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At least 19 records

Environmental stress mediates groundwater microbial community assembly

Community assembly describes how different ecological processes shape microbial community composition and structure. How environmental factors impact community assembly remains elusive. Here we sampled microbial communities and >200 biogeochemical variables in groundwater at the Oak Ridge Field Research Center, a former nuclear waste disposal site, and developed a theoretical framework to conceptualize the relationships between community assembly processes and environmental stresses. We found that stochastic assembly processes were critical (>60% on average) in shaping community structure, but their relative importance decreased as stress increased. Dispersal limitation and ‘drift’ related to random birth and death had negative correlations with stresses, whereas the selection processes leading to dissimilar communities increased with stresses, primarily related to pH, cobalt and molybdenum. Assembly mechanisms also varied greatly among different phylogenetic groups. As a result, our findings highlight the importance of microbial dispersal limitation and environmental heterogeneity in ecosystem restoration and management.

54 ENVIRONMENTAL SCIENCES↗

Respiration data, microbial community assembly data, and FTICR-MS data associated with: “Disturbance Triggers Non-Linear Microbe-Environment Feedbacks. Sengupta et al., 2021, Biogeosciences”

This data package is associated with the manuscript “Disturbance Triggers Non-Linear Microbe-Environment Feedbacks, in revision in Biogeosciences (Sengupta et al. and 2021;https://bg.copernicus.org/preprints/bg-2021-51/). The study used hyporheic zone sediments as a model system to provide an integrated view of how disturbance modulates linkages among microbial ecology, biogeochemistry, and organic matter thermodynamics. Laboratory experiments exposed hyporheic sediment to varying wetting/drying dynamics. Data types include dissolved oxygen rates used to derive respiration rates, Fourier-transform ion cyclotron resonance mass spectrometry (FTICR-MS) data used to derive thermodynamic properties of organic matter, and microbial community assembly metrics derived from amplicon-sequence data of putatively active (cDNA) and whole community (gDNA). The outcomes of the study are condensed into a broadly applicable conceptual model linking external forcing, internal dynamics, and history. This data package is comprised of a file-level metadata (FLMD) csv, metadata csv, and seven folders that contain csv files, R scripts, xml files, and associated documentation: (1) Rates, (2) bNTI, and (3) FTICR, (4) Statistics_Analyses, (5) Raw OTU Beta dispersion Analysis, (6) bMNTD Randomizations, and (7) Data Dictionaries. The FLMD file has a description of each file included in the data package.

54 ENVIRONMENTAL SCIENCES↗

A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming

Abstract Unraveling the drivers controlling community assembly is a central issue in ecology. Although it is generally accepted that selection, dispersal, diversification and drift are major community assembly processes, defining their relative importance is very challenging. Here, we present a framework to quantitatively infer community assembly mechanisms by phylogenetic bin-based null model analysis (iCAMP). iCAMP shows high accuracy (0.93–0.99), precision (0.80–0.94), sensitivity (0.82–0.94), and specificity (0.95–0.98) on simulated communities, which are 10–160% higher than those from the entire community-based approach. Application of iCAMP to grassland microbial communities in response to experimental warming reveals dominant roles of homogeneous selection (38%) and ‘drift’ (59%). Interestingly, warming decreases ‘drift’ over time, and enhances homogeneous selection which is primarily imposed on Bacillales. In addition, homogeneous selection has higher correlations with drought and plant productivity under warming than control. iCAMP provides an effective and robust tool to quantify microbial assembly processes, and should also be useful for plant and animal ecology.

59 BASIC BIOLOGICAL SCIENCES↗

Altering plant carbon allocation to stems has distinct effects on rhizosphere soil microbiome assembly, interactions, and potential functions in sorghum

Abstract Altering plant carbon allocation from leaves to stems is key to improve biomass for forage, fuel, and renewable chemicals. The sorghum dry stalk ( D ) locus controls a quantitative trait for sugar accumulation, with enhanced carbon allocation in the stems of juicy green ( dd ) sorghum but reduced carbon allocation in that of dry white ( DD ) sorghum. However, it remains unclear whether altering sorghum sugar accumulation in stem affects below‐ground microbiome. Here we investigated sorghum rhizosphere soil microbiome in near isogenic lines with different magnitude of carbon allocations and accumulation in the stems. Results showed that enhanced carbon accumulation in stems of juicy green sorghum results in stronger selection in rhizosphere microbiome assembly. The rhizosphere soil microbial communities selected in juicy green sorghum tended to be fast‐growing microbial taxa which possessed potential functions that would promote higher potential capacity to use chemically labile carbon sources and potentially result in higher potential decomposition rates. We found the rhizosphere microbes selected by juicy green sorghum form weaker interactions than dry white sorghum. This is the first comprehensive study revealing how the different magnitude of carbon allocations to stems regulates microbial community assembly, microbial interaction, and microbial functions. This study indicates that future plant modification for bioenergy crops should also consider the impacts on belowground microbial community without compromising the sustainability.

59 BASIC BIOLOGICAL SCIENCES↗

Distinct Assembly Processes and Microbial Communities Constrain Soil Organic Carbon Formation

Soil stores more carbon (C) than all vegetation and the atmosphere combined. Soil C stocks are broadly shaped by temperature, moisture, soil physical characteristics, vegetation, and microbial-mediated metabolic processes. The efficiency with which microorganisms use soil C regulates the balance between C storage in soil and the atmosphere. In this review, we discuss how microbial physiology and community assembly processes determine microbial growth rate and efficiency and, in turn, soil organic C cycling through the lens of community ecology. We introduce a conceptual framework cataloging life history (i.e., growth rate, resource acquisition, and stress tolerance) and assembly traits (i.e., competition, facilitation, and dispersal) that correspond with different growth efficiencies. We also compare how dominant mycorrhizal fungal type affects growth efficiency. We propose that further development and inclusion of specific community parameters in microbial-explicit Earth system models are needed for accurately predicting soil organic C responses to global change.

carbon sequestration↗

A method for achieving complete microbial genomes and improving bins from metagenomics data

Metagenomics facilitates the study of the genetic information from uncultured microbes and complex microbial communities. Assembling complete microbial genomes ( i.e ., circular with no misassemblies) from metagenomics data is difficult because most samples have high organismal complexity and strain diversity. Less than 100 circularized bacterial and archaeal genomes have been assembled from metagenomics data despite the thousands of datasets that are available. Circularized genomes are important for (1) building a reference collection as scaffolds for future assemblies, (2) providing complete gene content of a genome, (3) confirming little or no contamination of a genome, (4) studying the genomic context and synteny of genes, and (5) linking protein coding genes to ribosomal RNA genes to aid metabolic inference in 16S rRNA gene sequencing studies. We developed a method to achieve circularized genomes using iterative assembly, binning, and read mapping. In addition, this method exposes potential misassemblies from k-mer based assemblies. We chose species of the Candidate Phyla Radiation (CPR) to focus our initial efforts because they have small genomes and are only known to have one ribosomal RNA operon. We present 34 circular CPR genomes, one circular Margulisbacteria genome, and two circular megaphage genomes from 19 public and published datasets. We demonstrate findings that would likely be difficult without circularizing genomes, including that ribosomal genes are likely not operonic in the majority of CPR, and that some CPR harbor diverged forms of RNase P RNA. Code and a tutorial for this method is available at https://github.com/lmlui/Jorg .

Lui, Lauren↗

Landscape connectivity for the invisibles

Because of land use changes, a worldwide decrease in biodiversity is underway, mostly driven by habitat degradation and fragmentation. Increasing landscape connectivity (i.e. the degree to which the landscape facilitates movement between habitat patches) has been proposed as a key landscape-level strategy to counterbalance the negative effects of habitat fragmentation. A robust theoretical and methodological framework has been developed for the concept of connectivity, and an increasing body of empirical evidence supports the relevance of connectivity for biodiversity. However, the framework was built ignoring species that represent the dominant proportion of biodiversity on earth: microorganisms. The extent to which the existing conceptual and methodological frameworks on connectivity can be applied to microorganisms remain unknown. We reviewed existing evidence and analyzed methods to test the influence of connectivity on microorganisms. We included all types of microorganisms, from symbiotic to pathogenic and free-living microorganisms, across all ecosystems. We describe the effect of connectivity on microorganism populations and communities, and identify the limitations and large gaps in current knowledge. Microorganisms can differ from macroorganisms in their response to connectivity due to short (distance less than a meter) dispersal distance of some groups, longer time lag of microorganisms response (possibly accompanied by evolutionary processes) and host association. The latter relies on tight interactions and feedback effects that drive microbial-landscape relationships and lead to possible coadaptation processes. Incorporating the connectivity concept in microbial community assembly rules to preserve the diversity of microbial communities and the ecosystem services they provide could be a crucial step forward in the face of pressing global changes.

60 APPLIED LIFE SCIENCES↗

Contrasting Community Assembly Forces Drive Microbial Structural and Potential Functional Responses to Precipitation in an Incipient Soil System

Microbial communities in incipient soil systems serve as the only biotic force shaping landscape evolution. However, the underlying ecological forces shaping microbial community structure and function are inadequately understood. We used amplicon sequencing to determine microbial taxonomic assembly and metagenome sequencing to evaluate microbial functional assembly in incipient basaltic soil subjected to precipitation. Community composition was stratified with soil depth in the pre-precipitation samples, with surficial communities maintaining their distinct structure and diversity after precipitation, while the deeper soil samples appeared to become more uniform. The structural community assembly remained deterministic in pre- and post-precipitation periods, with homogenous selection being dominant. Metagenome analysis revealed that carbon and nitrogen functional potential was assembled stochastically. Sub-populations putatively involved in the nitrogen cycle and carbon fixation experienced counteracting assembly pressures at the deepest depths, suggesting the communities may functionally assemble to respond to short-term environmental fluctuations and impact the landscape-scale response to perturbations. We propose that contrasting assembly forces impact microbial structure and potential function in an incipient landscape; in situ landscape characteristics (here homogenous parent material) drive community structure assembly, while short-term environmental fluctuations (here precipitation) shape environmental variations that are random in the soil depth profile and drive stochastic sub-population functional dynamics.

16S amplicon sequencing↗

Formation of a constructed microbial community in a nutrient-rich environment indicates bacterial interspecific competition

ABSTRACT Understanding the organizational principles of microbial communities is essential for interpreting ecosystem stability. Previous studies have investigated the formation of bacterial communities under nutrient-poor conditions or obligate relationships to observe cooperative interactions among different species. How microorganisms form stabilized communities in nutrient-rich environments, without obligate metabolic interdependency for growth, is still not fully disclosed. In this study, three bacterial strains isolated from the Populus deltoides rhizosphere were co-cultured in complex medium, and their growth behavior was tracked. These strains co-exist in mixed culture over serial transfer for multiple growth-dilution cycles. Competition is proposed as an emergent interaction relationship among the three bacteria based on their significantly decreased growth levels. The effects of different initial inoculum ratios, up to three orders of magnitude, on community structure were investigated, and the final compositions of the mixed communities with various starting composition indicate that community structure is not dependent on the initial inoculum ratio. Furthermore, the competitive relationships within the community were not altered by different initial inoculum ratios. The community structure was simulated by generalized Lotka-Volterra and dynamic flux balance analysis to provide mechanistic predictions into emergence of community structure under a nutrient-rich environment. Metaproteomic analyses provide support for the metabolite exchanges predicted by computational modeling and for highly altered physiologies when microbes are grown in co-culture. These findings broaden our understanding of bacterial community dynamics and metabolic diversity in higher-order interactions and could be significant in the management of rhizospheric bacterial communities. IMPORTANCE Bacteria naturally co-exist in multispecies consortia, and the ability to engineer such systems can be useful in biotechnology. Despite this, few studies have been performed to understand how bacteria form a stable community and interact with each other under nutrient-rich conditions. In this study, we investigated the effects of initial inoculum ratios on bacterial community structure using a complex medium and found that the initial inoculum ratio has no significant impact on resultant community structure or on interaction patterns between community members. The microbial population profiles were simulated using computational tools in order to understand intermicrobial relationships and to identify potential metabolic exchanges that occur during stabilization of the bacterial community. Studying microbial community assembly processes is essential for understanding fundamental ecological principles in microbial ecosystems and can be critical in predicting microbial community structure and function.

59 BASIC BIOLOGICAL SCIENCES↗

RhizoGrid Indexed Sorghum Rhizosphere Multi-Omics

PerCon SFA project data dentification of spatially resolved biomarkers of drought in Sorghum bicolor rhizosphere molecular-microbe interactions using a novel root cartography "RhizoGrid" system for sampling plants under drought and control conditions across 10 equally sized root zone environments (4 quadrants each). Each quadrant was sampled and processed for 16S amplicon, metabolomics, and X-ray computed tomography (XCT). Data download includes experimental metadata and results files for 16S rRNA sequence analysis of microbial community assembly (processed data files), liquid chromatography mass spectrometry (LC-MS) metabolomics analysis of microbial community root exudates (processed data files), X-ray computed tomography (XCT) spatial gradient analysis (raw and processed data files) of microbial community composition, and related computational modeling outputs.

59 BASIC BIOLOGICAL SCIENCES↗

Assembly of the Populus Microbiome Is Temporally Dynamic and Determined by Selective and Stochastic Factors

Recent work shows that the plant microbiome, particularly the initial assembly of this microbiome, influences plant health, survival, and fitness. Here, we characterize the initial assembly of the Populus microbiome across ten genotypes belonging to two poplar species in a common garden using 16S rRNA gene and ITS2 region amplicon sequencing of the leaf endosphere, leaf surface, root endosphere, and rhizosphere. We sampled these microbiomes three times throughout the first growing season and found that the composition of the microbiome changed dramatically over time across all plant-associated habitats and host genotypes. For archaea and bacteria, these changes were dominated by strong homogenizing selection (accounting for 29 to 62% of pairwise comparisons). However, fungal assembly was generally characterized by multiple ecological assembly processes (i.e., a mix of weak selective and dispersal processes). Interestingly, genotype, while a significant moderator of microbiome composition, generally explained less variation than sample date across plant-associated habitats. We defined a set of core genera that accounted for, on average, 36% of the microbiome. The relative abundance of this core community was consistent over time. Additionally, using source tracking modeling, we determined that new microbial taxa colonize from both aboveground and belowground sources, and combined with our ecological assembly null models, we found that both selective and dispersal processes explained the differences between exo- (i.e., leaf surface and rhizosphere) and endospheric microbiomes. Taken together, our results suggest that the initial assembly of the Populus microbiome is time-, genotype-, and habitat-dependent and is moderated by both selective and stochastic factors.

16S rRNA↗

Prescribed fire selects for a pyrophilous soil sub‐community in a northern California mixed conifer forest

Abstract Prescribed fire is a critical strategy for mitigating the effects of catastrophic wildfires. While the above‐ground response to fire has been well‐documented, fewer studies have addressed the effect of prescribed fire on soil microorganisms. To understand how soil microbial communities respond to prescribed fire, we sampled four plots at a high temporal resolution (two burned, two controls), for 17 months, in a mixed conifer forest in northern California, USA. Using amplicon sequencing, we found that prescribed fire significantly altered both fungal and bacterial community structure. We found that most differentially abundant fungal taxa had a positive fold‐change, while differentially abundant bacterial taxa generally had a negative fold‐change. We tested the null hypothesis that these communities assembled due to neutral processes (i.e., drift and/or dispersal), finding that >90% of taxa fit this neutral prediction. However, a dynamic sub‐community composed of burn‐associated indicator taxa that were positively differentially abundant was enriched for non‐neutral amplicon sequence variants, suggesting assembly via deterministic processes. In synthesizing these results, we identified 15 pyrophilous taxa with a significant and positive response to prescribed burns. Together, these results lay the foundation for building a process‐driven understanding of microbial community assembly in the context of the classical disturbance regime of fire.

Microbiology↗

Inferring microbial interactions with their environment from genomic and metagenomic data

Microbial communities assemble through a complex set of interactions between microbes and their environment, and the resulting metabolic impact on the host ecosystem can be profound. Microbial activity is known to impact human health, plant growth, water quality, and soil carbon storage which has lead to the development of many approaches and products meant to manipulate the microbiome. In order to understand, predict, and improve microbial community engineering, genome-scale modeling techniques have been developed to translate genomic data into inferred microbial dynamics. However, these techniques rely heavily on simulation to draw conclusions which may vary with unknown parameters or initial conditions, rather than more robust qualitative analysis. To better understand microbial community dynamics using genome-scale modeling, we provide a tool to investigate the network of interactions between microbes and environmental metabolites over time. Using our previously developed algorithm for simulating microbial communities from genome-scale metabolic models (GSMs), we infer the set of microbe-metabolite interactions within a microbial community in a particular environment. Because these interactions depend on the available environmental metabolites, we refer to the networks that we infer as metabolically contextualized , and so name our tool MetConSIN: Met abolically Con textualized S pecies I nteraction N etworks.

59 BASIC BIOLOGICAL SCIENCES↗

Mechanism Across Scales: A Holistic Modeling Framework Integrating Laboratory and Field Studies for Microbial Ecology

Over the last century, leaps in technology for imaging, sampling, detection, high-throughput sequencing, and -omics analyses have revolutionized microbial ecology to enable rapid acquisition of extensive datasets for microbial communities across the ever-increasing temporal and spatial scales. The present challenge is capitalizing on our enhanced abilities of observation and integrating diverse data types from different scales, resolutions, and disciplines to reach a causal and mechanistic understanding of how microbial communities transform and respond to perturbations in the environment. This type of causal and mechanistic understanding will make predictions of microbial community behavior more robust and actionable in addressing microbially mediated global problems. To discern drivers of microbial community assembly and function, we recognize the need for a conceptual, quantitative framework that connects measurements of genomic potential, the environment, and ecological and physical forces to rates of microbial growth at specific locations. We describe the Framework for Integrated, Conceptual, and Systematic Microbial Ecology (FICSME), an experimental design framework for conducting process-focused microbial ecology studies that incorporates biological, chemical, and physical drivers of a microbial system into a conceptual model. Through iterative cycles that advance our understanding of the coupling across scales and processes, we can reliably predict how perturbations to microbial systems impact ecosystem-scale processes or vice versa. We describe an approach and potential applications for using the FICSME to elucidate the mechanisms of globally important ecological and physical processes, toward attaining the goal of predicting the structure and function of microbial communities in chemically complex natural environments.

59 BASIC BIOLOGICAL SCIENCES↗

Fire alters plant microbiome assembly patterns: integrating the plant and soil microbial response to disturbance

Summary It is increasingly evident that the plant microbiome is a strong determinant of plant health. While the ability to manipulate the microbiome in plants and ecosystems recovering from disturbance may be useful, our understanding of the plant microbiome in regenerating plant communities is currently limited. Using 16S ribosomal RNA (rRNA) gene and internal transcribed spacer (ITS) region amplicon sequencing, we characterized the leaf, stem, fine root, rhizome, and rhizosphere microbiome of < 1‐yr‐old aspen saplings and the associated bulk soil after a recent high‐intensity prescribed fire across a burn severity gradient. Consistent with previous studies, we found that soil microbiomes are responsive to fire. We extend these findings by showing that certain plant tissue microbiomes also change in response to fire. Differences in soil microbiome compositions could be attributed to soil chemical characteristics, but, generally, plant tissue microbiomes were not related to plant tissue elemental concentrations. Using source tracking modeling, we also show that fire influences the relative dominance of microbial inoculum and the vertical inheritance of the sapling microbiome from the parent tree. Overall, our results demonstrate how fire impacts plant microbiome assembly, diversity, and composition and highlights potential for further research towards increasing plant fitness and ecosystem recovery after fire events.

16rRNA↗

Nutrient limitation shapes functional traits of mycorrhizal fungi and phosphorus-cycling bacteria across an elevation gradient

In nutrient-limited high-elevation ecosystems, plants rely on arbuscular mycorrhizal (AM) fungi to provide mineral phosphorus (P) in the form of phosphate (PO43-). AM fungi gather these nutrients from phosphorus-cycling bacteria (PCBs) that can mineralize PO43- from organic matter and solubilize mineral-bound P. How climate, soil factors, and nutrient limitation influence AM fungi and PCB assembly remains unclear. We collected soil from montane meadows across a 1,000-m elevation gradient on three replicate mountainsides and analyzed AM fungal marker genes, P-cycling genes from shotgun metagenomes, and edaphic measurements. High-elevation soils had nearly 50-fold less soil PO₄³⁻ and 60% more AM fungal hyphae than low-elevation soils. AM fungal turnover was linked to changes in pH, organic carbon, and PO₄³-. The composition of 198 P-cycling genes was influenced by the AM fungal community structure. Drivers of individual PCB functional genes, including pH and organic carbon, varied with gene phylogeny. We found a trade-off in P-cycling strategies across elevation: P-rich, low-elevation soils supported root-colonizing AM fungi and organic P-mineralizing bacteria. P-poor, high-elevation soils were dominated by stress-tolerant AM fungi and mineral P-solubilizing bacteria. Our results suggest that AM fungi and PCB community turnover across elevation are both shaped by pH, organic carbon, and P availability. With continued climate warming, the structure and function of mountaintop ecosystems might shift to resemble lower elevations, disrupting long-established and specialized microbial assemblages, with consequences for P-cycling dynamics and the total P available to plant communities.IMPORTANCEPhosphorus (P) limits plant productivity in high-elevation ecosystems, yet the microbial networks that mobilize P, including arbuscular mycorrhizal (AM) fungi and phosphorus-cycling bacteria (PCBs), remain under-characterized in these nutrient-poor soils. We show that across a 10,00-m elevation gradient, AM fungi and P-cycling gene assemblages shift predictably with pH, organic carbon, and phosphate availability. Higher elevations, with less available P, select for stress-tolerant AM fungal taxa and PCB strategies geared toward mineral solubilization, while low-elevation sites favor root colonization by AM fungi and organic P mineralization. These results suggest that nutrient limitation can constrain microbial community assembly in consistent ways across landscapes. High mountain soils are low in P and rely on a network of underground AM fungi and PCB to deliver nutrients to plants. This study shows how those underground relationships reorganize with elevation and how climate change could collapse long-standing microbial strategies by pushing high-elevation ecosystems toward lowland conditions. As soils warm and dry, the microbial scaffolding that supports alpine plant life may become increasingly unstable.

arbuscular mycorrhizal fungi↗

The microbial rare biosphere: current concepts, methods and ecological principles

ABSTRACT Our ability to describe the highly diverse pool of low abundance populations present in natural microbial communities is increasing at an unprecedented pace. Yet we currently lack an integrative view of the key taxa, functions and metabolic activity which make-up this communal pool, usually referred to as the ‘rare biosphere’, across the domains of life. In this context, this review examines the microbial rare biosphere in its broader sense, providing an historical perspective on representative studies which enabled to bridge the concept from macroecology to microbial ecology. It then addresses our current knowledge of the prokaryotic rare biosphere, and covers emerging insights into the ecology, taxonomy and evolution of low abundance microeukaryotic, viral and host-associated communities. We also review recent methodological advances and provide a synthetic overview on how the rare biosphere fits into different conceptual models used to explain microbial community assembly mechanisms, composition and function.

Pascoal, Francisco↗