Showing papers in "The ISME Journal in 2019"

Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots

Abstract: Root-associated microbes play a key role in plant performance and productivity, making them important players in agroecosystems. So far, very few studies have assessed the impact of different farming systems on the root microbiota and it is still unclear whether agricultural intensification influences the structure and complexity of microbial communities. We investigated the impact of conventional, no-till, and organic farming on wheat root fungal communities using PacBio SMRT sequencing on samples collected from 60 farmlands in Switzerland. Organic farming harbored a much more complex fungal network with significantly higher connectivity than conventional and no-till farming systems. The abundance of keystone taxa was the highest under organic farming where agricultural intensification was the lowest. We also found a strong negative association (R2 = 0.366; P < 0.0001) between agricultural intensification and root fungal network connectivity. The occurrence of keystone taxa was best explained by soil phosphorus levels, bulk density, pH, and mycorrhizal colonization. The majority of keystone taxa are known to form arbuscular mycorrhizal associations with plants and belong to the orders Glomerales, Paraglomerales, and Diversisporales. Supporting this, the abundance of mycorrhizal fungi in roots and soils was also significantly higher under organic farming. To our knowledge, this is the first study to report mycorrhizal keystone taxa for agroecosystems, and we demonstrate that agricultural intensification reduces network complexity and the abundance of keystone taxa in the root microbiome.

Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China.

Abstract: Revealing the linkages between community assembly and species coexistence, which is crucial for the understanding of ecosystem diversity and functioning, is a fundamental but rarely investigated subject in microbial ecology. Here we examined archaeal, bacterial, and fungal community assembly in adjacent pairs of maize (water-unsaturated) and rice (water-saturated) fields across different habitats and regions throughout Eastern China. The high-throughput sequencing dataset was analyzed by variation partitioning, null model, and neutral community model analyses. We demonstrated that microbial community assembly was governed more by species sorting than by dispersal limitation in maize fields, and to a lesser extent in rice fields. The relative importance of species sorting in maize soils was greater at low latitudes than at high latitudes, while rice soils exhibited an opposite trend. Microbial co-occurrence associations tended to be higher when communities were primarily driven by dispersal limitation relative to species sorting. There were greater community dissimilarities between maize and rice soils in low-latitude regions, which was consistent with the higher proportion of negative edges in the correlation networks. The results indicate that a balance between species sorting and dispersal limitation mediates species coexistence in soil microbiomes. This study enhances our understanding of contemporary coexistence theory in microbial ecosystems.

Wastewater treatment plant resistomes are shaped by bacterial composition, genetic exchange, and upregulated expression in the effluent microbiomes

Abstract: Wastewater treatment plants (WWTPs) are implicated as hotspots for the dissemination of antibacterial resistance into the environment However, the in situ processes governing removal, persistence, and evolution of resistance genes during wastewater treatment remain poorly understood Here, we used quantitative metagenomic and metatranscriptomic approaches to achieve a broad-spectrum view of the flow and expression of genes related to antibacterial resistance to over 20 classes of antibiotics, 65 biocides, and 22 metals All compartments of 12 WWTPs share persistent resistance genes with detectable transcriptional activities that were comparatively higher in the secondary effluent, where mobility genes also show higher relative abundance and expression ratios The richness and abundance of resistance genes vary greatly across metagenomes from different treatment compartments, and their relative and absolute abundances correlate with bacterial community composition and biomass concentration No strong drivers of resistome composition could be identified among the chemical stressors analyzed, although the sub-inhibitory concentration (hundreds of ng/L) of macrolide antibiotics in wastewater correlates with macrolide and vancomycin resistance genes Contig-based analysis shows considerable co-localization between resistance and mobility genes and implies a history of substantial horizontal resistance transfer involving human bacterial pathogens Based on these findings, we propose future inclusion of mobility incidence (M%) and host pathogenicity of antibiotic resistance genes in their quantitative health risk ranking models with an ultimate goal to assess the biological significance of wastewater resistomes with regard to disease control in humans or domestic livestock

Linking bacterial community composition to soil salinity along environmental gradients

Abstract: Salinization is recognized as a threat to soil fertility worldwide. A challenge in understanding the effects of salinity on soil microbial communities is the fact that it can be difficult to disentangle the effects of salinity from those of other variables that may co-vary with salinity. Here we use a trait-based approach to identify direct effects of salinity on soil bacterial communities across two salinity gradients. Through dose–response relationships between salinity and bacterial growth, we quantified distributions of the trait salt tolerance within the communities. Community salt tolerance was closely correlated with soil salinity, indicating a strong filtering effect of salinity on the bacterial communities. Accompanying the increases in salt tolerance were consistent shifts in bacterial community composition. We identified specific bacterial taxa that increased in relative abundances with community salt tolerance, which could be used as bioindicators for high community salt tolerance. A strong filtering effect was also observed for pH across the gradients, with pH tolerance of bacterial communities correlated to soil pH. We propose phenotypic trait distributions aggregated at the community level as a useful approach to study the role of environmental factors as filters of microbial community composition.

Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing

Abstract: Delignification, or lignin-modification, facilitates the decomposition of lignocellulose in woody plant biomass. The extant diversity of lignin-degrading bacteria and fungi is underestimated by culture-dependent methods, limiting our understanding of the functional and ecological traits of decomposers populations. Here, we describe the use of stable isotope probing (SIP) coupled with amplicon and shotgun metagenomics to identify and characterize the functional attributes of lignin, cellulose and hemicellulose-degrading fungi and bacteria in coniferous forest soils from across North America. We tested the extent to which catabolic genes partitioned among different decomposer taxa; the relative roles of bacteria and fungi, and whether taxa or catabolic genes correlated with variation in lignocellulolytic activity, measured as the total assimilation of 13C-label into DNA and phospholipid fatty acids. We found high overall bacterial degradation of our model lignin substrate, particularly by gram-negative bacteria (Comamonadaceae and Caulobacteraceae), while fungi were more prominent in cellulose-degradation. Very few taxa incorporated 13C-label from more than one lignocellulosic polymer, suggesting specialization among decomposers. Collectively, members of Caulobacteraceae could degrade all three lignocellulosic polymers, providing new evidence for their importance in lignocellulose degradation. Variation in lignin-degrading activity was better explained by microbial community properties, such as catabolic gene content and community structure, than cellulose-degrading activity. SIP significantly improved shotgun metagenome assembly resulting in the recovery of several high-quality draft metagenome-assembled genomes and over 7500 contigs containing unique clusters of carbohydrate-active genes. These results improve understanding of which organisms, conditions and corresponding functional genes contribute to lignocellulose decomposition.

High proportions of bacteria and archaea across most biomes remain uncultured.

Abstract: A recent paper by Martiny argues that “high proportions” of bacteria in diverse Earth environments have been cultured. Here we reanalyze a portion of the data in that paper, and argue that the conclusion is based on several technical errors, most notably a calculation of sequence similarity that does not account for sequence gaps, and the reliance on 16S rRNA gene amplicons that are known to be biased towards cultured organisms. We further argue that the paper is also based on a conceptual error: namely, that sequence similarity cannot be used to infer “culturability” because one cannot infer physiology from 16S rRNA gene sequences. Combined with other recent, more reliable studies, the evidence supports the conclusion that most bacterial and archaeal taxa remain uncultured.

Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation.

Abstract: Although the early coral reef-bleaching warning system (NOAA/USA) is established, there is no feasible treatment that can minimize temperature bleaching and/or disease impacts on corals in the field. Here, we present the first attempts to extrapolate the widespread and well-established use of bacterial consortia to protect or improve health in other organisms (e.g., humans and plants) to corals. Manipulation of the coral-associated microbiome was facilitated through addition of a consortium of native (isolated from Pocillopora damicornis and surrounding seawater) putatively beneficial microorganisms for corals (pBMCs), including five Pseudoalteromonas sp., a Halomonas taeanensis and a Cobetia marina-related species strains. The results from a controlled aquarium experiment in two temperature regimes (26 °C and 30 °C) and four treatments (pBMC; pBMC with pathogen challenge – Vibrio coralliilyticus, VC; pathogen challenge, VC; and control) revealed the ability of the pBMC consortium to partially mitigate coral bleaching. Significantly reduced coral-bleaching metrics were observed in pBMC-inoculated corals, in contrast to controls without pBMC addition, especially challenged corals, which displayed strong bleaching signs as indicated by significantly lower photopigment contents and Fv/Fm ratios. The structure of the coral microbiome community also differed between treatments and specific bioindicators were correlated with corals inoculated with pBMC (e.g., Cobetia sp.) or VC (e.g., Ruegeria sp.). Our results indicate that the microbiome in corals can be manipulated to lessen the effect of bleaching, thus helping to alleviate pathogen and temperature stresses, with the addition of BMCs representing a promising novel approach for minimizing coral mortality in the face of increasing environmental impacts.

Antiepileptic drug carbamazepine promotes horizontal transfer of plasmid-borne multi-antibiotic resistance genes within and across bacterial genera.

Abstract: Antibiotic resistance is a severe global threat for public health, causing around 700,000 deaths per year. Horizontal gene transfer (HGT) is one of the most significant pathways to disseminate antibiotic resistance. It is commonly acknowledged that sub-minimum inhibition concentrations of antibiotics are major contributors in promoting antibiotic resistance through HGT. Pharmaceuticals are occurring in our environments at increased levels, yet little is known whether non-antibiotic pharmaceuticals cause or accelerate the dissemination of antibiotic resistance. Here, we report for the first time that the antiepileptic drug, carbamazepine, promotes conjugative transfer of antibiotic resistance genes. It was seen that environmentally relevant concentrations of carbamazepine (e.g., 0.05 mg/L) significantly enhanced the conjugative transfer of multiresistance genes carried by plasmid within and across bacterial genera. The underlying mechanisms of the enhanced HGT were revealed by detecting oxidative stress and cell membrane permeability, in combination with MinION DNA sequencing, genome-wide RNA sequencing, and proteomic analysis. Carbamazepine induced a series of acute responses, including increased levels of reactive oxygen species, the SOS response; increased cell membrane permeability, and pilus generation. Expressional levels of genes related to these processes were significantly upregulated during carbamazepine exposure. Given that HGT occurs widely among different species in various environments, these findings are an early warning for a wide assessment of the roles of non-antibiotic pharmaceuticals in the spread of antibiotic resistance.

Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes.

Abstract: Over the past decade several studies have reported that the gut microbiomes of mammals with similar dietary niches exhibit similar compositional and functional traits. However, these studies rely heavily on samples from captive individuals and often confound host phylogeny, gut morphology, and diet. To more explicitly test the influence of host dietary niche on the mammalian gut microbiome we use 16S rRNA gene amplicon sequencing and shotgun metagenomics to compare the gut microbiota of 18 species of wild non-human primates classified as either folivores or closely related non-folivores, evenly distributed throughout the primate order and representing a range of gut morphological specializations. While folivory results in some convergent microbial traits, collectively we show that the influence of host phylogeny on both gut microbial composition and function is much stronger than that of host dietary niche. This pattern does not result from differences in host geographic location or actual dietary intake at the time of sampling, but instead appears to result from differences in host physiology. These findings indicate that mammalian gut microbiome plasticity in response to dietary shifts over both the lifespan of an individual host and the evolutionary history of a given host species is constrained by host physiological evolution. Therefore, the gut microbiome cannot be considered separately from host physiology when describing host nutritional strategies and the emergence of host dietary niches.

Bacterial persistence promotes the evolution of antibiotic resistance by increasing survival and mutation rates

Abstract: Persisters are transiently antibiotic-tolerant cells that complicate the treatment of bacterial infections. Both theory and experiments have suggested that persisters facilitate genetic resistance by constituting an evolutionary reservoir of viable cells. Here, we provide evidence for a strong positive correlation between persistence and the likelihood to become genetically resistant in natural and lab strains of E. coli. This correlation can be partly attributed to the increased availability of viable cells associated with persistence. However, our data additionally show that persistence is pleiotropically linked with mutation rates. Our theoretical model further demonstrates that increased survival and mutation rates jointly affect the likelihood of evolving clinical resistance. Overall, these results suggest that the battle against antibiotic resistance will benefit from incorporating anti-persister therapies.

Defining the role of Parasutterella, a previously uncharacterized member of the core gut microbiota.

Abstract: The genus of Parasutterella has been defined as a core component of the human and mouse gut microbiota, and has been correlated with various health outcomes. However, like most core microbes in the gastrointestinal tract (GIT), very little is known about the biology of Parasutterella and its role in intestinal ecology. In this study, Parasutterella was isolated from the mouse GIT and characterized in vitro and in vivo. Mouse, rat, and human Parasutterella isolates were all asaccharolytic and producers of succinate. The murine isolate stably colonized the mouse GIT without shifting bacterial composition. Notable changes in microbial-derived metabolites were aromatic amino acid, bilirubin, purine, and bile acid derivatives. The impacted bile acid profile was consistent with altered expression of ileal bile acid transporter genes and hepatic bile acid synthesis genes, supporting the potential role of Parasutterella in bile acid maintenance and cholesterol metabolism. The successful colonization of Parasutterella with a single environmental exposure to conventional adult mice demonstrates that it fills the ecological niche in the GIT and contributes to metabolic functionalities. This experiment provides the first indication of the role of Parasutterella in the GIT, beyond correlation, and provides insight into how it may contribute to host health.

Metabolic regulation of the maize rhizobiome by benzoxazinoids

Abstract: The rhizobiome is an important regulator of plant growth and health. Plants shape their rhizobiome communities through production and release of primary and secondary root metabolites. Benzoxazinoids (BXs) are common tryptophan-derived secondary metabolites in grasses that regulate belowground and aboveground biotic interactions. In addition to their biocidal activity, BXs can regulate plant–biotic interactions as semiochemicals or within-plant defence signals. However, the full extent and mechanisms by which BXs shape the root-associated microbiome has remained largely unexplored. Here, we have taken a global approach to examine the regulatory activity of BXs on the maize root metabolome and associated bacterial and fungal communities. Using untargeted mass spectrometry analysis in combination with prokaryotic and fungal amplicon sequencing, we compared the impacts of three genetic mutations in different steps in the BX pathway. We show that BXs regulate global root metabolism and concurrently influence the rhizobiome in a root type-dependent manner. Correlation analysis between BX-controlled root metabolites and bacterial taxa suggested a dominant role for BX-dependent metabolites, particularly flavonoids, in constraining a range of soil microbial taxa, while stimulating methylophilic bacteria. Our study supports a multilateral model by which BXs control root–microbe interactions via a global regulatory function in root secondary metabolism.

Use and abuse of correlation analyses in microbial ecology

Abstract: Correlation analyses are often included in bioinformatic pipelines as methods for inferring taxon–taxon interactions. In this perspective, we highlight the pitfalls of inferring interactions from covariance and suggest methods, study design considerations, and additional data types for improving high-throughput interaction inferences. We conclude that correlation, even when augmented by other data types, almost never provides reliable information on direct biotic interactions in real-world ecosystems. These bioinformatically inferred associations are useful for reducing the number of potential hypotheses that we might test, but will never preclude the necessity for experimental validation.

Linking the resistome and plasmidome to the microbiome.

Abstract: The rapid spread of antibiotic resistance among bacterial pathogens is a serious human health threat. While a range of environments have been identified as reservoirs of antibiotic resistance genes (ARGs), we lack understanding of the origins of these ARGs and their spread from environment to clinic. This is partly due to our inability to identify the natural bacterial hosts of ARGs and the mobile genetic elements that mediate this spread, such as plasmids and integrons. Here we demonstrate that the in vivo proximity-ligation method Hi-C can reconstruct a known plasmid-host association from a wastewater community, and identify the in situ host range of ARGs, plasmids, and integrons by physically linking them to their host chromosomes. Hi-C detected both previously known and novel associations between ARGs, mobile genetic elements and host genomes, thus validating this method. We showed that IncQ plasmids and class 1 integrons had the broadest host range in this wastewater, and identified bacteria belonging to Moraxellaceae, Bacteroides, and Prevotella, and especially Aeromonadaceae as the most likely reservoirs of ARGs in this community. A better identification of the natural carriers of ARGs will aid the development of strategies to limit resistance spread to pathogens.

A new widespread subclass of carbonic anhydrase in marine phytoplankton.

Abstract: Most aquatic photoautotrophs depend on CO2-concentrating mechanisms (CCMs) to maintain productivity at ambient concentrations of CO2, and carbonic anhydrase (CA) plays a key role in these processes. Here we present different lines of evidence showing that the protein LCIP63, identified in the marine diatom Thalassiosira pseudonana, is a CA. However, sequence analysis showed that it has a low identity with any known CA and therefore belongs to a new subclass that we designate as iota-CA. Moreover, LCIP63 unusually prefers Mn2+ to Zn2+ as a cofactor, which is potentially of ecological relevance since Mn2+ is more abundant than Zn2+ in the ocean. LCIP63 is located in the chloroplast and only expressed at low concentrations of CO2. When overexpressed using biolistic transformation, the rate of photosynthesis at limiting concentrations of dissolved inorganic carbon increased, confirming its role in the CCM. LCIP63 homologs are present in the five other sequenced diatoms and in other algae, bacteria, and archaea. Thus LCIP63 is phylogenetically widespread but overlooked. Analysis of the Tara Oceans database confirmed this and showed that LCIP63 is widely distributed in marine environments and is therefore likely to play an important role in global biogeochemical carbon cycling.

Legacy of land use history determines reprogramming of plant physiology by soil microbiome.

Abstract: Microorganisms associated with roots are thought to be part of the so-called extended plant phenotypes with roles in the acquisition of nutrients, production of growth hormones, and defense against diseases. Since the crops selectively enrich most rhizosphere microbes out of the bulk soil, we hypothesized that changes in the composition of bulk soil communities caused by agricultural management affect the extended plant phenotype. In the current study, we performed shotgun metagenome sequencing of the rhizosphere microbiome of the peanut (Arachis hypogaea) and metatranscriptome analysis of the roots of peanut plants grown in the soil with different management histories, peanut monocropping and crop rotation. We found that the past planting record had a significant effect on the assembly of the microbial community in the peanut rhizosphere, indicating a soil memory effect. Monocropping resulted in a reduction of the rhizosphere microbial diversity, an enrichment of several rare species, and a reduced representation of traits related to plant performance, such as nutrients metabolism and phytohormone biosynthesis. Furthermore, peanut plants in monocropped soil exhibited a significant reduction in growth coinciding with a down-regulation of genes related to hormone production, mainly auxin and cytokinin, and up-regulation of genes related to the abscisic acid, salicylic acid, jasmonic acid, and ethylene pathways. These findings suggest that land use history affects crop rhizosphere microbiomes and plant physiology.

Uneven distribution of cobamide biosynthesis and dependence in bacteria predicted by comparative genomics.

Abstract: The vitamin B12 family of cofactors known as cobamides are essential for a variety of microbial metabolisms. We used comparative genomics of 11,000 bacterial species to analyze the extent and distribution of cobamide production and use across bacteria. We find that 86% of bacteria in this data set have at least one of 15 cobamide-dependent enzyme families, but only 37% are predicted to synthesize cobamides de novo. The distribution of cobamide biosynthesis and use vary at the phylum level. While 57% of Actinobacteria are predicted to biosynthesize cobamides, only 0.6% of Bacteroidetes have the complete pathway, yet 96% of species in this phylum have cobamide-dependent enzymes. The form of cobamide produced by the bacteria could be predicted for 58% of cobamide-producing species, based on the presence of signature lower ligand biosynthesis and attachment genes. Our predictions also revealed that 17% of bacteria have partial biosynthetic pathways, yet have the potential to salvage cobamide precursors. Bacteria with a partial cobamide biosynthesis pathway include those in a newly defined, experimentally verified category of bacteria lacking the first step in the biosynthesis pathway. These predictions highlight the importance of cobamide and cobamide precursor salvaging as examples of nutritional dependencies in bacteria.

Resolving the individual contribution of key microbial populations to enhanced biological phosphorus removal with Raman–FISH

Abstract: Enhanced biological phosphorus removal (EBPR) is a globally important biotechnological process and relies on the massive accumulation of phosphate within special microorganisms. Candidatus Accumulibacter conform to the classical physiology model for polyphosphate accumulating organisms and are widely believed to be the most important player for the process in full-scale EBPR systems. However, it was impossible till now to quantify the contribution of specific microbial clades to EBPR. In this study, we have developed a new tool to directly link the identity of microbial cells to the absolute quantification of intracellular poly-P and other polymers under in situ conditions, and applied it to eight full-scale EBPR plants. Besides Ca. Accumulibacter, members of the genus Tetrasphaera were found to be important microbes for P accumulation, and in six plants they were the most important. As these Tetrasphaera cells did not exhibit the classical phenotype of poly-P accumulating microbes, our entire understanding of the microbiology of the EBPR process has to be revised. Furthermore, our new single-cell approach can now also be applied to quantify storage polymer dynamics in individual populations in situ in other ecosystems and might become a valuable tool for many environmental microbiologists.

Response of the eukaryotic plankton community to the cyanobacterial biomass cycle over 6 years in two subtropical reservoirs

Abstract: Although it is widely recognized that cyanobacterial blooms have substantial influence on the plankton community in general, their correlations with the whole community of eukaryotic plankton at longer time scales remain largely unknown. Here, we investigated the temporal dynamics of eukaryotic plankton communities in two subtropical reservoirs over a 6-year period (2010-2015) following one cyanobacterial biomass cycle-the cyanobacterial bloom (middle 2010), cyanobacteria decrease (late 2010-early 2011), non-bloom (2011-2014), cyanobacteria increase, and second bloom (late 2014-2015). The eukaryotic community succession that strongly correlated with this cyanobacterial biomass cycle was divided into four periods, and each period had distinct characteristics in cyanobacterial biomass and environments in both reservoirs. Integrated co-occurrence networks of eukaryotic plankton based on the whole study period revealed that the cyanobacterial biomass had remarkably high network centralities, and the eukaryotic OTUs that had stronger correlations with the cyanobacterial biomass exhibited higher centralities. The integrated networks were also modularly responded to different eukaryotic succession periods, and therefore correlated with the cyanobacterial biomass cycle. Moreover, sub-networks based on the different eukaryotic succession periods indicated that the eukaryotic co-occurrence patterns were not constant but varied largely associating with the cyanobacterial biomass. Based on these long-term observations, our results reveal that the cyanobacterial biomass cycle created distinct niches between persistent bloom, non-bloom, decrease and increase of cyanobacteria, and therefore associated with distinct eukaryotic plankton patterns. Our results have important implications for understanding how complex aquatic plankton communities respond to cyanobacterial blooms under the changing environments.

Polysaccharide utilization loci of North Sea Flavobacteriia as basis for using SusC/D-protein expression for predicting major phytoplankton glycans

Abstract: Marine algae convert a substantial fraction of fixed carbon dioxide into various polysaccharides. Flavobacteriia that are specialized on algal polysaccharide degradation feature genomic clusters termed polysaccharide utilization loci (PULs). As knowledge on extant PUL diversity is sparse, we sequenced the genomes of 53 North Sea Flavobacteriia and obtained 400 PULs. Bioinformatic PUL annotations suggest usage of a large array of polysaccharides, including laminarin, α-glucans, and alginate as well as mannose-, fucose-, and xylose-rich substrates. Many of the PULs exhibit new genetic architectures and suggest substrates rarely described for marine environments. The isolates’ PUL repertoires often differed considerably within genera, corroborating ecological niche-associated glycan partitioning. Polysaccharide uptake in Flavobacteriia is mediated by SusCD-like transporter complexes. Respective protein trees revealed clustering according to polysaccharide specificities predicted by PUL annotations. Using the trees, we analyzed expression of SusC/D homologs in multiyear phytoplankton bloom-associated metaproteomes and found indications for profound changes in microbial utilization of laminarin, α-glucans, β-mannan, and sulfated xylan. We hence suggest the suitability of SusC/D-like transporter protein expression within heterotrophic bacteria as a proxy for the temporal utilization of discrete polysaccharides.

The gut microbiota is largely independent of host genetics in regulating fat deposition in chickens.

Abstract: The gut microbiota has an important role in animal health and performance, but its contribution is difficult to determine, in particular given the effects of host genetic factors. Here, whole-genome sequencing of the hosts and 16S rRNA gene sequencing of the microbiota were performed to separate the effects between host genetics and the microbiota in the duodenum, jejunum, ileum, caecum and faeces on fat deposition in 206 yellow broilers reared under identical conditions. Despite the notable spatial variation in the diversity, composition and potential function of the gut microbiota, host genetics exerted limited effects on the gut microbial community. The duodenal and caecal microbiota made greater contributions to fat deposition and could separately account for 24% and 21% of the variance in the abdominal fat mass after correcting for host genetic effects. We further identified two caecal microbial taxa, Methanobrevibacter and Mucispirillum schaedleri, which were significantly correlated with fat deposition. Chickens with a lower Methanobrevibacter abundance had significantly lower abdominal fat content than those with a higher abundance of Methanobrevibacter (35.51 vs. 55.59 g), and the body weights of these chickens did not notably differ. Chickens with a higher M. schaedleri abundance exhibited lower abdominal fat accumulation (39.88 vs. 55.06 g) and body weight (2.23 vs. 2.41 kg) than those with a lower abundance of this species. These findings may aid the development of strategies for altering the gut microbiota to control fat deposition during broiler production.

A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea ( Ca . Poseidoniales ord. nov.)

Abstract: Marine Group II (MGII) archaea represent the most abundant planktonic archaeal group in ocean surface waters, but our understanding of the group has been limited by a lack of cultured representatives and few sequenced genomes. Here, we conducted a comparative phylogenomic analysis of 270 recently available MGII metagenome-assembled genomes (MAGs) to investigate their evolution and ecology. Based on a rank-normalised genome phylogeny, we propose that MGII is an order-level lineage for which we propose the name Candidatus Poseidoniales (after Gr. n. Poseidon, God of the sea), comprising the families Candidatus Poseidonaceae fam. nov. (formerly subgroup MGIIa) and Candidatus Thalassarchaeaceae fam. nov. (formerly subgroup MGIIb). Within these families, 21 genera could be resolved, many of which had distinct biogeographic ranges and inferred nutrient preferences. Phylogenetic analyses of key metabolic functions suggest that the ancestor of Ca. Poseidoniales was a surface water-dwelling photoheterotroph that evolved to occupy multiple related ecological niches based primarily on spectral tuning of proteorhodopsin genes. Interestingly, this adaptation appears to involve an overwrite mechanism whereby an existing single copy of the proteorhodopsin gene is replaced by a horizontally transferred copy, which in many instances should allow an abrupt change in light absorption capacity. Phototrophy was lost entirely from five Ca. Poseidoniales genera coinciding with their adaptation to deeper aphotic waters. We also report the first instances of nitrate reductase in two genera acquired via horizontal gene transfer (HGT), which was a potential adaptation to oxygen limitation. Additional metabolic traits differentiating families and genera include flagellar-based adhesion, transporters, and sugar, amino acid, and peptide degradation. Our results suggest that HGT has shaped the evolution of Ca. Poseidoniales to occupy a variety of ecological niches and to become the most successful archaeal lineage in ocean surface waters.

Atmospheric carbon monoxide oxidation is a widespread mechanism supporting microbial survival.

Abstract: Carbon monoxide (CO) is a ubiquitous atmospheric trace gas produced by natural and anthropogenic sources. Some aerobic bacteria can oxidize atmospheric CO and, collectively, they account for the net loss of ~250 teragrams of CO from the atmosphere each year. However, the physiological role, genetic basis, and ecological distribution of this process remain incompletely resolved. In this work, we addressed these knowledge gaps through culture-based and culture-independent work. We confirmed through shotgun proteomic and transcriptional analysis that the genetically tractable aerobic soil actinobacterium Mycobacterium smegmatis upregulates expression of a form I molydenum-copper carbon monoxide dehydrogenase by 50-fold when exhausted for organic carbon substrates. Whole-cell biochemical assays in wild-type and mutant backgrounds confirmed that this organism aerobically respires CO, including at sub-atmospheric concentrations, using the enzyme. Contrary to current paradigms on CO oxidation, the enzyme did not support chemolithoautotrophic growth and was dispensable for CO detoxification. However, it significantly enhanced long-term survival, suggesting that atmospheric CO serves a supplemental energy source during organic carbon starvation. Phylogenetic analysis indicated that atmospheric CO oxidation is widespread and an ancestral trait of CO dehydrogenases. Homologous enzymes are encoded by 685 sequenced species of bacteria and archaea, including from seven dominant soil phyla, and we confirmed genes encoding this enzyme are abundant and expressed in terrestrial and marine environments. On this basis, we propose a new survival-centric model for the evolution of aerobic CO oxidation and conclude that, like atmospheric H2, atmospheric CO is a major energy source supporting persistence of aerobic heterotrophic bacteria in deprived or changeable environments.

The soil organic matter decomposition mechanisms in ectomycorrhizal fungi are tuned for liberating soil organic nitrogen

Abstract: Many trees form ectomycorrhizal symbiosis with fungi. During symbiosis, the tree roots supply sugar to the fungi in exchange for nitrogen, and this process is critical for the nitrogen and carbon cycles in forest ecosystems. However, the extents to which ectomycorrhizal fungi can liberate nitrogen and modify the soil organic matter and the mechanisms by which they do so remain unclear since they have lost many enzymes for litter decomposition that were present in their free-living, saprotrophic ancestors. Using time-series spectroscopy and transcriptomics, we examined the ability of two ectomycorrhizal fungi from two independently evolved ectomycorrhizal lineages to mobilize soil organic nitrogen. Both species oxidized the organic matter and accessed the organic nitrogen. The expression of those events was controlled by the availability of glucose and inorganic nitrogen. Despite those similarities, the decomposition mechanisms, including the type of genes involved as well as the patterns of their expression, differed markedly between the two species. Our results suggest that in agreement with their diverse evolutionary origins, ectomycorrhizal fungi use different decomposition mechanisms to access organic nitrogen entrapped in soil organic matter. The timing and magnitude of the expression of the decomposition activity can be controlled by the below-ground nitrogen quality and the above-ground carbon supply.

Diverse hydrogen production and consumption pathways influence methane production in ruminants.

Abstract: Farmed ruminants are the largest source of anthropogenic methane emissions globally. The methanogenic archaea responsible for these emissions use molecular hydrogen (H2), produced during bacterial and eukaryotic carbohydrate fermentation, as their primary energy source. In this work, we used comparative genomic, metatranscriptomic and co-culture-based approaches to gain a system-wide understanding of the organisms and pathways responsible for ruminal H2 metabolism. Two-thirds of sequenced rumen bacterial and archaeal genomes encode enzymes that catalyse H2 production or consumption, including 26 distinct hydrogenase subgroups. Metatranscriptomic analysis confirmed that these hydrogenases are differentially expressed in sheep rumen. Electron-bifurcating [FeFe]-hydrogenases from carbohydrate-fermenting Clostridia (e.g., Ruminococcus) accounted for half of all hydrogenase transcripts. Various H2 uptake pathways were also expressed, including methanogenesis (Methanobrevibacter), fumarate and nitrite reduction (Selenomonas), and acetogenesis (Blautia). Whereas methanogenesis-related transcripts predominated in high methane yield sheep, alternative uptake pathways were significantly upregulated in low methane yield sheep. Complementing these findings, we observed significant differential expression and activity of the hydrogenases of the hydrogenogenic cellulose fermenter Ruminococcus albus and the hydrogenotrophic fumarate reducer Wolinella succinogenes in co-culture compared with pure culture. We conclude that H2 metabolism is a more complex and widespread trait among rumen microorganisms than previously recognised. There is evidence that alternative hydrogenotrophs, including acetogenic and respiratory bacteria, can prosper in the rumen and effectively compete with methanogens for H2. These findings may help to inform ongoing strategies to mitigate methane emissions by increasing flux through alternative H2 uptake pathways, including through animal selection, dietary supplementation and methanogenesis inhibitors.

Modeling microbial communities from atrazine contaminated soils promotes the development of biostimulation solutions.

Abstract: Microbial communities play a vital role in biogeochemical cycles, allowing the biodegradation of a wide range of pollutants. The composition of the community and the interactions between its members affect degradation rate and determine the identity of the final products. Here, we demonstrate the application of sequencing technologies and metabolic modeling approaches towards enhancing biodegradation of atrazine-a herbicide causing environmental pollution. Treatment of agriculture soil with atrazine is shown to induce significant changes in community structure and functional performances. Genome-scale metabolic models were constructed for Arthrobacter, the atrazine degrader, and four other non-atrazine degrading species whose relative abundance in soil was changed following exposure to the herbicide. By modeling community function we show that consortia including the direct degrader and non-degrader differentially abundant species perform better than Arthrobacter alone. Simulations predict that growth/degradation enhancement is derived by metabolic exchanges between community members. Based on simulations we designed endogenous consortia optimized for enhanced degradation whose performances were validated in vitro and biostimulation strategies that were tested in pot experiments. Overall, our analysis demonstrates that understanding community function in its wider context, beyond the single direct degrader perspective, promotes the design of biostimulation strategies.

Sulfate-reducing bacteria and methanogens are involved in arsenic methylation and demethylation in paddy soils

Abstract: Microbial arsenic (As) methylation and demethylation are important components of the As biogeochemical cycle. Arsenic methylation is enhanced under flooded conditions in paddy soils, producing mainly phytotoxic dimethylarsenate (DMAs) that can cause rice straighthead disease, a physiological disorder occurring widely in some rice growing regions. The key microbial groups responsible for As methylation and demethylation in paddy soils are unknown. Three paddy soils were incubated under flooded conditions. DMAs initially accumulated in the soil porewater, followed by a rapid disappearance coinciding with the production of methane. The soil from a rice straighthead disease paddy field produced a much larger amount of DMAs than the other two soils. Using metabolic inhibition, quantification of functional gene transcripts, microbial enrichment cultures and 13C-labeled DMAs, we show that sulfate-reducing bacteria (SRB) and methanogenic archaea are involved in As methylation and demethylation, respectively, controlling the dynamics of DMAs in paddy soils. We present a model of As biogeochemical cycle in paddy soils, linking the dynamics of changing soil redox potential with arsenite mobilization, arsenite methylation and subsequent demethylation driven by different microbial groups. The model provides a basis for controlling DMAs accumulation and incidence of straighthead disease in rice.

Microdiversity ensures the maintenance of functional microbial communities under changing environmental conditions

Abstract: Microdiversity can lead to different ecotypes within the same species. These are assumed to provide stability in time and space to those species. However, the role of microdiversity in the stability of whole microbial communities remains underexplored. Understanding the drivers of microbial community stability is necessary to predict community response to future disturbances. Here, we analyzed 16S rRNA gene amplicons from eight different temperate bog lakes at the 97% OTU and amplicon sequence variant (ASV) levels and found ecotypes within the same OTU with different distribution patterns in space and time. We observed that these ecotypes are adapted to different values of environmental factors such as water temperature and oxygen concentration. Our results showed that the existence of several ASVs within a OTU favored its persistence across changing environmental conditions. We propose that microdiversity aids the stability of microbial communities in the face of fluctuations in environmental factors.

Temperature and soil moisture control microbial community composition in an arctic-alpine ecosystem along elevational and micro-topographic gradients.

Abstract: Microbial communities in arctic-alpine soils show biogeographic patterns related to elevation, but the effect of fine-scale heterogeneity and possibly related temperature and soil moisture regimes remains unclear. We collected soil samples from different micro-topographic positions and elevational levels in two mountain regions of the Scandes, Central Norway. Microbial community composition was characterized by 16S rRNA gene amplicon sequencing and was dependent on micro-topography and elevation. Underlying environmental drivers were identified by integration of microbial community data with a comprehensive set of site-specific long-term recorded temperature and soil moisture data. Partial least square regression analysis allowed the description of ecological response patterns and the identification of the important environmental drivers for each taxonomic group. This demonstrated for the first time that taxa responding to elevation were indeed most strongly defined by temperature, rather than by other environmental factors. Micro-topography affected taxa were primarily controlled by temperature and soil moisture. In general, 5-year datasets had higher explanatory power than 1-year datasets, indicating that the microbial community composition is dependent on long-term developments of near-ground temperature and soil moisture regimes and possesses a certain resilience, which is in agreement with an often observed delayed response in global warming studies in arctic-alpine regions.

In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes.

Abstract: We investigated Bacteroidetes during spring algae blooms in the southern North Sea in 2010–2012 using a time series of 38 deeply sequenced metagenomes Initial partitioning yielded 6455 bins, from which we extracted 3101 metagenome-assembled genomes (MAGs) including 1286 Bacteroidetes MAGs covering ~120 mostly uncultivated species We identified 13 dominant, recurrent Bacteroidetes clades carrying a restricted set of conserved polysaccharide utilization loci (PULs) that likely mediate the bulk of bacteroidetal algal polysaccharide degradation The majority of PULs were predicted to target the diatom storage polysaccharide laminarin, alpha-glucans, alpha-mannose-rich substrates, and sulfated xylans Metaproteomics at 14 selected points in time revealed expression of SusC-like proteins from PULs targeting all of these substrates Analyses of abundant key players and their PUL repertoires over time furthermore suggested that fewer and simpler polysaccharides dominated early bloom stages, and that more complex polysaccharides became available as blooms progressed