Publications by authors named "Noah Fierer"

177 Publications

Variable influences of soil and seed-associated bacterial communities on the assembly of seedling microbiomes.

ISME J 2021 Mar 29. Epub 2021 Mar 29.

Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, USA.

Plants grown in distinct soils typically harbor distinct microbial communities, but the degree of the soil microbiome influence on plant microbiome assembly remains largely undetermined. We also know that the microbes associated with seeds can contribute to the plant microbiome, but the magnitude of this contribution is likely variable. We quantified the influence of soil and seed microbiomes on the bacterial community composition of seedlings by independently inoculating seeds from a single cultivar of wheat (Triticum aestivum) with 219 unique soil slurries while holding other environmental factors constant, determining the composition of the seed, soil, and seedling bacterial communities via cultivation-independent methods. Soil bacterial communities exert a strong, but variable, influence on seedling bacterial community structure, with the extent of the soil bacterial contribution dependent on the soil in question. By testing a wide range of soils, we were able to show that the specific composition of the seedling microbiome is predictable from knowing which bacterial taxa are found in soil. Although the most ubiquitous taxa associated with the seedlings were seed derived, the contributions of the seed microbiome to the seedling microbiome were variable and dependent on soil bacterial community composition. Together this work improves our predictive understanding of how the plant microbiome assembles and how the seedling microbiome could be directly or indirectly manipulated to improve plant health.
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http://dx.doi.org/10.1038/s41396-021-00967-1DOI Listing
March 2021

The bacterial communities of Alaskan mosses and their contributions to N-fixation.

Microbiome 2021 02 23;9(1):53. Epub 2021 Feb 23.

Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA.

Background: Mosses in high-latitude ecosystems harbor diverse bacterial taxa, including N-fixers which are key contributors to nitrogen dynamics in these systems. Yet the relative importance of moss host species, and environmental factors, in structuring these microbial communities and their N-fixing potential remains unclear. We studied 26 boreal and tundra moss species across 24 sites in Alaska, USA, from 61 to 69° N. We used cultivation-independent approaches to characterize the variation in moss-associated bacterial communities as a function of host species identity and site characteristics. We also measured N-fixation rates via N isotopic enrichment and identified potential N-fixing bacteria using available literature and genomic information.

Results: Host species identity and host evolutionary history were both highly predictive of moss microbiome composition, highlighting strong phylogenetic coherence in these microbial communities. Although less important, light availability and temperature also influenced composition of the moss microbiome. Finally, we identified putative N-fixing bacteria specific to some moss hosts, including potential N-fixing bacteria outside well-studied cyanobacterial clades.

Conclusions: The strong effect of host identity on moss-associated bacterial communities demonstrates mosses' utility for understanding plant-microbe interactions in non-leguminous systems. Our work also highlights the likely importance of novel bacterial taxa to N-fixation in high-latitude ecosystems. Video Abstract.
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http://dx.doi.org/10.1186/s40168-021-01001-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7903681PMC
February 2021

Antarctic Water Tracks: Microbial Community Responses to Variation in Soil Moisture, pH, and Salinity.

Front Microbiol 2021 27;12:616730. Epub 2021 Jan 27.

Department of Biology, Brigham Young University, Provo, UT, United States.

Ice-free soils in the McMurdo Dry Valleys select for taxa able to cope with challenging environmental conditions, including extreme chemical water activity gradients, freeze-thaw cycling, desiccation, and solar radiation regimes. The low biotic complexity of Dry Valley soils makes them well suited to investigate environmental and spatial influences on bacterial community structure. Water tracks are annually wetted habitats in the cold-arid soils of Antarctica that form briefly each summer with moisture sourced from snow melt, ground ice thaw, and atmospheric deposition via deliquescence and vapor flow into brines. Compared to neighboring arid soils, water tracks are highly saline and relatively moist habitats. They represent a considerable area (∼5-10 km) of the Dry Valley terrestrial ecosystem, an area that is expected to increase with ongoing climate change. The goal of this study was to determine how variation in the environmental conditions of water tracks influences the composition and diversity of microbial communities. We found significant differences in microbial community composition between on- and off-water track samples, and across two distinct locations. Of the tested environmental variables, soil salinity was the best predictor of community composition, with members of the phylum being relatively more abundant at higher salinities and the phylum showing the opposite pattern. There was also a significant, inverse relationship between salinity and bacterial diversity. Our results suggest water track formation significantly alters dry soil microbial communities, likely influencing subsequent ecosystem functioning. We highlight how Dry Valley water tracks could be a useful model system for understanding the potential habitability of transiently wetted environments found on the surface of Mars.
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http://dx.doi.org/10.3389/fmicb.2021.616730DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7873294PMC
January 2021

The diversity and function of sourdough starter microbiomes.

Elife 2021 Jan 26;10. Epub 2021 Jan 26.

Department of Biology, Tufts University, Medford, United States.

Humans have relied on sourdough starter microbial communities to make leavened bread for thousands of years, but only a small fraction of global sourdough biodiversity has been characterized. Working with a community-scientist network of bread bakers, we determined the microbial diversity of 500 sourdough starters from four continents. In sharp contrast with widespread assumptions, we found little evidence for biogeographic patterns in starter communities. Strong co-occurrence patterns observed in situ and recreated in vitro demonstrate that microbial interactions shape sourdough community structure. Variation in dough rise rates and aromas were largely explained by acetic acid bacteria, a mostly overlooked group of sourdough microbes. Our study reveals the extent of microbial diversity in an ancient fermented food across diverse cultural and geographic backgrounds.
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http://dx.doi.org/10.7554/eLife.61644DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7837699PMC
January 2021

The Role of Phosphorus Limitation in Shaping Soil Bacterial Communities and Their Metabolic Capabilities.

mBio 2020 10 27;11(5). Epub 2020 Oct 27.

Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, USA

Phosphorus (P) is an essential nutrient that is often in limited supply, with P availability constraining biomass production in many terrestrial ecosystems. Despite decades of work on plant responses to P deficiency and the importance of soil microbes to terrestrial ecosystem processes, how soil microbes respond to, and cope with, P deficiencies remains poorly understood. We studied 583 soils from two independent sample sets that each span broad natural gradients in extractable soil P and collectively represent diverse biomes, including tropical forests, temperate grasslands, and arid shrublands. We paired marker gene and shotgun metagenomic analyses to determine how soil bacterial and archaeal communities respond to differences in soil P availability and to detect corresponding shifts in functional attributes. We identified microbial taxa that are consistently responsive to extractable soil P, with those taxa found in low P soils being more likely to have traits typical of oligotrophic life history strategies. Using environmental niche modeling of genes and gene pathways, we found an enriched abundance of key genes in low P soils linked to the carbon-phosphorus (C-P) lyase and phosphonotase degradation pathways, along with key components of the high-affinity phosphate-specific transporter (Pst) and phosphate regulon (Pho) systems. Taken together, these analyses suggest that catabolism of phosphonates is an important strategy used by bacteria to scavenge phosphate in P-limited soils. Surprisingly, these same pathways are important for bacterial growth in P-limited marine waters, highlighting the shared metabolic strategies used by both terrestrial and marine microbes to cope with P limitation.
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http://dx.doi.org/10.1128/mBio.01718-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7593963PMC
October 2020

Comparing the effects of two different strains of mycobacteria, Mycobacterium vaccae NCTC 11659 and M. vaccae ATCC 15483, on stress-resilient behaviors and lipid-immune signaling in rats.

Brain Behav Immun 2021 Jan 1;91:212-229. Epub 2020 Oct 1.

Department of Integrative Physiology, University of Colorado Boulder, Boulder, CO 80309, USA; Center for Neuroscience, University of Colorado Boulder, Boulder, CO 80309, USA; Center for Microbial Exploration, University of Colorado Boulder, Boulder, CO 80309, USA; Department of Physical Medicine and Rehabilitation and Center for Neuroscience, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; Veterans Health Administration, Rocky Mountain Mental Illness Research Education and Clinical Center (MIRECC), Rocky Mountain Regional Veterans Affairs Medical Center (RMRVAMC), Aurora, CO 80045, USA; Military and Veteran Microbiome: Consortium for Research and Education (MVM-CoRE), Aurora, CO 80045, USA; inVIVO Planetary Health, of the Worldwide Universities Network (WUN), West New York, NJ 07093, USA. Electronic address:

Stress-related disorders, such as posttraumatic stress disorder (PTSD), are highly prevalent and often difficult to treat. In rodents, stress-related, anxiety-like defensive behavioral responses may be characterized by social avoidance, exacerbated inflammation, and altered metabolic states. We have previously shown that, in rodents, subcutaneous injections of a heat-killed preparation of the soil-derived bacterium Mycobacterium vaccae NCTC 11659 promotes stress resilience effects that are associated with immunoregulatory signaling in the periphery and the brain. In the current study, we sought to determine whether treatment with a heat-killed preparation of the closely related M. vaccae type strain, M. vaccae ATCC 15483, would also promote stress-resilience in adult male rats, likely due to biologically similar characteristics of the two strains. Here we show that immunization with either M. vaccae NCTC 11659 or M. vaccae ATCC 15483 prevents stress-induced increases in hippocampal interleukin 6 mRNA expression, consistent with previous studies showing that M. vaccae NCTC 11659 prevents stress-induced increases in peripheral IL-6 secretion, and prevents exaggeration of anxiety-like defensive behavioral responses assessed 24 h after exposure to inescapable tail shock stress (IS) in adult male rats. Analysis of mRNA expression, protein abundance, and flow cytometry data demonstrate overlapping but also unique effects of treatment with the two M. vaccae strains on immunological and metabolic signaling in the host. These data support the hypothesis that treatment with different M. vaccae strains may immunize the host against stress-induced dysregulation of physiology and behavior.
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http://dx.doi.org/10.1016/j.bbi.2020.09.030DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7749860PMC
January 2021

Butterflies Host Characteristic and Phylogenetically Structured Adult-Stage Microbiomes.

Appl Environ Microbiol 2020 11 24;86(24). Epub 2020 Nov 24.

Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, Boulder, Colorado, USA.

Lepidoptera (butterflies and moths) are diverse and ecologically important, yet we know little about how they interact with microbes as adults. Due to metamorphosis, the form and function of their adult-stage microbiomes might be very different from those of microbiomes in the larval stage (caterpillars). We studied adult-stage microbiomes of and closely related passion-vine butterflies (Heliconiini), which are an important model system in evolutionary biology. To characterize the structure and dynamics of heliconiine microbiomes, we used field collections of wild butterflies, 16S rRNA gene sequencing, quantitative PCR, and shotgun metagenomics. We found that butterflies harbor simple and abundant bacterial communities that are moderately consistent among conspecific individuals and over time. Heliconiine microbiomes also exhibited a strong signal of the host phylogeny, with a major distinction between and other butterflies. These patterns were largely driven by differing relative abundances of bacterial phylotypes shared among host species and genera, as opposed to the presence or absence of host-specific phylotypes. We suggest that the phylogenetic structure in heliconiine microbiomes arises from conserved host traits that differentially filter microbes from the environment. While the relative importance of different traits remains unclear, our data indicate that pollen feeding (unique to ) is not a primary driver. Using shotgun metagenomics, we also discovered trypanosomatids and microsporidia to be prevalent in butterfly guts, raising the possibility of antagonistic interactions between eukaryotic parasites and colocalized gut bacteria. Our discovery of characteristic and phylogenetically structured microbiomes provides a foundation for tests of adult-stage microbiome function, a poorly understood aspect of lepidopteran biology. Many insects host microbiomes with important ecological functions. However, the prevalence of this phenomenon is unclear because in many insect taxa, microbiomes have been studied in only part of the life cycle, if at all. A prominent example is butterflies and moths, in which the composition and functional role of adult-stage microbiomes are largely unknown. We comprehensively characterized microbiomes in adult passion-vine butterflies. Butterfly-associated bacterial communities are generally abundant in guts, consistent within populations, and composed of taxa widely shared among hosts. More closely related butterflies harbor more similar microbiomes, with the most dramatic shift in microbiome composition occurring in tandem with a suite of ecological and life history traits unique to the genus Butterflies are also frequently infected with previously undescribed eukaryotic parasites, which may interact with bacteria in important ways. These findings advance our understanding of butterfly biology and insect-microbe interactions generally.
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http://dx.doi.org/10.1128/AEM.02007-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7688219PMC
November 2020

The influence of soil age on ecosystem structure and function across biomes.

Nat Commun 2020 09 18;11(1):4721. Epub 2020 Sep 18.

Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, 80309, USA.

The importance of soil age as an ecosystem driver across biomes remains largely unresolved. By combining a cross-biome global field survey, including data for 32 soil, plant, and microbial properties in 16 soil chronosequences, with a global meta-analysis, we show that soil age is a significant ecosystem driver, but only accounts for a relatively small proportion of the cross-biome variation in multiple ecosystem properties. Parent material, climate, vegetation and topography predict, collectively, 24 times more variation in ecosystem properties than soil age alone. Soil age is an important local-scale ecosystem driver; however, environmental context, rather than soil age, determines the rates and trajectories of ecosystem development in structure and function across biomes. Our work provides insights into the natural history of terrestrial ecosystems. We propose that, regardless of soil age, changes in the environmental context, such as those associated with global climatic and land-use changes, will have important long-term impacts on the structure and function of terrestrial ecosystems across biomes.
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http://dx.doi.org/10.1038/s41467-020-18451-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7501311PMC
September 2020

Volatile organic compounds from leaf litter decomposition alter soil microbial communities and carbon dynamics.

Ecology 2020 10 22;101(10):e03130. Epub 2020 Sep 22.

Department of Soil and Water Systems, University of Idaho, Moscow, Idaho, 83844, USA.

Investigations into the transfer of carbon from plant litter to underlying soil horizons have primarily focused on the leaching of soluble carbon from litter belowground or the mixing of litter directly into soil. However, previous work has largely ignored the role of volatile organic compounds (VOCs) released during litter decomposition. Unlike most leaf carbon, these litter-derived VOCs are able to diffuse directly into the soil matrix. Here, we used a 99-d microcosm experiment to track VOCs produced during microbial decomposition of C-labeled leaf litter into soil carbon fractions where the decomposing litters were only sharing headspace with the soil samples, thus preventing direct contact and aqueous movement of litter carbon. We also determined the effects of these litter-derived VOCs on soil microbial community structure. We demonstrated that the litter VOCs contributed to all measured soil carbon pools. Specifically, VOC-derived carbon accounted for 2.0, 0.61, 0.18, and 0.08% of carbon in the microbial biomass, dissolved organic matter, mineral-associated organic matter, and particulate organic matter pools, respectively. We also show that litter-derived VOCs can affect soil bacterial and fungal community diversity and composition. These findings highlight the importance of an underappreciated pathway where VOCs alter soil microbial communities and carbon dynamics.
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http://dx.doi.org/10.1002/ecy.3130DOI Listing
October 2020

A synthesis of bacterial and archaeal phenotypic trait data.

Sci Data 2020 06 5;7(1):170. Epub 2020 Jun 5.

Department of Biological Sciences, Macquarie University, Sydney, NSW, 2109, Australia.

A synthesis of phenotypic and quantitative genomic traits is provided for bacteria and archaea, in the form of a scripted, reproducible workflow that standardizes and merges 26 sources. The resulting unified dataset covers 14 phenotypic traits, 5 quantitative genomic traits, and 4 environmental characteristics for approximately 170,000 strain-level and 15,000 species-aggregated records. It spans all habitats including soils, marine and fresh waters and sediments, host-associated and thermal. Trait data can find use in clarifying major dimensions of ecological strategy variation across species. They can also be used in conjunction with species and abundance sampling to characterize trait mixtures in communities and responses of traits along environmental gradients.
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http://dx.doi.org/10.1038/s41597-020-0497-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7275036PMC
June 2020

Use of standardized bioinformatics for the analysis of fungal DNA signatures applied to sample provenance.

Forensic Sci Int 2020 May 12;310:110250. Epub 2020 Mar 12.

Department of Molecular Biomedical Sciences, North Carolina State University, 1060 William Moore Dr., Raleigh, NC, 27607, USA; Battelle Memorial Institute, 505 King Ave., Columbus, OH, 43201, USA.

The use of environmental trace material to aid criminal investigations is an ongoing field of research within forensic science. The application of environmental material thus far has focused upon a variety of different objectives relevant to forensic biology, including sample provenance (also referred to as sample attribution). The capability to predict the provenance or origin of an environmental DNA sample would be an advantageous addition to the suite of investigative tools currently available. A metabarcoding approach is often used to predict sample provenance, through the extraction and comparison of the DNA signatures found within different environmental materials, such as the bacteria within soil or fungi within dust. Such approaches are combined with bioinformatics workflows and statistical modelling, often as part of large-scale study, with less emphasis on the investigation of the adaptation of these methods to a smaller scale method for forensic use. The present work was investigating a small-scale approach as an adaptation of a larger metabarcoding study to develop a model for global sample provenance using fungal DNA signatures collected from dust swabs. This adaptation was to facilitate a standardized method for consistent, reproducible sample treatment, including bioinformatics processing and final application of resulting data to the available prediction model. To investigate this small-scale method, 76 DNA samples were treated as anonymous test samples and analyzed using the standardized process to demonstrate and evaluate processing and customized sequence data analysis. This testing included samples originating from countries previously used to train the model, samples artificially mixed to represent multiple or mixed countries, as well as outgroup samples. Positive controls were also developed to monitor laboratory processing and bioinformatics analysis. Through this evaluation we were able to demonstrate that the samples could be processed and analyzed in a consistent manner, facilitated by a relatively user-friendly bioinformatic pipeline for sequence data analysis. Such investigation into standardized analyses and application of metabarcoding data is of key importance for the future use of applied microbiology in forensic science.
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http://dx.doi.org/10.1016/j.forsciint.2020.110250DOI Listing
May 2020

The global-scale distributions of soil protists and their contributions to belowground systems.

Sci Adv 2020 01 24;6(4):eaax8787. Epub 2020 Jan 24.

Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA.

Protists are ubiquitous in soil, where they are key contributors to nutrient cycling and energy transfer. However, protists have received far less attention than other components of the soil microbiome. We used amplicon sequencing of soils from 180 locations across six continents to investigate the ecological preferences of protists and their functional contributions to belowground systems. We complemented these analyses with shotgun metagenomic sequencing of 46 soils to validate the identities of the more abundant protist lineages. We found that most soils are dominated by consumers, although parasites and phototrophs are particularly abundant in tropical and arid ecosystems, respectively. The best predictors of protist composition (primarily annual precipitation) are fundamentally distinct from those shaping bacterial and archaeal communities (namely, soil pH). Some protists and bacteria co-occur globally, highlighting the potential importance of these largely undescribed belowground interactions. Together, this study allowed us to identify the most abundant and ubiquitous protists living in soil, with our work providing a cross-ecosystem perspective on the factors structuring soil protist communities and their likely contributions to soil functioning.
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http://dx.doi.org/10.1126/sciadv.aax8787DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6981079PMC
January 2020

Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities.

mBio 2020 01 21;11(1). Epub 2020 Jan 21.

Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado, USA

Few studies have comprehensively investigated the temporal variability in soil microbial communities despite widespread recognition that the belowground environment is dynamic. In part, this stems from the challenges associated with the high degree of spatial heterogeneity in soil microbial communities and because the presence of relic DNA (DNA from dead cells or secreted extracellular DNA) may dampen temporal signals. Here, we disentangle the relationships among spatial, temporal, and relic DNA effects on prokaryotic and fungal communities in soils collected from contrasting hillslopes in Colorado, USA. We intensively sampled plots on each hillslope over 6 months to discriminate between temporal variability, intraplot spatial heterogeneity, and relic DNA effects on the soil prokaryotic and fungal communities. We show that the intraplot spatial variability in microbial community composition was strong and independent of relic DNA effects and that these spatial patterns persisted throughout the study. When controlling for intraplot spatial variability, we identified significant temporal variability in both plots over the 6-month study. These microbial communities were more dissimilar over time after relic DNA was removed, suggesting that relic DNA hinders the detection of important temporal dynamics in belowground microbial communities. We identified microbial taxa that exhibited shared temporal responses and show that these responses were often predictable from temporal changes in soil conditions. Our findings highlight approaches that can be used to better characterize temporal shifts in soil microbial communities, information that is critical for predicting the environmental preferences of individual soil microbial taxa and identifying linkages between soil microbial community composition and belowground processes. Nearly all microbial communities are dynamic in time. Understanding how temporal dynamics in microbial community structure affect soil biogeochemistry and fertility are key to being able to predict the responses of the soil microbiome to environmental perturbations. Here, we explain the effects of soil spatial structure and relic DNA on the determination of microbial community fluctuations over time. We found that intensive spatial sampling was required to identify temporal effects in microbial communities because of the high degree of spatial heterogeneity in soil and that DNA from nonliving sources masks important temporal patterns. We identified groups of microbes with shared temporal responses and show that these patterns were predictable from changes in soil characteristics. These results provide insight into the environmental preferences and temporal relationships between individual microbial taxa and highlight the importance of considering relic DNA when trying to detect temporal dynamics in belowground communities.
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http://dx.doi.org/10.1128/mBio.02776-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6974563PMC
January 2020

Unlinked rRNA genes are widespread among bacteria and archaea.

ISME J 2020 02 11;14(2):597-608. Epub 2019 Nov 11.

Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, USA.

Ribosomes are essential to cellular life and the genes for their RNA components are the most conserved and transcribed genes in bacteria and archaea. Ribosomal RNA genes are typically organized into a single operon, an arrangement thought to facilitate gene regulation. In reality, some bacteria and archaea do not share this canonical rRNA arrangement-their 16S and 23S rRNA genes are separated across the genome and referred to as "unlinked". This rearrangement has previously been treated as an anomaly or a byproduct of genome degradation in intracellular bacteria. Here, we leverage complete genome and long-read metagenomic data to show that unlinked 16S and 23S rRNA genes are more common than previously thought. Unlinked rRNA genes occur in many phyla, most significantly within Deinococcus-Thermus, Chloroflexi, and Planctomycetes, and occur in differential frequencies across natural environments. We found that up to 41% of rRNA genes in soil were unlinked, in contrast to the human gut, where all sequenced rRNA genes were linked. The frequency of unlinked rRNA genes may reflect meaningful life history traits, as they tend to be associated with a mix of slow-growing free-living species and intracellular species. We speculate that unlinked rRNA genes may confer selective advantages in some environments, though the specific nature of these advantages remains undetermined and worthy of further investigation. More generally, the prevalence of unlinked rRNA genes in poorly-studied taxa serves as a reminder that paradigms derived from model organisms do not necessarily extend to the broader diversity of bacteria and archaea.
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http://dx.doi.org/10.1038/s41396-019-0552-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6976660PMC
February 2020

The Future of Environmental DNA in Forensic Science.

Appl Environ Microbiol 2020 01 7;86(2). Epub 2020 Jan 7.

Department of Applied Ecology, North Carolina State University, Raleigh, North Carolina, USA.

DNA sequencing technologies continue to improve, and there has been a corresponding expansion of DNA-based applications in the forensic sciences. DNA recovered from dust and environmental debris can be used to identify the organisms associated with these sample types, including bacteria, plants, fungi, and insects. Such results can then be leveraged to discern sample origin or geolocation and investigate individual identification. Here, we take a critical look at the current DNA-based technologies using microbiome and environmental sample sources that are focused on the generation of some investigative tools for use in forensic science. We discuss the pitfalls and contentions associated with the use of these techniques and highlight some of the future research required to expand the utility of these methods in the forensic sciences.
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http://dx.doi.org/10.1128/AEM.01504-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6952231PMC
January 2020

Earthworms' place on Earth.

Authors:
Noah Fierer

Science 2019 10;366(6464):425-426

Department of Ecology and Evolutionary Biology, Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO 80305, USA.

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http://dx.doi.org/10.1126/science.aaz5670DOI Listing
October 2019

Ecological and Genomic Attributes of Novel Bacterial Taxa That Thrive in Subsurface Soil Horizons.

mBio 2019 10 1;10(5). Epub 2019 Oct 1.

Department of Ecology and Evolutionary Biology, Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado, USA

While most bacterial and archaeal taxa living in surface soils remain undescribed, this problem is exacerbated in deeper soils, owing to the unique oligotrophic conditions found in the subsurface. Additionally, previous studies of soil microbiomes have focused almost exclusively on surface soils, even though the microbes living in deeper soils also play critical roles in a wide range of biogeochemical processes. We examined soils collected from 20 distinct profiles across the United States to characterize the bacterial and archaeal communities that live in subsurface soils and to determine whether there are consistent changes in soil microbial communities with depth across a wide range of soil and environmental conditions. We found that bacterial and archaeal diversity generally decreased with depth, as did the degree of similarity of microbial communities to those found in surface horizons. We observed five phyla that consistently increased in relative abundance with depth across our soil profiles: , , , and candidate phyla GAL15 and (formerly AD3). Leveraging the unusually high abundance of at depth, we assembled genomes representative of this candidate phylum and identified traits that are likely to be beneficial in low-nutrient environments, including the synthesis and storage of carbohydrates, the potential to use carbon monoxide (CO) as a supplemental energy source, and the ability to form spores. Together these attributes likely allow members of the candidate phylum to flourish in deeper soils and provide insight into the survival and growth strategies employed by the microbes that thrive in oligotrophic soil environments. Soil profiles are rarely homogeneous. Resource availability and microbial abundances typically decrease with soil depth, but microbes found in deeper horizons are still important components of terrestrial ecosystems. By studying 20 soil profiles across the United States, we documented consistent changes in soil bacterial and archaeal communities with depth. Deeper soils harbored communities distinct from those of the more commonly studied surface horizons. Most notably, we found that the candidate phylum (formerly AD3) was often dominant in subsurface soils, and we used genomes from uncultivated members of this group to identify why these taxa are able to thrive in such resource-limited environments. Simply digging deeper into soil can reveal a surprising number of novel microbes with unique adaptations to oligotrophic subsurface conditions.
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http://dx.doi.org/10.1128/mBio.01318-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6775450PMC
October 2019

Microbial responses to warming enhance soil carbon loss following translocation across a tropical forest elevation gradient.

Ecol Lett 2019 Nov 6;22(11):1889-1899. Epub 2019 Sep 6.

School of Geosciences, University of Edinburgh, Crew Building, Kings Buildings, Edinburgh, EH9 3FF, UK.

Tropical soils contain huge carbon stocks, which climate warming is projected to reduce by stimulating organic matter decomposition, creating a positive feedback that will promote further warming. Models predict that the loss of carbon from warming soils will be mediated by microbial physiology, but no empirical data are available on the response of soil carbon and microbial physiology to warming in tropical forests, which dominate the terrestrial carbon cycle. Here we show that warming caused a considerable loss of soil carbon that was enhanced by associated changes in microbial physiology. By translocating soils across a 3000 m elevation gradient in tropical forest, equivalent to a temperature change of ± 15 °C, we found that soil carbon declined over 5 years by 4% in response to each 1 °C increase in temperature. The total loss of carbon was related to its original quantity and lability, and was enhanced by changes in microbial physiology including increased microbial carbon-use-efficiency, shifts in community composition towards microbial taxa associated with warmer temperatures, and increased activity of hydrolytic enzymes. These findings suggest that microbial feedbacks will cause considerable loss of carbon from tropical forest soils in response to predicted climatic warming this century.
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http://dx.doi.org/10.1111/ele.13379DOI Listing
November 2019

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

ISME J 2019 12 6;13(12):3126-3130. Epub 2019 Aug 6.

Department of Biological Sciences, University of Southern California, Los Angeles, CA, 90089, USA.

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.
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http://dx.doi.org/10.1038/s41396-019-0484-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6863901PMC
December 2019

Global ecological predictors of the soil priming effect.

Nat Commun 2019 08 2;10(1):3481. Epub 2019 Aug 2.

Departamento de Biología y Geología, Física y Química Inorgánica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, Calle Tulipán Sin Número, 28933, Móstoles, Spain.

Identifying the global drivers of soil priming is essential to understanding C cycling in terrestrial ecosystems. We conducted a survey of soils across 86 globally-distributed locations, spanning a wide range of climates, biotic communities, and soil conditions, and evaluated the apparent soil priming effect using C-glucose labeling. Here we show that the magnitude of the positive apparent priming effect (increase in CO release through accelerated microbial biomass turnover) was negatively associated with SOC content and microbial respiration rates. Our statistical modeling suggests that apparent priming effects tend to be negative in more mesic sites associated with higher SOC contents. In contrast, a single-input of labile C causes positive apparent priming effects in more arid locations with low SOC contents. Our results provide solid evidence that SOC content plays a critical role in regulating apparent priming effects, with important implications for the improvement of C cycling models under global change scenarios.
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http://dx.doi.org/10.1038/s41467-019-11472-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6677791PMC
August 2019

A Global Survey of Mycobacterial Diversity in Soil.

Appl Environ Microbiol 2019 09 14;85(17). Epub 2019 Aug 14.

Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, USA

Mycobacteria are a diverse bacterial group ubiquitous in many soil and aquatic environments. Members of this group have been associated with human and other animal diseases, including the nontuberculous mycobacteria (NTM), which are of growing relevance to public health worldwide. Although soils are often considered an important source of environmentally acquired NTM infections, the biodiversity and ecological preferences of soil mycobacteria remain largely unexplored across contrasting climates and ecosystem types. Using a culture-independent approach by combining 16S rRNA marker gene sequencing with mycobacterium-specific gene sequencing, we analyzed the diversity, distributions, and environmental preferences of soil-dwelling mycobacteria in 143 soil samples collected from a broad range of ecosystem types. The surveyed soils harbored highly diverse mycobacterial communities that span the full extent of the known mycobacterial phylogeny, with most soil mycobacteria (97% of mycobacterial clades) belonging to previously undescribed lineages. While mycobacteria tended to have higher relative abundances in cool, wet, and acidic soil environments, several individual mycobacterial clades had contrasting environmental preferences. We identified the environmental preferences of many mycobacterial clades, including the clinically relevant complex that was more commonly detected in wet and acidic soils. However, most of the soil mycobacteria detected were not closely related to known pathogens, calling into question previous assumptions about the general importance of soil as a source of NTM infections. Together, this work provides novel insights into the diversity, distributions, and ecological preferences of soil mycobacteria and lays the foundation for future efforts to link mycobacterial phenotypes to their distributions. Mycobacteria are common inhabitants of soil, and while most members of this bacterial group are innocuous, some mycobacteria can cause environmentally acquired infections of humans and other animals. Human infections from nontuberculous mycobacteria (NTM) are increasingly prevalent worldwide, and some areas appear to be "hotspots" for NTM disease. While exposure to soil is frequently implicated as an important mode of NTM transmission, the diversity, distributions, and ecological preferences of soil mycobacteria remain poorly understood. We analyzed 143 soils from a range of ecosystems and found that mycobacteria and lineages within the group often exhibited predictable preferences for specific environmental conditions. Soils harbor large amounts of previously undescribed mycobacterial diversity, and lineages that include known pathogens were rarely detected in soil. Together, these findings suggest that soil is an unlikely source of many mycobacterial infections. The biogeographical patterns we documented lend insight into the ecology of this important group of soil-dwelling bacteria.
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http://dx.doi.org/10.1128/AEM.01180-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6696970PMC
September 2019

Metagenomic analyses reveal previously unrecognized variation in the diets of sympatric Old World monkey species.

PLoS One 2019 26;14(6):e0218245. Epub 2019 Jun 26.

Department of Environmental Studies, University of Colorado, Boulder, CO, United States of America.

Insectivory, or the consumption of insects and other arthropods, is a significant yet cryptic component of omnivorous primate diets. Here, we used high-throughput DNA sequencing to identify arthropods from fecal DNA and assess variation in insectivory by closely-related sympatric primates. We identified arthropod prey taxa and tested the hypothesis that variation in insectivory facilitates niche differentiation and coexistence among closely-related species with high dietary overlap. We collected 233 fecal samples from redtail (Cercopithecus ascanius; n = 118) and blue monkeys (C. mitis; n = 115) and used a CO1 metabarcoding approach to identify arthropod DNA in each fecal sample. Arthropod DNA was detected in 99% of samples (N = 223 samples), and a total of 68 families (15 orders) were identified. Redtails consumed arthropods from 54 families, of which 12 (21.8%) were absent from blue monkey samples. Blue monkeys consumed arthropods from 56 families, of which 14 (24.6%) were absent from redtail samples. For both species, >97% of taxa present belonged to four orders (Araneae, Diptera, Hymenoptera, Lepidoptera). Redtail samples contained more Lepidoptera taxa (p<0.05), while blue monkey samples contained more Araneae (p<0.05). Blue monkeys consumed a greater diversity of arthropod taxa than redtail monkeys (p<0.05); however, the average number of arthropod families present per fecal sample was greater in the redtail monkey samples (p<0.05). These results indicate that while overlap exists in the arthropod portion of their diets, 20-25% of taxa consumed are unique to each group. Our findings suggest that variation in arthropod intake may help decrease dietary niche overlap and hence facilitate coexistence of closely-related primate species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0218245PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6594596PMC
February 2020

Microbial Dynamics of Biosand Filters and Contributions of the Microbial Food Web to Effective Treatment of Wastewater-Impacted Water Sources.

Appl Environ Microbiol 2019 09 14;85(17). Epub 2019 Aug 14.

Center for Interdisciplinary Research in Environmental Sciences, University of Colorado, Boulder, Colorado, USA

Biosand filtration systems are widely used for drinking water treatment, from household-level, intermittently operated filters to large-scale continuous municipal systems. While it is well-established that microbial activity within the filter is essential for the removal of potential pathogens and other contaminants, the microbial ecology of these systems and how microbial succession relates to their performance remain poorly resolved. We determined how different source waters influence the composition, temporal dynamics, and performance of microbial communities in intermittently operated biosand filters. We operated lab-scale biosand filters, adding daily inputs from two contrasting water sources with differing nutrient concentrations and found that total coliform removal increased and became less variable after 4 weeks, regardless of water source. Total effluent biomass was also lower than total influent biomass for both water sources. Bacterial community composition, assessed via cultivation-independent DNA sequencing, varied by water source, sample type (influent, effluent, or sand), and time. Despite these differences, we identified specific taxa that were consistently removed, including common aquatic and wastewater bacteria. In contrast, taxa consistently more abundant in the sand and effluent included predatory, intracellular, and symbiotic bacteria. Although microbial activities are known to contribute to the effectiveness of biosand filtration for drinking water treatment, we have a limited understanding of what microbial groups are most effectively removed, colonize the sand, or make it through the filter. This study tracked the microbial communities in the influent, sand, and effluent of lab-scale, intermittently operated biosand filters over 8 weeks. These results represent the most detailed and time-resolved investigation of the microbial communities in biosand filters typical of those implemented at the household level in many developing countries. We show the importance of the microbial food web in biosand filtration, and we identified taxa that are preferentially removed from wastewater-impacted water sources. We found consistent patterns in filter effectiveness from source waters with differing nutrient loads and, likewise, identified specific bacterial taxa that were consistently more abundant in effluent waters, taxa that are important targets for further study and posttreatment.
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http://dx.doi.org/10.1128/AEM.01142-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6696957PMC
September 2019

Not all animals need a microbiome.

FEMS Microbiol Lett 2019 05;366(10)

Department of Ecology & Evolutionary Biology, University of Colorado at Boulder, 216 UCB, Boulder, CO 80309, USA.

It is often taken for granted that all animals host and depend upon a microbiome, yet this has only been shown for a small proportion of species. We propose that animals span a continuum of reliance on microbial symbionts. At one end are the famously symbiont-dependent species such as aphids, humans, corals and cows, in which microbes are abundant and important to host fitness. In the middle are species that may tolerate some microbial colonization but are only minimally or facultatively dependent. At the other end are species that lack beneficial symbionts altogether. While their existence may seem improbable, animals are capable of limiting microbial growth in and on their bodies, and a microbially independent lifestyle may be favored by selection under some circumstances. There is already evidence for several 'microbiome-free' lineages that represent distantly related branches in the animal phylogeny. We discuss why these animals have received such little attention, highlighting the potential for contaminants, transients, and parasites to masquerade as beneficial symbionts. We also suggest ways to explore microbiomes that address the limitations of DNA sequencing. We call for further research on microbiome-free taxa to provide a more complete understanding of the ecology and evolution of macrobe-microbe interactions.
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http://dx.doi.org/10.1093/femsle/fnz117DOI Listing
May 2019

Changes in belowground biodiversity during ecosystem development.

Proc Natl Acad Sci U S A 2019 04 15;116(14):6891-6896. Epub 2019 Mar 15.

Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO 80309.

Belowground organisms play critical roles in maintaining multiple ecosystem processes, including plant productivity, decomposition, and nutrient cycling. Despite their importance, however, we have a limited understanding of how and why belowground biodiversity (bacteria, fungi, protists, and invertebrates) may change as soils develop over centuries to millennia (pedogenesis). Moreover, it is unclear whether belowground biodiversity changes during pedogenesis are similar to the patterns observed for aboveground plant diversity. Here we evaluated the roles of resource availability, nutrient stoichiometry, and soil abiotic factors in driving belowground biodiversity across 16 soil chronosequences (from centuries to millennia) spanning a wide range of globally distributed ecosystem types. Changes in belowground biodiversity during pedogenesis followed two main patterns. In lower-productivity ecosystems (i.e., drier and colder), increases in belowground biodiversity tracked increases in plant cover. In more productive ecosystems (i.e., wetter and warmer), increased acidification during pedogenesis was associated with declines in belowground biodiversity. Changes in the diversity of bacteria, fungi, protists, and invertebrates with pedogenesis were strongly and positively correlated worldwide, highlighting that belowground biodiversity shares similar ecological drivers as soils and ecosystems develop. In general, temporal changes in aboveground plant diversity and belowground biodiversity were not correlated, challenging the common perception that belowground biodiversity should follow similar patterns to those of plant diversity during ecosystem development. Taken together, our findings provide evidence that ecological patterns in belowground biodiversity are predictable across major globally distributed ecosystem types and suggest that shifts in plant cover and soil acidification during ecosystem development are associated with changes in belowground biodiversity over centuries to millennia.
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http://dx.doi.org/10.1073/pnas.1818400116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6452688PMC
April 2019

A Phylogenetic and Functional Perspective on Volatile Organic Compound Production by .

mSystems 2019 Mar-Apr;4(2). Epub 2019 Mar 5.

Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Boulder, Colorado, USA.

Soil microbes produce an immense diversity of metabolites, including volatile organic compounds (VOCs), which can shape the structure and function of microbial communities. VOCs mediate a multitude of microbe-microbe interactions, including antagonism. Despite their importance, the diversity and functional relevance of most microbial volatiles remain uncharacterized. We assembled a taxonomically diverse collection of 48 isolated from soil and airborne dust and surveyed the VOCs produced by these strains on two different medium types using gas chromatography-mass spectrometry (GC-MS). We detected 126 distinct VOCs and structurally identified approximately 20% of these compounds, which were predominately C to C hetero-VOCs, including (oxygenated) alcohols, ketones, esters, and nitrogen- and sulfur-containing compounds. Each strain produced a unique VOC profile. While the most common VOCs were likely by-products of primary metabolism, most of the VOCs were strain specific. We observed a strong taxonomic and phylogenetic signal for VOC profiles, suggesting their role in finer-scale patterns of ecological diversity. Finally, we investigated the functional potential of these VOCs by assessing their effects on growth rates of both pathogenic and nonpathogenic pseudomonad strains. We identified sets of VOCs that correlated with growth inhibition and stimulation, information that may facilitate the development of microbial VOC-based pathogen control strategies. Soil microbes produce a diverse array of natural products, including volatile organic compounds (VOCs). Volatile compounds are important molecules in soil habitats, where they mediate interactions between bacteria, fungi, insects, plants, and animals. We measured the VOCs produced by a broad diversity of soil- and dust-dwelling . We detected a total of 126 unique volatile compounds, and each strain produced a unique combination of VOCs. While some of the compounds were produced by many strains, most were strain specific. Importantly, VOC profiles were more similar between closely related strains, indicating that evolutionary and ecological processes generate predictable patterns of VOC production. Finally, we observed that actinobacterial VOCs had both stimulatory and inhibitory effects on the growth of bacteria that represent a plant-beneficial symbiont and a plant-pathogenic strain, information that may lead to the development of novel strategies for plant disease prevention.
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http://dx.doi.org/10.1128/mSystems.00295-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6401417PMC
March 2019

Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation.

Nat Ecol Evol 2019 01 14;3(2):223-231. Epub 2019 Jan 14.

Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA.

Climate warming may stimulate microbial metabolism of soil carbon, causing a carbon-cycle-climate feedback whereby carbon is redistributed from the soil to atmospheric CO. The magnitude of this feedback is uncertain, in part because warming-induced shifts in microbial physiology and/or community composition could retard or accelerate soil carbon losses. Here, we measure microbial respiration rates for soils collected from 22 sites in each of 3 years, at locations spanning boreal to tropical climates. Respiration was measured in the laboratory with standard temperatures, moisture and excess carbon substrate, to allow physiological and community effects to be detected independent of the influence of these abiotic controls. Patterns in respiration for soils collected across the climate gradient are consistent with evolutionary theory on physiological responses that compensate for positive effects of temperature on metabolism. Respiration rates per unit microbial biomass were as much as 2.6 times higher for soils sampled from sites with a mean annual temperature of -2.0 versus 21.7 °C. Subsequent 100-d incubations suggested differences in the plasticity of the thermal response among microbial communities, with communities sampled from sites with higher mean annual temperature having a more plastic response. Our findings are consistent with adaptive metabolic responses to contrasting thermal regimes that are also observed in plants and animals. These results may help build confidence in soil-carbon-climate feedback projections by improving understanding of microbial processes represented in biogeochemical models.
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http://dx.doi.org/10.1038/s41559-018-0771-4DOI Listing
January 2019

Fungal diversity regulates plant-soil feedbacks in temperate grassland.

Sci Adv 2018 11 28;4(11):eaau4578. Epub 2018 Nov 28.

School of Earth and Environmental Sciences, Michael Smith Building, The University of Manchester, Oxford Road, Manchester M13 9PT, UK.

Feedbacks between plants and soil microbial communities play an important role in vegetation dynamics, but the underlying mechanisms remain unresolved. Here, we show that the diversity of putative pathogenic, mycorrhizal, and saprotrophic fungi is a primary regulator of plant-soil feedbacks across a broad range of temperate grassland plant species. We show that plant species with resource-acquisitive traits, such as high shoot nitrogen concentrations and thin roots, attract diverse communities of putative fungal pathogens and specialist saprotrophs, and a lower diversity of mycorrhizal fungi, resulting in strong plant growth suppression on soil occupied by the same species. Moreover, soil properties modulate feedbacks with fertile soils, promoting antagonistic relationships between soil fungi and plants. This study advances our capacity to predict plant-soil feedbacks and vegetation dynamics by revealing fundamental links between soil properties, plant resource acquisition strategies, and the diversity of fungal guilds in soil.
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http://dx.doi.org/10.1126/sciadv.aau4578DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6261650PMC
November 2018

Linking bacterial community composition to soil salinity along environmental gradients.

ISME J 2019 03 16;13(3):836-846. Epub 2018 Nov 16.

Department of Biology, Section of Microbial Ecology, Lund University, Lund, Sweden.

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.
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http://dx.doi.org/10.1038/s41396-018-0313-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6461869PMC
March 2019