Publications by authors named "Julien Tremblay"

50 Publications

Impact of sample collection on prokaryotic and eukaryotic diversity of niche environments of the oil-sand mining impacted Athabasca River.

Can J Microbiol 2021 Jun 25. Epub 2021 Jun 25.

Environment and Climate Change Canada, Canada Centre for Inland Waters, Burlington, Ontario, Canada;

Microbial communities are an important aspect of overall riverine ecology; however, appreciation of the effects of anthropogenic activities on unique riverine microbial niches, and how the collection of these samples affects the observed diversity and community profile is lacking. We analyzed prokaryotic and eukaryotic communities from surface water, biofilm, suspended load niches along a gradient of oil sands-related contamination in the Athabasca River (Alberta, Canada), with suspended load or particle-associated communities collected either via Kenney Sampler or centrifugation manifold. At the level of phyla, different niche communities were highly similar to one another and across locations. However, there were significant differences in the abundance of specific genera amongst different niches and across sampling locations. A generalized linear model revealed that use of the Kenney Sampler resulted in more diverse bacterial and eukaryotic suspended load community than centrifugal collection, though "suspended load" communities collected by any means remained stably diverse across locations. Though there was influence of water quality parameters on community composition, all sampled sites support diverse bacterial and eukaryotic communities regardless of the degree of contamination, highlighting the need to look beyond ecological diversity as means of assessing ecological perturbations, and consider collecting samples from multiple niche environments.
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http://dx.doi.org/10.1139/cjm-2021-0058DOI Listing
June 2021

In situ microcosms deployed at the coast of British Columbia (Canada) to study dilbit weathering and associated microbial communities under marine conditions.

FEMS Microbiol Ecol 2021 06;97(7)

Energy, Mining and Environment Research Center, National Research Council of Canada (NRC), 6100 Royalmount Ave, Montreal, QC H4P 2R2, Canada.

Douglas Channel and the adjacent Hecate Strait (British Columbia, Canada) are part of a proposed route to ship diluted bitumen (dilbit). This study presents how two types of dilbit naturally degrade in this environment by using an in situ microcosm design based on dilbit-coated beads. We show that dilbit-associated n-alkanes were microbially biodegraded with estimated half-lives of 57-69 days. n-Alkanes appeared to be primarily degraded using the aerobic alkB, ladA and CYP153 pathways. The loss of dilbit polycyclic aromatic hydrocarbons (PAHs) was slower than of n-alkanes, with half-lives of 89-439 days. A biodegradation of PAHs could not be conclusively determined, although a significant enrichment of the phnAc gene (a marker for aerobic PAH biodegradation) was observed. PAH degradation appeared to be slower in Hecate Strait than in Douglas Channel. Microcosm-associated microbial communities were shaped by the presence of dilbit, deployment location and incubation time but not by dilbit type. Metagenome-assembled genomes of putative dilbit-degraders were obtained and could be divided into populations of early, late and continuous degraders. The majority of the identified MAGs could be assigned to the orders Flavobacteriales, Methylococcales, Pseudomonadales and Rhodobacterales. A high proportion of the MAGs represent currently unknown lineages or lineages with currently no cultured representative.
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http://dx.doi.org/10.1093/femsec/fiab082DOI Listing
June 2021

In situ microcosms deployed at the coast of British Columbia (Canada) to study dilbit weathering and associated microbial communities under marine conditions.

FEMS Microbiol Ecol 2021 06;97(7)

Energy, Mining and Environment Research Center, National Research Council of Canada (NRC), 6100 Royalmount Ave, Montreal, QC H4P 2R2, Canada.

Douglas Channel and the adjacent Hecate Strait (British Columbia, Canada) are part of a proposed route to ship diluted bitumen (dilbit). This study presents how two types of dilbit naturally degrade in this environment by using an in situ microcosm design based on dilbit-coated beads. We show that dilbit-associated n-alkanes were microbially biodegraded with estimated half-lives of 57-69 days. n-Alkanes appeared to be primarily degraded using the aerobic alkB, ladA and CYP153 pathways. The loss of dilbit polycyclic aromatic hydrocarbons (PAHs) was slower than of n-alkanes, with half-lives of 89-439 days. A biodegradation of PAHs could not be conclusively determined, although a significant enrichment of the phnAc gene (a marker for aerobic PAH biodegradation) was observed. PAH degradation appeared to be slower in Hecate Strait than in Douglas Channel. Microcosm-associated microbial communities were shaped by the presence of dilbit, deployment location and incubation time but not by dilbit type. Metagenome-assembled genomes of putative dilbit-degraders were obtained and could be divided into populations of early, late and continuous degraders. The majority of the identified MAGs could be assigned to the orders Flavobacteriales, Methylococcales, Pseudomonadales and Rhodobacterales. A high proportion of the MAGs represent currently unknown lineages or lineages with currently no cultured representative.
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http://dx.doi.org/10.1093/femsec/fiab082DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8213973PMC
June 2021

Rhizosphere shotgun metagenomic analyses fail to show differences between ancestral and modern wheat genotypes grown under low fertilizer inputs.

FEMS Microbiol Ecol 2021 06;97(6)

Centre Armand-Frappier Santé Biotechnologie, Institut national de la recherche scientifique, 531 boul. des Prairies, Laval, QC, H7V 1B7, Canada.

It is thought that modern wheat genotypes have lost their capacity to associate with soil microbes that would help them acquire nutrients from the soil. To test this hypothesis, ten ancestral and modern wheat genotypes were seeded in a field experiment under low fertilization conditions. The rhizosphere soil was collected, its DNA extracted and submitted to shotgun metagenomic sequencing. In contrast to our hypothesis, there was no significant difference in the global rhizosphere metagenomes of the different genotypes, and this held true when focusing the analyses on specific taxonomic or functional categories of genes. Some genes were significantly more abundant in the rhizosphere of one genotype or another, but they comprised only a small portion of the total genes identified and did not affect the global rhizosphere metagenomes. Our study shows for the first time that the rhizosphere metagenome of wheat is stable across a wide variety of genotypes when growing under nutrient poor conditions.
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http://dx.doi.org/10.1093/femsec/fiab071DOI Listing
June 2021

Microbiota succession during aerobic stability of maize silage inoculated with Lentilactobacillus buchneri NCIMB 40788 and Lentilactobacillus hilgardii CNCM-I-4785.

Microbiologyopen 2021 01 24;10(1):e1153. Epub 2020 Dec 24.

Lallemand SAS, Blagnac, France.

Aerobic deterioration of silage following feeding out is responsible for the deterioration of its quality. Inoculation of silage with lactic acid bacteria is one strategy to limit these effects. A trial was performed using whole-plant corn ensiled in bag silo, and forage was inoculated with Lentilactobacillus buchneri NCIMB 40788 (Lactobacillus buchneri) and Lentilactobacillus hilgardii CNCM-I-4785 (Lactobacillus hilgardii) or not (Control silage). After 159 days of fermentation, the silos were opened and the silage was sampled at 24-h intervals during a 10-day aerobic stability assay to measure pH, the fermentation profile, mycotoxins, and microbial and fungal populations. In inoculated silage, lactic acid concentrations and pH remained stable during the aerobic phase and higher microorganism alpha-diversity was observed. Treated silage was characterized by a high abundance of Saccharomycetes and maintenance of Lactobacillus throughout the aerobic stability assay. The high aerobic stability of the inoculated silage contrasted with the decrease in lactic acid contents and the increase in pH observed in the Control silage, concomitantly with an increase in lactate-assimilating yeast (Pichia and Issatchenkia), and in Acetobacter and Paenibacillus OTUs. Remarkably, Penicillium and roquefortine C were detected in this silage by day 8 following exposure to air. Our study highlighted the fact that the use of L. buchneri with L. hilgardii modified the consequences of exposure to air by maintaining higher microbial diversity, avoiding the dominance of a few bacteria, and preventing fungi from having a detrimental effect on silage quality.
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http://dx.doi.org/10.1002/mbo3.1153DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7885010PMC
January 2021

Temporal and spatial interactions modulate the soybean microbiome.

FEMS Microbiol Ecol 2021 01;97(1)

Institut national de la recherche scientifique, Centre Armand-Frappier Santé Biotechnologie, 531 boulevard des Prairies, Laval, Québec, H7V1B7, Canada.

Managed agricultural ecosystems are unique systems where crops and microbes are intrinsically linked. This study focuses on discerning microbiome successional patterns across all plant organs and tests for evidence of niche differentiation along temporal and spatial axes. Soybean plants were grown in an environmental chamber till seed maturation. Samples from various developmental stages (emergence, growth, flowering and maturation) and compartments (leaf, stem, root and rhizosphere) were collected. Community structure and composition were assessed with 16S rRNA gene and ITS region amplicon sequencing. Overall, the interaction between spatial and temporal dynamics modulated alpha and beta diversity patterns. Time lag analysis on measured diversity indices highlighted a strong temporal dependence of communities. Spatial and temporal interactions influenced the relative abundance of the most abundant genera, whilst random forest predictions reinforced the observed localisation patterns of abundant genera. Overall, our results show that spatial and temporal interactions tend to maintain high levels of biodiversity within the bacterial/archaeal community, whilst in fungal communities OTUs within the same genus tend to have overlapping niches.
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http://dx.doi.org/10.1093/femsec/fiaa206DOI Listing
January 2021

Draft Whole-Genome Sequence of the Alkane-Synthesizing Polar Cyanobacterium Pseudanabaena biceps Strain O-153.

Microbiol Resour Announc 2020 Nov 19;9(47). Epub 2020 Nov 19.

McGill University, Department of Natural Resource Sciences, Ste-Anne-de-Bellevue, Quebec, Canada.

Alkane biosynthesis by polar cyanobacteria has not yet been reported. We present here the draft whole-genome sequence of an alkane-synthesizing polar cyanobacterium, strain O-153. The genes coding for the two key enzymes involved in the alkane biosynthetic pathway were found contiguously in the genome.
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http://dx.doi.org/10.1128/MRA.00904-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7679089PMC
November 2020

Vegetation drives the structure of active microbial communities on an acidogenic mine tailings deposit.

PeerJ 2020 21;8:e10109. Epub 2020 Oct 21.

Centre SÈVE, Département de biologie, Faculté des Sciences, Université de Sherbrooke, Sherbrooke, Québec, Canada.

Plant-microbe associations are increasingly recognized as an inextricable part of plant biology and biogeochemistry. Microbes play an essential role in the survival and development of plants, allowing them to thrive in diverse environments. The composition of the rhizosphere soil microbial communities is largely influenced by edaphic conditions and plant species. In order to decipher how environmental conditions on a mine site can influence the dynamics of microbial communities, we characterized the rhizosphere soil microbial communities associated with paper birch, speckled alder, and spruce that had naturally colonized an acidogenic mine tailings deposit containing heavy metals. The study site, which had been largely undisturbed for five decades, had highly variable vegetation density; with some areas remaining almost barren, and others having a few stands or large thickets of mature trees. Using Illumina sequencing and ordination analyses (redundancy analysis and principal coordinate analysis), our study showed that soil bacterial and fungal community structures correlated mainly with vegetation density, and plant species. Tailings without any vegetation were the most different in bacterial community structure, compared to all other areas on the mine site, as well as an adjacent natural forest (comparison plot). The bacterial genera and were more abundant in tailings without vegetation than in any of the other sites, while sp. were more abundant in areas of the tailings deposit having higher vegetation density. sp. is equally represented in each of the vegetation densities and sp. present a greater relative abundance in boreal forest. Furthermore, alder rhizosphere showed a greater relative abundance of sp. (in comparison with birch and spruce) as well as sp. (in comparison with birch). In contrast, fungal community structures were similar across the tailings deposit regardless of vegetation density, showing a greater relative abundance of sp. Tailings deposit fungal communities were distinct from those found in boreal forest soils. Alder rhizosphere had greater relative abundances of sp. and sp., while birch rhizosphere were more often associated with sp. Our results indicate that, with increasing vegetation density on the mine site, the bacterial communities associated with the individual deciduous or coniferous species studied were increasingly similar to the bacterial communities found in the adjacent forest. In order to properly assess and restore disturbed sites, it is important to characterize and understand the plant-microbe associations that occur since they likely improve plant fitness in these harsh environments.
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http://dx.doi.org/10.7717/peerj.10109DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7585372PMC
October 2020

Soil Characteristics Constrain the Response of Microbial Communities and Associated Hydrocarbon Degradation Genes during Phytoremediation.

Appl Environ Microbiol 2021 01 4;87(2). Epub 2021 Jan 4.

Centre Armand Frappier Santé Biotechnologie, Institut National de la Recherche Scientifique, Université du Québec, Laval, Quebec, Canada

Rhizodegradation is a promising cleanup technology where microorganisms degrade soil contaminants in the rhizosphere. A symbiotic relationship is expected to occur between plant roots and soil microorganisms in contaminated soils that enhances natural microbial degradation. However, little is known about how different initial microbiotas influence the rhizodegradation outcome. Recent studies have hinted that soil initial diversity has a determining effect on the outcome of contaminant degradation. To test this, we either planted (P) or not (NP) balsam poplars () in two soils of contrasting diversity (agricultural and forest) that were contaminated or not with 50 mg kg of phenanthrene (PHE). The DNA from the rhizosphere of the P and the bulk soil of the NP pots was extracted and the bacterial genes encoding the 16S rRNA, the PAH ring-hydroxylating dioxygenase alpha subunits (PAH-RHDα) of Gram-positive and Gram-negative bacteria, and the fungal ITS region were sequenced to characterize the microbial communities. The abundances of the PAH-RHDα genes were quantified by real-time quantitative PCR. Plant presence had a significant effect on PHE degradation only in the forest soil, whereas both NP and P agricultural soils degraded the same amount of PHE. Fungal communities were mainly affected by plant presence, whereas bacterial communities were principally affected by the soil type, and upon contamination the dominant PAH-degrading community was similarly constrained by soil type. Our results highlight the crucial importance of soil microbial and physicochemical characteristics in the outcome of rhizoremediation. Polycyclic aromatic hydrocarbons (PAH) are a group of organic contaminants that pose a risk to ecosystems' health. Phytoremediation is a promising biotechnology with the potential to restore PAH-contaminated soils. However, some limitations prevent it from becoming the remediation technology of reference, despite being environmentally friendlier than mainstream physicochemical alternatives. Recent reports suggest that the original soil microbial diversity is the key to harnessing the potential of phytoremediation. Therefore, this study focused on determining the effect of two different soil types in the fate of phenanthrene (a polycyclic aromatic hydrocarbon) under balsam poplar remediation. Poplar increased the degradation of phenanthrene in forest, but not in agricultural soil. The fungi were affected by poplars, whereas total bacteria and specific PAH-degrading bacteria were constrained by soil type, leading to different degradation patterns between soils. These results highlight the importance of performing preliminary microbiological studies of contaminated soils to determine whether plant presence could improve remediation rates or not.
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http://dx.doi.org/10.1128/AEM.02170-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7783334PMC
January 2021

Draft Whole-Genome Sequence of the Anthracene-Degrading Strain Mycolicibacterium frederiksbergense LB501T, Isolated from a Polycyclic Aromatic Hydrocarbon-Contaminated Soil.

Microbiol Resour Announc 2020 Oct 22;9(43). Epub 2020 Oct 22.

Earth & Life Institute, Laboratory of Bioengineering, Catholic University of Louvain, Louvain-la-Neuve, Belgium

Here, we report the draft whole-genome sequence of an anthracene-degrading bacterium, strain LB501T, using the PacBio and Illumina sequencing platforms. The complete genome sequence of strain LB501T consists of 6,713,618 bp and provides new insights into its metabolic capabilities, including aromatic conversion pathways with promiscuous activities.
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http://dx.doi.org/10.1128/MRA.00671-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7585852PMC
October 2020

Four decades of soil water stress history together with host genotype constrain the response of the wheat microbiome to soil moisture.

FEMS Microbiol Ecol 2020 07;96(7)

Centre Armand-Frappier Santé Biotechnologie, Institut national de la recherche scientifique, Laval, Québec, H7V 1B7, Canada.

There is little understanding about how soil water stress history and host genotype influence the response of wheat-associated microbiome under short-term decreases in soil moisture. To address this, we investigated how plant breeding history (four wheat genotypes; two with recognized drought resistance and two without) and soil water stress history (same wheat field soil from Saskatchewan with contrasting long-term irrigation) independently or interactively influenced the response of the rhizosphere, root and leaf bacterial and fungal microbiota to short-term decreases in soil water content (SWC). We used amplicon sequencing (16S rRNA gene for bacteria and ITS region for fungi) to characterize the wheat microbiome. Fungal and bacterial communities responses to short-term decreases in SWC were mainly constrained by soil water stress history, with some smaller, but significant influence of plant genotype. One exception was the leaf-associated fungal communities, for which the largest constraint was genotype, resulting in a clear differentiation of the communities based on the genotype's sensitivity to water stress. Our results clearly indicate that soil legacy does not only affect the response to water stress of the microbes inhabiting the soil, but also of the microorganisms more closely associated with the plant tissues, and even of the plant itself.
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http://dx.doi.org/10.1093/femsec/fiaa098DOI Listing
July 2020

Biodegradation of weathered crude oil in seawater with frazil ice.

Mar Pollut Bull 2020 May 6;154:111090. Epub 2020 Apr 6.

SINTEF Ocean AS, Environment and New Resources, Trondheim, Norway.

As ice extent in the Arctic is declining, oil and gas activities will increase, with higher risk of oil spills to the marine environment. To determine biotransformation of dispersed weathered oil in newly formed ice, oil dispersions (2-3 ppm) were incubated in a mixture of natural seawater and frazil ice for 125 days at -2 °C. Dispersed oil in seawater without frazil ice were included in the experimental setup. Presence or absence of frazil ice was a strong driver for microbial community structures and affected the rate of oil degradation. n-alkanes were degraded faster in the presence of frazil ice, the opposite was the case for naphthalenes and 2-3 ring PAHs. No degradation of 4-6 ring PAHs was observed in any of the treatments. The total petroleum oil was not degraded to any significant degree, suggesting that oil will freeze into the ice matrix and persist throughout the icy season.
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http://dx.doi.org/10.1016/j.marpolbul.2020.111090DOI Listing
May 2020

Metatranscriptomic Insights Into the Response of River Biofilm Communities to Ionic and Nano-Zinc Oxide Exposures.

Front Microbiol 2020 26;11:267. Epub 2020 Feb 26.

Environment and Climate Change Canada, Saskatoon, SK, Canada.

Manufactured Zn oxide nanoparticle (ZnO-NP) are extensively used world-wide in personal care and industrial products and are important contaminants of aquatic environments. To understand the overall impact of ZnO-NP contamination on aquatic ecosystems, investigation of their toxicity on aquatic biofilms is of particular consequence, given biofilms are known sinks for NP contaminants. In order to assess alterations in the functional activity of river microbial biofilm communities as a result of environmentally-relevant ZnO-NP exposure, biofilms were exposed to ionic zinc salt or ZnOPs that were uncoated (hydrophilic), coated with silane (hydrophobic) or stearic acid (lipophilic), at a total concentration of 188 μg l Zn. ICP-MS analyses of biofilms indicated ZnO-NP concentrated in the biofilms, with hydrophilic, hydrophobic, and lipophilic treatments reaching 0.310, 0.250, and 0.220 μg Zn cm of biofilm, respectively, while scanning transmission X-ray microspectroscopy (STXM) analyses of biofilms confirmed that Zn was extensively- and differentially-sorbed to biofilm material. Microbial community composition, based on taxonomic affiliation of mRNA sequences and enumeration of protozoa and micrometazoa, was not affected by these treatments, and the total transcriptional response of biofilms to all experimental exposures was not indicative of a global toxic-response, as cellular processes involved in general cell maintenance and housekeeping were abundantly transcribed. Transcripts related to major biological processes, including photosynthesis, energy metabolism, nitrogen metabolism, lipid metabolism, membrane transport, antibiotic resistance and xenobiotic degradation, were differentially expressed in Zn-exposures relative to controls. Notably, transcripts involved in nitrogen fixation and photosynthesis were decreased in abundance in response to Zn-exposure, while transcripts related to lipid degradation and motility-chemotaxis were increased, suggesting a potential role of Zn in biofilm dissolution. ZnO-NP and ionic Zn exposures elicited generally overlapping transcriptional responses, however hydrophilic and hydrophobic ZnO-NPs induced a more distinct effect than that of lipophilic ZnO-NPs, which had an effect similar to that of low ionic Zn exposure. While the physical coating of ZnO-NP may not induce specific toxicity observable at a community level, alteration of ecologically important processes of photosynthesis and nitrogen cycling are an important potential consequence of exposure to ionic Zn and Zn oxides.
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http://dx.doi.org/10.3389/fmicb.2020.00267DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7055177PMC
February 2020

Probiotic Supplementation in a -Infected Gastrointestinal Model Is Associated with Restoring Metabolic Function of Microbiota.

Microorganisms 2019 Dec 29;8(1). Epub 2019 Dec 29.

School of Human Nutrition, McGill University, 21111 Lakeshore, Ste. Anne de Bellevue, Montréal, QC H9X3V9, Canada.

() -infection (CDI), a nosocomial gastrointestinal disorder, is of growing concern due to its rapid rise in recent years. Antibiotic therapy of CDI is associated with disrupted metabolic function and altered gut microbiota. The use of probiotics as an adjunct is being studied extensively due to their potential to modulate metabolic functions and the gut microbiota. In the present study, we assessed the ability of several single strain probiotics and a probiotic mixture to change the metabolic functions of normal and -infected fecal samples. The production of short-chain fatty acids (SCFAs), hydrogen sulfide (HS), and ammonia was measured, and changes in microbial composition were assessed by 16S rRNA gene amplicon sequencing. The -infection in fecal samples resulted in a significant decrease ( < 0.05) in SCFA and HS production, with a lower microbial alpha diversity. All probiotic treatments were associated with significantly increased ( < 0.05) levels of SCFAs and restored HS levels. Probiotics showed no effect on microbial composition of either normal or -infected fecal samples. These findings indicate that probiotics may be useful to improve the metabolic dysregulation associated with infection.
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http://dx.doi.org/10.3390/microorganisms8010060DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7023328PMC
December 2019

Microbial indicators are better predictors of wheat yield and quality than N fertilization.

FEMS Microbiol Ecol 2020 02;96(2)

Energy Mining Environment, National Research Council Canada, Montréal, Québec, H4P 2R2, Canada.

In view of their key roles in many soil- and plant-related processes, we hypothesized that soil microorganisms could play a larger role in determining wheat baking quality than nitrogen fertilization. A field experiment was conducted under bread wheat production conditions, where different fertilization treatments, ranging from 0-120 kg/ha NH4NO3, were applied. Soil samples were taken in May, June and July. Functional genes in the nitrogen cycle were quantified and amplicons of the 16S rRNA gene and the ITS region were sequenced. Wheat yields were measured, and the grain baking quality was analysed for each plot. Fertilisation did not significantly influence the yields and the grain quality. Many bacterial and fungal Amplicon Sequence Variants showed significant positive or negative correlations with yield and grain baking quality parameters. Among the functional gene quantified, the archaeal amoA showed strong negative correlations with the wheat yields and many grain and flour quality parameters. Regression models were able to explain up to 81% of the variability in grain quality based on the microbial data from the May sampling. A better understanding of the microbiology of wheat fields could lead to an optimized management of the N fertilization to maximize yields and grain quality.
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http://dx.doi.org/10.1093/femsec/fiz205DOI Listing
February 2020

Systematic processing of ribosomal RNA gene amplicon sequencing data.

Gigascience 2019 12;8(12)

Centre INRS-Institut Armand-Frappier, Institut national de la recherche scientifique, 531ad Boul. des Prairies, Laval, QC H7V-1B7, Canada.

Background: With the advent of high-throughput sequencing, microbiology is becoming increasingly data-intensive. Because of its low cost, robust databases, and established bioinformatic workflows, sequencing of 16S/18S/ITS ribosomal RNA (rRNA) gene amplicons, which provides a marker of choice for phylogenetic studies, has become ubiquitous. Many established end-to-end bioinformatic pipelines are available to perform short amplicon sequence data analysis. These pipelines suit a general audience, but few options exist for more specialized users who are experienced in code scripting, Linux-based systems, and high-performance computing (HPC) environments. For such an audience, existing pipelines can be limiting to fully leverage modern HPC capabilities and perform tweaking and optimization operations. Moreover, a wealth of stand-alone software packages that perform specific targeted bioinformatic tasks are increasingly accessible, and finding a way to easily integrate these applications in a pipeline is critical to the evolution of bioinformatic methodologies.

Results: Here we describe AmpliconTagger, a short rRNA marker gene amplicon pipeline coded in a Python framework that enables fine tuning and integration of virtually any potential rRNA gene amplicon bioinformatic procedure. It is designed to work within an HPC environment, supporting a complex network of job dependencies with a smart-restart mechanism in case of job failure or parameter modifications. As proof of concept, we present end results obtained with AmpliconTagger using 16S, 18S, ITS rRNA short gene amplicons and Pacific Biosciences long-read amplicon data types as input.

Conclusions: Using a selection of published algorithms for generating operational taxonomic units and amplicon sequence variants and for computing downstream taxonomic summaries and diversity metrics, we demonstrate the performance and versatility of our pipeline for systematic analyses of amplicon sequence data.
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http://dx.doi.org/10.1093/gigascience/giz146DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6901069PMC
December 2019

Dynamic Succession of Microbiota during Ensiling of Whole Plant Corn Following Inoculation with and Alone or in Combination.

Microorganisms 2019 Nov 21;7(12). Epub 2019 Nov 21.

Lallemand SAS, 19 rue des Briquetiers, 31702 Blagnac CEDEX, France.

Lactic acid bacteria (LAB) used as silage additives have been shown to improve several fermentation parameters, including aerobic stability. Inoculation with a combination of NCIMB40788 and CNCM-I-4785, contributes to an increase in aerobic stability, compared to each strain inoculated independently. To understand the mode of action of the combination on the LAB community, a fermentation-kinetic study was performed on corn. Four treatments, Control, , and a combination of the two strains, were fermented 1, 2, 4, 8, 16, 32, and 64 days. Corn silage inoculated by both strains had a lactate:acetate ratio of 0.59 after 64 days and a higher concentration of lactate than . Analysis of the microbiota by 16S and ITS amplicon metasequencing demonstrated that inoculation led to lower bacterial diversity after 1 day, from 129.4 down to 40.7 observed operational taxonomic units (OTUs). represented the dominant population by day 1, with 48.1%. dominated the succession by day 4, with 21.9%. After 32 days, inoculation by both strains had the lowest bacterial alpha diversity level, with 29.0 observed OTUs, compared to 61.3 for the Control. These results confirm the increased fermentation efficiency when the two strains are co-inoculated, which also led to a specific yeast OTUs diversity profile, with as the main OTU.
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http://dx.doi.org/10.3390/microorganisms7120595DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6955939PMC
November 2019

Long-term effects of nitrogen and phosphorus fertilization on soil microbial community structure and function under continuous wheat production.

Environ Microbiol 2020 03 4;22(3):1066-1088. Epub 2019 Nov 4.

Quebec Research and Development Centre, Agriculture and Agri-Food Canada, 2560 Hochelaga Boulevard, Quebec City, Quebec, G1V 2J3, Canada.

Soil microorganisms play a critical role in the biosphere, and the influence of cropland fertilization on the evolution of soil as a living entity is being actively documented. In this study, we used a shotgun metagenomics approach to globally expose the effects of 50-year N and P fertilization of wheat on soil microbial community structure and function, and their potential involvement in overall N cycling. Nitrogen (N) fertilization increased alpha diversity in archaea and fungi while reducing it in bacteria. Beta diversity of archaea, bacteria and fungi, as well as soil function, were also mainly driven by N fertilization. The abundance of archaea was negatively impacted by N fertilization while bacterial and fungal abundance was increased. The responses of N metabolism-related genes to fertilization differed in archaea, bacteria and fungi. All archaeal N metabolic processes were decreased by N fertilization, while denitrification, assimilatory nitrate reduction and organic-N metabolism were highly increased by N fertilization in bacteria. Nitrate assimilation was the main contribution of fungi to N cycling. Thaumarchaeota and Halobacteria in archaea; Actinobacteria, Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria and Deltaproteobacteria in bacteria; and Sordariomycetes in fungi participated dominantly and widely in soil N metabolic processes.
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http://dx.doi.org/10.1111/1462-2920.14824DOI Listing
March 2020

GenPipes: an open-source framework for distributed and scalable genomic analyses.

Gigascience 2019 06;8(6)

Canadian Centre for Computational Genomics, Montréal, QC, Canada.

Background: With the decreasing cost of sequencing and the rapid developments in genomics technologies and protocols, the need for validated bioinformatics software that enables efficient large-scale data processing is growing.

Findings: Here we present GenPipes, a flexible Python-based framework that facilitates the development and deployment of multi-step workflows optimized for high-performance computing clusters and the cloud. GenPipes already implements 12 validated and scalable pipelines for various genomics applications, including RNA sequencing, chromatin immunoprecipitation sequencing, DNA sequencing, methylation sequencing, Hi-C, capture Hi-C, metagenomics, and Pacific Biosciences long-read assembly. The software is available under a GPLv3 open source license and is continuously updated to follow recent advances in genomics and bioinformatics. The framework has already been configured on several servers, and a Docker image is also available to facilitate additional installations.

Conclusions: GenPipes offers genomics researchers a simple method to analyze different types of data, customizable to their needs and resources, as well as the flexibility to create their own workflows.
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http://dx.doi.org/10.1093/gigascience/giz037DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6559338PMC
June 2019

A water stress-adapted inoculum affects rhizosphere fungi, but not bacteria nor wheat.

FEMS Microbiol Ecol 2019 07;95(7)

Centre Armand-Frappier Santé Biotechnologie, Institut national de la recherche scientifique, 531 boulevard des Prairies, Laval, QC, H7V 1B7, Canada.

Here, we tested if inoculating microbial communities adapted to water stress would increase wheat resistance to water stress. Wheat plants were grown for 4 weeks in high and low diversity soils under well-watered conditions, after which they were subjected to a water stress. After another 2 weeks, the rhizospheres were inoculated with microbial communities extracted from soils with or without a history of water stress. The inoculations did not have significant effects on the plant growth, water content and catalase activity, and on the bacterial communities. However, the inoculation did successfully, though modestly, modify the fungal community, shifting the rhizosphere communities toward the inoculated communities. As hypothesized, these shifts were more pronounced and significant in the low diversity soil, and for the inoculum with a water stress history. Whereas the effects of inoculation were relatively subtle, the water stress resulted in large differences in the wheat phenotype and in both the bacterial and fungal communities. Generally, the microbial changes that followed the water stress were in large part due to shifts in the relative abundance of OTUs that were already present before the stress, rather than to the recruitment of microorganisms from the inoculum or the bulk soil.
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http://dx.doi.org/10.1093/femsec/fiz080DOI Listing
July 2019

Structural dynamics and transcriptomic analysis of Dehalococcoides mccartyi within a TCE-Dechlorinating community in a completely mixed flow reactor.

Water Res 2019 Jul 19;158:146-156. Epub 2019 Apr 19.

Department of Civil and Environmental Engineering, University of California, Berkeley, CA, 94720-1710, USA; Earth and Environmental Sciences Area, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA. Electronic address:

A trichloroethene (TCE)-dechlorinating community (CANAS) maintained in a completely mixed flow reactor was established from a semi-batch enrichment culture (ANAS) and was monitored for 400 days at a low solids retention time (SRT) under electron acceptor limitation. Around 85% of TCE supplied to CANAS (0.13 mmol d) was converted to ethene at a rate of 0.1 mmol d, with detection of low production rates of vinyl chloride (6.8 × 10 mmol d) and cis-dichloroethene (2.3 × 10 mmol d). Two distinct Dehalococcoides mccartyi strains (ANAS1 and ANAS2) were stably maintained at 6.2 ± 2.8 × 10 cells mL and 5.8 ± 1.2 × 10 cells mL, respectively. Electron balance analysis showed 107% electron recovery, in which 6.1% were involved in dechlorination. 16 S rRNA amplicon sequencing revealed a structural regime shift between ANAS and CANAS while maintaining robust TCE dechlorination due to similar relative abundances of D. mccartyi and functional redundancy among each functional guild supporting D. mccartyi activity. D. mccartyi transcriptomic analysis identified the genes encoding for ribosomal RNA and the reductive dehalogenases tceA and vcrA as the most expressed genes in CANAS, while hup and vhu were the most critical hydrogenases utilized by D. mccartyi in the community.
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http://dx.doi.org/10.1016/j.watres.2019.04.038DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7053656PMC
July 2019

Metagenomic and metatranscriptomic responses of natural oil degrading bacteria in the presence of dispersants.

Environ Microbiol 2019 07 25;21(7):2307-2319. Epub 2019 Apr 25.

Energy, Mining and Environment, National Research Council Canada, 6100 Royalmount Avenue, Montreal, Quebec, H4P2R2, Canada.

Oil biodegradation has been extensively studied in the wake of the deepwater horizon spill, but the application of dispersant to oil spills in marine environments remains controversial. Here, we report metagenomic (MG) and metatranscriptomic (MT) data mining from microcosm experiments investigating the oil degrading potential of Canadian west and east coasts to estimate the gene abundance and activity of oil degrading bacteria in the presence of dispersant. We found that the addition of dispersant to crude oil mainly favours the abundance of Thalassolituus in the summer and Oleispira in the winter, two key natural oil degrading bacteria. We found a high abundance of genes related not only to n-alkane and aromatics degradation but also associated with transporters, two-component systems, bacterial motility, secretion systems and bacterial chemotaxis.
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http://dx.doi.org/10.1111/1462-2920.14609DOI Listing
July 2019

Potential for Microbially Mediated Natural Attenuation of Diluted Bitumen on the Coast of British Columbia (Canada).

Appl Environ Microbiol 2019 05 2;85(10). Epub 2019 May 2.

Energy, Mining and Environment Research Center, National Research Council Canada, Montreal, Quebec, Canada.

Western Canada produces large amounts of bitumen, a heavy, highly weathered crude oil. Douglas Channel and Hecate Strait on the coast of British Columbia are two water bodies that may be impacted by a proposed pipeline and marine shipping route for diluted bitumen (dilbit). This study investigated the potential of microbial communities from these waters to mitigate the impacts of a potential dilbit spill. Microcosm experiments were set up with water samples representing different seasons, years, sampling stations, and dilbit blends. While the alkane fraction of the tested dilbit blends was almost completely degraded after 28 days, the majority of the polycyclic aromatic hydrocarbons (PAHs) remained. The addition of the dispersant Corexit 9500A most often had either no effect or an enhancing effect on dilbit degradation. Dilbit-degrading microbial communities were highly variable between seasons, years, and stations, with dilbit type having little impact on community trajectories. Potential oil-degrading genera showed a clear succession pattern and were for the most part recruited from the "rare biosphere." At the community level, dispersant appeared to stimulate an accelerated enrichment of genera typically associated with hydrocarbon degradation, even in dilbit-free controls. This suggests that dispersant-induced growth of hydrocarbon degraders (and not only increased bioavailability of oil-associated hydrocarbons) contributes to the degradation-enhancing effect previously reported for Corexit 9500A. Western Canada hosts large petroleum deposits, which ultimately enter the market in the form of dilbit. Tanker-based shipping represents the primary means to transport dilbit to international markets. With anticipated increases in production to meet global energy needs, the risk of a dilbit spill is expected to increase. This study investigated the potential of microbial communities naturally present in the waters of a potential dilbit shipping lane to mitigate the effects of a spill. Here we show that microbial degradation of dilbit was mostly limited to -alkanes, while the overall concentration of polycyclic aromatic hydrocarbons, which represent the most toxic fraction of dilbit, decreased only slightly within the time frame of our experiments. We further investigated the effect of the oil dispersant Corexit 9500A on microbial dilbit degradation. Our results highlight the fact that dispersant-associated growth stimulation, and not only increased bioavailability of hydrocarbons and inhibition of specific genera, contributes to the overall effect of dispersant addition.
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http://dx.doi.org/10.1128/AEM.00086-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6498151PMC
May 2019

Nitrogen- and phosphorus-starved Triticum aestivum show distinct belowground microbiome profiles.

PLoS One 2019 20;14(2):e0210538. Epub 2019 Feb 20.

Energy, Mining and Environment Research Centre, National Research Council Canada, Montréal, QC, Canada.

Many plants have natural partnerships with microbes that can boost their nitrogen (N) and/or phosphorus (P) acquisition. To assess whether wheat may have undiscovered associations of these types, we tested if N/P-starved Triticum aestivum show microbiome profiles that are simultaneously different from those of N/P-amended plants and those of their own bulk soils. The bacterial and fungal communities of root, rhizosphere, and bulk soil samples from the Historical Dryland Plots (Lethbridge, Canada), which hold T. aestivum that is grown both under N/P fertilization and in conditions of extreme N/P-starvation, were taxonomically described and compared (bacterial 16S rRNA genes and fungal Internal Transcribed Spacers-ITS). As the list may include novel N- and/or P-providing wheat partners, we then identified all the operational taxonomic units (OTUs) that were proportionally enriched in one or more of the nutrient starvation- and plant-specific communities. These analyses revealed: a) distinct N-starvation root and rhizosphere bacterial communities that were proportionally enriched, among others, in OTUs belonging to families Enterobacteriaceae, Chitinophagaceae, Comamonadaceae, Caulobacteraceae, Cytophagaceae, Streptomycetaceae, b) distinct N-starvation root fungal communities that were proportionally enriched in OTUs belonging to taxa Lulworthia, Sordariomycetes, Apodus, Conocybe, Ascomycota, Crocicreas, c) a distinct P-starvation rhizosphere bacterial community that was proportionally enriched in an OTU belonging to genus Agrobacterium, and d) a distinct P-starvation root fungal community that was proportionally enriched in OTUs belonging to genera Parastagonospora and Phaeosphaeriopsis. Our study might have exposed wheat-microbe connections that can form the basis of novel complementary yield-boosting tools.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0210538PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6382137PMC
October 2019

Comparative Transcriptomics of Cold Growth and Adaptive Features of a Eury- and Steno-Psychrophile.

Front Microbiol 2018 31;9:1565. Epub 2018 Jul 31.

Department of Natural Resource Sciences, McGill University, Sainte-Anne-de-Bellevue, QC, Canada.

Permafrost subzero environments harbor diverse, active communities of microorganisms. However, our understanding of the subzero growth, metabolisms, and adaptive properties of these microbes remains very limited. We performed transcriptomic analyses on two subzero-growing permafrost isolates with different growth profiles in order to characterize and compare their cold temperature growth and cold-adaptive strategies. The two organisms, sp. JG3 (-5 to 30°C) and sp. Eur3 1.2.1 (-5 to 22°C), shared several common responses during low temperature growth, including induction of translation and ribosomal processes, upregulation of nutrient transport, increased oxidative and osmotic stress responses, and stimulation of polysaccharide capsule synthesis. Recombination appeared to be an important adaptive strategy for both isolates at low temperatures, likely as a mechanism to increase genetic diversity and the potential for survival in cold systems. While sp. JG3 favored upregulating iron and amino acid transport, sustaining redox potential, and modulating fatty acid synthesis and composition during growth at -5°C compared to 25°C, sp. Eur3 1.2.1 increased the relative abundance of transcripts involved in primary energy metabolism and the electron transport chain, in addition to signal transduction and peptidoglycan synthesis at 0°C compared to 20°C. The increase in energy metabolism may explain why sp. Eur3 1.2.1 is able to sustain growth rates at 0°C comparable to those at higher temperatures. For sp. JG3, flexibility in use of carbon sources, iron acquisition, control of membrane fatty acid composition, and modulating redox and co-factor potential may be ways in which this organism is able to sustain growth over a wider range of temperatures. Increasing our understanding of the microbes in these habitats helps us better understand active pathways and metabolisms in extreme environments. Identifying novel, thermolabile, and cold-active enzymes from studies such as this is also of great interest to the biotechnology and food industries.
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http://dx.doi.org/10.3389/fmicb.2018.01565DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6080646PMC
July 2018

Long-Term Land Use Affects Phosphorus Speciation and the Composition of Phosphorus Cycling Genes in Agricultural Soils.

Front Microbiol 2018 20;9:1643. Epub 2018 Jul 20.

Swift Current Research and Development Centre, Agriculture and Agri-Food Canada, Swift Current, SK, Canada.

Agriculturally-driven land transformation is increasing globally. Improving phosphorus (P) use efficiency to sustain optimum productivity in diverse ecosystems, based on knowledge of soil P dynamics, is also globally important in light of potential shortages of rock phosphate to manufacture P fertilizer. We investigated P chemical speciation and P cycling with solution P nuclear magnetic resonance, P K-edge X-ray absorption near-edge structure spectroscopy, phosphatase activity assays, and shotgun metagenomics in soil samples from long-term agricultural fields containing four different land-use types (native and tame grasslands, annual croplands, and roadside ditches). Across these land use types, native and tame grasslands showed high accumulation of organic P, principally orthophosphate monoesters, and high acid phosphomonoesterase activity but the lowest abundance of P cycling genes. The proportion of inositol hexaphosphates (IHP), especially the -IHP stereoisomer that likely originates from microbes rather than plants, was significantly increased in native grasslands than croplands. Annual croplands had the largest variances of soil P composition, and the highest potential capacity for P cycling processes based on the abundance of genes coding for P cycling processes. In contrast, roadside soils had the highest soil Olsen-P concentrations, lowest organic P, and highest tricalcium phosphate concentrations, which were likely facilitated by the neutral pH and high exchangeable Ca of these soils. Redundancy analysis demonstrated that IHP by NMR, potential phosphatase activity, Olsen-P, and pH were important P chemistry predictors of the P cycling bacterial community and functional gene composition. Combining chemical and metagenomics results provides important insights into soil P processes and dynamics in different land-use ecosystems.
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http://dx.doi.org/10.3389/fmicb.2018.01643DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6065304PMC
July 2018

Gut Bacterial Microbiota and its Resistome Rapidly Recover to Basal State Levels after Short-term Amoxicillin-Clavulanic Acid Treatment in Healthy Adults.

Sci Rep 2018 07 25;8(1):11192. Epub 2018 Jul 25.

Lallemand Health Solutions Inc., 6100 Royalmount Avenue, Montreal, Quebec, H4P 2R2, Canada.

Clinical effects of antimicrobials and probiotics in combination have been reported, however, little is known about their impact on gut microbiota and its resistome. In this study 16S rRNA gene amplicon, shotgun metagenomics sequencing and antibiotic resistance (ABR) microarray were used on fecal samples of 70 healthy participants, taken at four time points in probiotic (Lactobacillus rhamnosus R0011 and Lactobacillus helveticus R0052) and placebo groups to profile the gut bacterial microbiota and its resistome following administration of amoxicillin-clavulanic acid for one week. Significant shifts in microbiota family composition caused by the antimicrobial in both groups that included decreases in the proportion of Lachnospiraceae, Coriobacteriaceae and unidentified Clostridiales; and notable increases for the proportion of Enterobacteriaceae, Bacteroidaceae and Porphyromonadaceae compared to baseline levels. Resistome showed a corresponding enrichment of ABR genes compared to baseline from such classes as aminoglycosides and beta-lactams that were linked, by in silico inference, to the enrichment of the family Enterobacteriaceae. Despite perturbations caused by short-term antibiotic treatment, both gut microbiota and resistome showed prompt recovery to baseline levels one week after cessation of the antimicrobial. This rapid recovery may be explained by the hypothesis of community resilience.
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http://dx.doi.org/10.1038/s41598-018-29229-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6060159PMC
July 2018

Serratia marcescens Outbreak in a Neonatal Intensive Care Unit: New Insights from Next-Generation Sequencing Applications.

J Clin Microbiol 2018 09 27;56(9). Epub 2018 Aug 27.

Department of Microbiology, Infectious Diseases, and Immunology, Université de Montréal, Montréal, Québec, Canada

is an environmental bacterium that is commonly associated with outbreaks in neonatal intensive care units (NICUs). Investigations of outbreaks require efficient recovery and typing of clinical and environmental isolates. In this study, we investigated how the use of next-generation sequencing applications, such as bacterial whole-genome sequencing (WGS) and bacterial community profiling, could improve outbreak investigations. Phylogenomic links and potential antibiotic resistance genes and plasmids in isolates were investigated using WGS, while bacterial communities and relative abundances of in environmental samples were assessed using sequencing of bacterial phylogenetic marker genes (16S rRNA and genes). Typing results obtained using WGS for the 10 isolates recovered during a NICU outbreak investigation were highly consistent with those obtained using pulsed-field gel electrophoresis (PFGE), the current standard typing method for this bacterium. WGS also allowed the identification of genes associated with antibiotic resistance in all isolates, while no plasmids were detected. Sequencing of the 16S rRNA and genes both showed greater relative abundances of at environmental sampling sites that were in close contact with infected babies. Much lower relative abundances of were observed following disinfection of a room, indicating that the protocol used was efficient. Variations in the bacterial community composition and structure following room disinfection and among sampling sites were also identified through 16S rRNA gene sequencing. Together, results from this study highlight the potential for next-generation sequencing tools to improve and to facilitate outbreak investigations.
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http://dx.doi.org/10.1128/JCM.00235-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6113457PMC
September 2018

Draft Whole-Genome Sequence of the Fluorene-Degrading Sphingobium sp. Strain LB126, Isolated from Polycyclic Aromatic Hydrocarbon-Contaminated Soil.

Genome Announc 2018 Apr 12;6(15). Epub 2018 Apr 12.

Earth & Life Institute, Laboratory of Bioengineering, Catholic University of Louvain, Louvain-la-Neuve, Belgium

We report here the draft whole-genome sequence of a fluorene-degrading bacterium, sp. strain LB126. The genes involved in the upper biodegradation pathway of fluorene are located on a plasmid, and the lower pathway that generates tricarboxylic acid cycle intermediates is initiated by the -cleavage of protocatechuic acid that is chromosomally encoded.
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http://dx.doi.org/10.1128/genomeA.00249-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5897811PMC
April 2018

Soil contamination alters the willow root and rhizosphere metatranscriptome and the root-rhizosphere interactome.

ISME J 2018 03 12;12(3):869-884. Epub 2018 Jan 12.

National Research Council Canada, Energy, Mining and Environment, Montréal, QC, Canada.

Phytoremediation using willows is thought to be a sustainable alternative to traditional remediation techniques involving excavation, transport, and landfilling. However, the complexity of the interaction between the willow and its associated highly diverse microbial communities makes the optimization of phytoremediation very difficult. Here, we have sequenced the rhizosphere metatranscriptome of four willow species and the plant root metatranscriptome for two willow species growing in petroleum hydrocarbon-contaminated and non-contaminated soils on a former petroleum refinery site. Significant differences in the abundance of transcripts related to different bacterial and fungal taxa were observed between willow species, mostly in contaminated soils. When comparing transcript abundance in contaminated vs. non-contaminated soil for each willow species individually, transcripts for many microbial taxa and functions were significantly more abundant in contaminated rhizosphere soil for Salix eriocephala, S. miyabeana and S. purpurea, in contrast to what was observed in the rhizosphere of S. caprea. This agrees with the previously reported sensitivity of S. caprea to contamination, and the superior tolerance of S. miyabeana and S. purpurea to soil contamination at that site. The root metatranscriptomes of two species were compared and revealed that plants transcripts are mainly influenced by willow species, while microbial transcripts mainly responded to contamination. A comparison of the rhizosphere and root metatranscriptomes in the S. purpurea species revealed a complete reorganization of the linkages between root and rhizosphere pathways when comparing willows growing in contaminated and non-contaminated soils, mainly because of large shifts in the rhizosphere metatranscriptome.
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http://dx.doi.org/10.1038/s41396-017-0018-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5864237PMC
March 2018
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