Summary
Mosses are critical components of boreal ecosystems where they typically account for a large proportion of net primary productivity and harbour diverse bacterial communities that can be the ...major source of biologically‐fixed nitrogen in these ecosystems. Despite their ecological importance, we have limited understanding of how microbial communities vary across boreal moss species and the extent to which local site conditions may influence the composition of these bacterial communities. We used marker gene sequencing to analyze bacterial communities associated with seven boreal moss species collected near Fairbanks, AK, USA. We found that host identity was more important than site in determining bacterial community composition and that mosses harbour diverse lineages of potential N2‐fixers as well as an abundance of novel taxa assigned to understudied bacterial phyla (including candidate phylum WPS‐2). We performed shotgun metagenomic sequencing to assemble genomes from the WPS‐2 candidate phylum and found that these moss‐associated bacteria are likely anoxygenic phototrophs capable of carbon fixation via RuBisCo with an ability to utilize byproducts of photorespiration from hosts via a glyoxylate shunt. These results give new insights into the metabolic capabilities of understudied bacterial lineages that associate with mosses and the importance of plant hosts in shaping their microbiomes.
Nitrogen (N₂)-fixing moss microbial communities play key roles in nitrogen cycling of boreal forests. Forest type and leaf litter inputs regulate moss abundance, but how they control moss microbiomes ...and N₂-fixation remains understudied. We examined the impacts of forest type and broadleaf litter on microbial community composition and N₂-fixation rates of Hylocomium splendens and Pleurozium schreberi.
We conducted a moss transplant and leaf litter manipulation experiment at three sites with paired paper birch (Betula neoalaskana) and black spruce (Picea mariana) stands in Alaska. We characterized bacterial communities using marker gene sequencing, determined N₂-fixation rates using stable isotopes (15N₂) and measured environmental covariates.
Mosses native to and transplanted into spruce stands supported generally higher N₂-fixation and distinct microbial communities compared to similar treatments in birch stands. High leaf litter inputs shifted microbial community composition for both moss species and reduced N₂-fixation rates for H. splendens, which had the highest rates. N₂-fixation was positively associated with several bacterial taxa, including cyanobacteria.
The moss microbiome and environmental conditions controlled N₂-fixation at the stand and transplant scales. Predicted shifts from spruce- to deciduous-dominated stands will interact with the relative abundances of mosses supporting different microbiomes and N₂-fixation rates, which could affect stand-level N inputs.
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.
Genome-resolved environmental metagenomic sequencing has uncovered substantial previously unrecognized microbial diversity relevant for understanding the ecology and evolution of the biosphere, ...providing a more nuanced view of the distribution and ecological significance of traits including phototrophy across diverse niches. Recently, the capacity for bacteriochlorophyll-based anoxygenic photosynthesis has been proposed in the uncultured bacterial WPS-2 phylum (recently proposed as
Eremiobacterota) that are in close association with boreal moss. Here, we use phylogenomic analysis to investigate the diversity and evolution of phototrophic WPS-2. We demonstrate that phototrophic WPS-2 show significant genetic and metabolic divergence from other phototrophic and non-phototrophic lineages. The genomes of these organisms encode a new family of anoxygenic Type II photochemical reaction centers and other phototrophy-related proteins that are both phylogenetically and structurally distinct from those found in previously described phototrophs. We propose the name
Baltobacterales for the order-level aerobic WPS-2 clade which contains phototrophic lineages, from the Greek for "bog" or "swamp," in reference to the typical habitat of phototrophic members of this clade.
Abstract
Background
Mosses in high-latitude ecosystems harbor diverse bacterial taxa, including N
2
-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
2
-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
2
-fixation rates via
15
N
2
isotopic enrichment and identified potential N
2
-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
2
-fixing bacteria specific to some moss hosts, including potential N
2
-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
2
-fixation in high-latitude ecosystems.
From the aboveground vegetation to the belowground microbes, terrestrial communities differ between the highly divergent alpine (above treeline) and subalpine (below treeline) ecosystems. Yet, much ...less is known about the partitioning of microbial communities between alpine and subalpine lakes. Our goal was to determine whether the composition of bacterioplankton communities of high-elevation mountain lakes differed across treeline, identify key players in driving the community composition, and identify potential environmental factors that may be driving differences. To do so, we compared bacterial community composition (using 16S rDNA sequencing) of alpine and subalpine lakes in the Southern Rocky Mountain ecoregion at two time points: once in the early summer and once in the late summer. In the early summer (July), shortly after peak runoff, bacterial communities of alpine lakes were distinct from subalpine lakes. Interestingly, by the end of the summer (approximately 5 weeks after the first visit in August), bacterial communities of alpine and subalpine lakes were no longer distinct. Several bacterial amplicon sequence variants (ASVs) were also identified as key players by significantly contributing to the community dissimilarity. The community divergence across treeline found in the early summer was correlated with several environmental factors, including dissolved organic carbon (DOC), pH, chlorophyll-a (chl-a), and total dissolved nitrogen (TDN). In this paper, we offer several potential scenarios driven by both biotic and abiotic factors that could lead to the observed patterns. While the mechanisms for these patterns are yet to be determined, the community dissimilarity in the early summer correlates with the timing of increased hydrologic connections with the terrestrial environment. Springtime snowmelt brings the flushing of mountain watersheds that connects terrestrial and aquatic ecosystems. This connectivity declines precipitously throughout the summer after snowmelt is complete. Regional climate change is predicted to bring alterations to precipitation and snowpack, which can modify the flushing of solutes, nutrients, and terrestrial microbes into lakes. Future preservation of the unique alpine lake ecosystem is dependent on a better understanding of ecosystem partitioning across treeline and careful consideration of terrestrial-aquatic connections in mountain watersheds.
The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal ...(prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability.
Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth.
Wastewater microbial communities are not static and can vary significantly across time and space, but this variation and the factors driving the observed spatiotemporal variation often remain ...undetermined. We used a shotgun metagenomic approach to investigate changes in wastewater microbial communities across 17 locations in a sewer network, with samples collected from each location over a 3-week period. Fecal material-derived bacteria constituted a relatively small fraction of the taxa found in the collected samples, highlighting the importance of environmental sources to the sewage microbiome. The prokaryotic communities were highly variable in composition depending on the location within the sampling network, and this spatial variation was most strongly associated with location-specific differences in sewage pH. However, we also observed substantial temporal variation in the composition of the prokaryotic communities at individual locations. This temporal variation was asynchronous across sampling locations, emphasizing the importance of independently considering both spatial and temporal variation when assessing the wastewater microbiome. The spatiotemporal patterns in viral community composition closely tracked those of the prokaryotic communities, allowing us to putatively identify the bacterial hosts of some of the dominant viruses in these systems. Finally, we found that antibiotic resistance gene profiles also exhibit a high degree of spatiotemporal variability, with most of these genes unlikely to be derived from fecal bacteria. Together, these results emphasize the dynamic nature of the wastewater microbiome, the challenges associated with studying these systems, and the utility of metagenomic approaches for building a multifaceted understanding of these microbial communities and their functional attributes.
Sewage systems harbor extensive microbial diversity, including microbes derived from both human and environmental sources. Studies of the sewage microbiome are useful for monitoring public health and the health of our infrastructure, but the sewage microbiome can be highly variable in ways that are often unresolved. We sequenced DNA recovered from wastewater samples collected over a 3-week period at 17 locations in a single sewer system to determine how these communities vary across time and space. Most of the wastewater bacteria, and the antibiotic resistance genes they harbor, were not derived from human feces, but human usage patterns did impact how the amounts and types of bacteria and bacterial genes we found in these systems varied over time. Likewise, the wastewater communities, including both bacteria and their viruses, varied depending on location within the sewage network, highlighting the challenges and opportunities in efforts to monitor and understand the sewage microbiome.
Rhizosphere microbial communities play essential roles in plant growth and health, with plant-derived carbon serving as the primary resource fueling the growth and activity of these root-associated ...communities. However, not all rhizosphere microbes are likely equivalent in their ability to metabolize root-derived carbon inputs, and far fewer studies have sought to identify the rhizosphere taxa, and the traits of those taxa that actively consume plant photosynthates. Here, we labeled wheat plants (Triticum aestivum L.) with 13C–CO2, combining stable isotope probing, quantitative PCR, marker gene sequencing, and shotgun metagenomic sequencing to identify rhizosphere microbes that metabolized plant-derived carbon and their genomic attributes. Those rhizosphere taxa that incorporated the plant-derived 13C were not necessarily the most abundant taxa in the rhizosphere. Rhizosphere microbes clearly differed in their capacity to consume plant-derived carbon, with the bacterial photosynthate consumers having distinct metabolic and genomic profiles with higher estimated potential growth rates and more genes associated with carbon metabolism, resource uptake, and potential for plant growth promotion. Together, this work highlights the important roles and the differential contributions of rhizosphere microbes to belowground carbon dynamics, building a more nuanced understanding of the complexity of plant-microbe interactions in the rhizosphere.
•Rhizosphere microbes differed in their capacity to consume plant-derived carbon.•Bacterial photosynthate consumers have higher estimated potential growth rates.•Bacterial photosynthate consumers have more genes associated with carbon dynamics.
Soil carbon (C) sequestration has been proposed as one means to mitigate the effects of climate change and to guarantee food safety. However, forest conversion to managed land uses can deplete soil C ...stocks and affect soil microbial communities, potentially impacting a wide range of ecosystem services. Our objective was to investigate the effect of forest conversion to intensive land uses on soil C dynamics and soil microbial community structure and function in the subtropical portion of the Atlantic Forest biome. We evaluated four land uses - forest fragment, grassland, and agriculture with five or fifty years of cultivation. We analyzed soil C pools, edaphic variables, and soil bacterial/archaeal (16S) and fungal (ITS) communities. Forest conversion to managed land uses reduced soil C stocks and altered soil microbial community structure, with implications for soil C dynamics. Bacterial/archaeal and fungal community composition were strongly correlated with pH, base saturation, and calcium (Ca) and magnesium (Mg) content. However, soil C pools were not associated with potential extracellular enzyme activity or microbial diversity. Finally, the fungal species Mortierella minutissima ASV_1 and several bacterial groups were positively correlated with soil C stocks, potentially representing indicators of soil C storage. Our study indicates that land use change affects the interplay between soil microbial communities and soil C pools, with consequences to soil C storage. Our findings may support the development of soil C enhancement programs within the Atlantic Forest biome.
•The conversion from forest to managed land uses reduced soil carbon (C) stocks.•Potential beta-glucosidase and arylsulfatase activity were not related to soil C.•Land use shapes microbial associations with soil carbon pools in subtropical soils.
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