontal gene transfer has played a key role in defining its niche in the gut ecosystem. Shifts in gut microbiota composition have been associated with intestinal inflammation, but it remains unclear whether inflammation-associated bacteria are commensal or detrimental to their host. Here, we studied the lifestyle of the gut bacterium , which is associated with inflammation in widely used mouse models. We found that has specialized systems to handle oxidative stress during inflammation. Additionally, it expresses secretion systems and effector proteins and can modify the mucosal gene expression of its host. This suggests that undergoes intimate interactions with its host and may play a role in inflammation. The insights presented here aid our understanding of how commensal gut bacteria may be involved in altering susceptibility to disease.
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http://dx.doi.org/10.1128/mSystems.00171-16DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5285517PMC
January 2017