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DOE OSTI2023

Latent Dirichlet Allocation modeling of environmental microbiomes

Interactions between stressed organisms and their microbiome environments may provide new routes for understanding and controlling biological systems. However, microbiomes are a form of high-dimensional data, with thousands of taxa present in any given sample, which makes untangling the interaction between an organism and its microbial environment a challenge. Here we apply Latent Dirichlet Allocation (LDA), a technique for language modeling, which decomposes the microbial communities into a set of topics (non-mutually-exclusive sub-communities) that compactly represent the distribution of full communities. LDA provides a lens into the microbiome at broad and fine-grained taxonomic levels, which we show on two datasets. In the first dataset, from the literature, we show how LDA topics succinctly recapitulate many results from a previous study on diseased coral species. We then apply LDA to a new dataset of maize soil microbiomes under drought, and find a large number of significant associations between the microbiome topics and plant traits as well as associations between the microbiome and the experimental factors, e.g. watering level. This yields new information on the plant-microbial interactions in maize and shows that LDA technique is useful for studying the coupling between microbiomes and stressed organisms.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Evaluating a Laboratory Flume Microbiome as a Window Into Natural Riverbed Biogeochemistry

Riverbeds are hotspots for microbially-mediated reactions that exhibit pronounced variability in space and time. It is challenging to resolve biogeochemical mechanisms in natural riverbeds, as uncontrolled settings complicate data collection and interpretation. To overcome these challenges, laboratory flumes are often used as proxies for natural riverbed systems. Flumes capture spatiotemporal variability and thus allow for controlled investigations of riverbed biogeochemistry. These investigations implicitly rely on the assumption that the flume microbiome is similar to the microbiome of natural riverbeds. However, this assumption has not been tested and it is unknown how the microbiome of a flume compares to natural aquatic settings, including riverbeds. To evaluate the fundamental assumption that a flume hosts a microbiome similar to natural riverbed systems, we used 16s rRNA gene sequencing and publicly available data to compare the sediment microbiome of a single large laboratory flume to a wide variety of natural ecosystems including lake and marine sediments, river, lake, hyporheic, soil, and marine water, and bank and wetland soils. Richness and Shannon diversity metrics, analyses of variance, Bray-Curtis dissimilarity, and analysis of the common microbiomes between flume and river sediment all indicated that the flume microbiome more closely resembled natural riverbed sediments than other ecosystems, supporting the use of flume experiments for investigating natural microbially-mediated biogeochemical processes in riverbeds.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2023

Activity‐Based Protein Profiling – Enabling Phenotyping of Host‐Associated and Environmental Microbiomes

Abstract Host‐associated and environmental microbiomes play central roles in human health, biogeochemical cycling, response to ecosystem change, and agriculture. Scientific approaches that can reveal the functional activities that contribute to observed phenotypes are needed in microbiome research. Broad characterization of the functional activity of microbes within microbiomes is currently hampered by approaches that rely on inference of function from metagenomes or indirect measurements. Activity‐based protein profiling is uniquely positioned to overcome these challenges and reveal the protein‐level mechanisms associated with microbiome phenotypes. In this review we describe the progress made to date using ABPP in gut microbiome, plant‐microbe interaction, and soil microbiome research, and suggest how ABPP data can be coupled with advanced computational methods to enable phenotype prediction and bioengineering of microbiomes for applied purposes.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Drought conditioning of rhizosphere microbiome influences maize water use traits

Background and Aims: Beneficial plant–microbe interactions can improve plant performance under drought; however, we know less about how drought-induced shifts in microbial communities affect plant traits. Methods: We cultivated Zea mays in fritted clay with soil microbiomes originating from contrasting environments (agriculture or forest) under two irrigation treatments (well-watered or water limited). Using this design, we investigated whether water conditioning was carried forward through the microbiome to affect a subsequent plant cohort that was subjected to either a well-watered or water limited treatment. Results: Regardless of the microbiome-origin, plants inoculated with a microbiome from a water limited legacy had traits that allowed them to avoid stress but conserve water. They produced longer roots to explore soil, generated greater soil dissolved organic carbon, potentially stimulating the microbiome, and slower soil water content loss during drought. A well-watered legacy resulted in plants that delayed permanent stomatal closure and higher photosynthetic nitrogen use efficiency. In plants with a forest-originated microbiome, a well-watered legacy and water treatment also resulted in higher rates of photosynthesis and stomatal conductance. Conclusion: These results demonstrate that soil microbiomes can be developed to influence plant drought performance, impacting crop resilience, using short-term microbial conditioning.

60 APPLIED LIFE SCIENCES↗

DOE OSTI2022

Activity-based protein profiling identifies alternating activation of enzymes involved in the bifidobacterium shunt pathway or mucin degradation in the gut microbiome response to soluble dietary fiber

While deprivation of dietary fiber has been associated with adverse health outcomes, investigations concerning the effect of dietary fiber on the gut microbiome have been largely limited to compositional sequence-based analyses or utilize a defined microbiota not native to the host. To extend understanding of the microbiome’s functional response to dietary fiber deprivation beyond correlative evidence from sequence-based analyses, approaches capable of measuring functional enzymatic activity are needed. In this study, we use an activity-based protein profiling (ABPP) approach to identify sugar metabolizing and transport proteins in native mouse gut microbiomes that respond with differential activity to the deprivation or supplementation of the soluble dietary fibers inulin and pectin. We found that the microbiome of mice subjected to a high fiber diet high in soluble fiber had increased functional activity of multiple proteins, including glycoside hydrolases, polysaccharide lyases, and sugar transport proteins from diverse taxa. The results point to an increase in activity of the Bifidobacterium shunt metabolic pathway in the microbiome of mice fed high fiber diets. In those subjected to a low fiber diet, we identified a shift from the degradation of dietary fibers to that of gut mucins, in particular by the recently isolated taxon “Musculibacterium intestinale”, which experienced dramatic growth in response to fiber deprivation. When combined with metabolomics and shotgun metagenomics analyses, our findings provide a functional investigation of dietary fiber metabolism in the gut microbiome and demonstrates the power of a combined ABPP-multiomics approach for characterizing the response of the gut microbiome to perturbations.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

Salivary microbiome composition changes after bariatric surgery

Recent studies show that the salivary microbiome in subjects with obesity differ from those without obesity, but the mechanism of interaction between the salivary microbiome composition and body weight is unclear. Herein we investigate this relation by analyzing saliva samples from 35 adult patients with obesity undergoing bariatric surgery. Our aim was to describe salivary microbiome changes during body weight loss on an individual-specific level, and to elucidate the effect of bariatric surgery on the salivary microbiome which has not been studied before. Analysis of samples collected before and 1 day after surgery, as well as 3 and 12 months after surgery, showed that the salivary microbiome changed in all study participants, but these changes were heterogeneous. In the majority of participants proportions of Gemella species, Granulicatella elegans, Porphyromonas pasteri, Prevotella nanceiensis and Streptococcus oralis decreased, while Veillonella species, Megasphaera micronuciformis and Prevotella saliva increased. Nevertheless, we found participants deviating from this general trend which suggests that a variety of individual-specific factors influence the salivary microbiome composition more effectively than the body weight dynamics alone. The observed microbiome alternations could be related to dietary changes. Therefore, further studies should focus on association with altered taste preferences and potential oral health consequences.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Poisson hurdle model-based method for clustering microbiome features

Abstract Motivation High-throughput sequencing technologies have greatly facilitated microbiome research and have generated a large volume of microbiome data with the potential to answer key questions regarding microbiome assembly, structure and function. Cluster analysis aims to group features that behave similarly across treatments, and such grouping helps to highlight the functional relationships among features and may provide biological insights into microbiome networks. However, clustering microbiome data are challenging due to the sparsity and high dimensionality. Results We propose a model-based clustering method based on Poisson hurdle models for sparse microbiome count data. We describe an expectation–maximization algorithm and a modified version using simulated annealing to conduct the cluster analysis. Moreover, we provide algorithms for initialization and choosing the number of clusters. Simulation results demonstrate that our proposed methods provide better clustering results than alternative methods under a variety of settings. We also apply the proposed method to a sorghum rhizosphere microbiome dataset that results in interesting biological findings. Availability and implementation R package is freely available for download at https://cran.r-project.org/package=PHclust. Supplementary information Supplementary data are available at Bioinformatics online.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

Functional team selection as a framework for local adaptation in plants and their belowground microbiomes

Abstract Multicellular organisms are hosts to diverse communities of smaller organisms known as microbiomes. Plants have distinctive microbiomes that can provide important functions related to nutrition, defense, and stress tolerance. Empirical studies provide convincing evidence that in some—but not all—circumstances, belowground microbiomes help plants adapt to their local environment. The purpose of this review is to develop functional team selection (FTS) as a framework to help predict the conditions necessary for root microbiomes to generate local adaptation for their plant hosts. FTS envisions plants and their microbiomes as complex adaptive systems, and plant adaptations as emergent properties of these systems. If plants have the capacity to recognize and cultivate beneficial microbes and suppress pathogens, then it is possible for plants to evolve the capacity to gain adaptations by curating their microbiome. In resource-limited and stressful environments, the emergent functions of complex microbial systems may contribute to positive feedback linked to plant vigor, and ultimately, local adaptation. The key factors in this process are: (i) selective force, (ii) host constitution, (iii) microbial diversity, and (iv) time. There is increasing interest in harnessing beneficial microbial interactions in agriculture and many microbial growth-promoting products are commercially available, but their use is controversial because a large proportion of these products fail to consistently enhance plant growth. The FTS framework may help direct the development of durable plant-microbiome systems that enhance crop production and diminish pathogens. It may also provide valuable insights for understanding and managing other kinds of host-microbe systems.

Environmental Sciences & Ecology↗

DOE OSTI2021

Holo-omics for deciphering plant-microbiome interactions

Host-microbiome interactions are recognized for their importance to host health. An improved understanding of the molecular underpinnings of host-microbiome relationships will advance our capacity to accurately predict host fitness and manipulate interaction outcomes. Within the plant microbiome research field, unlocking the functional relationships between plants and their microbial partners is the next step to effectively using the microbiome to improve plant fitness. We propose that strategies that pair host and microbial datasets—referred to here as holo-omics—provide a powerful approach for hypothesis development and advancement in this area. We discuss several experimental design considerations and present a case study to highlight the potential for holo-omics to generate a more holistic perspective of molecular networks within the plant microbiome system. In addition, we discuss the biggest challenges for conducting holo-omics studies; specifically, the lack of vetted analytical frameworks, publicly available tools, and required technical expertise to process and integrate heterogeneous data. Finally, we conclude with a perspective on appropriate use-cases for holo-omics studies, the need for downstream validation, and new experimental techniques that hold promise for the plant microbiome research field. We argue that utilizing a holo-omics approach to characterize host-microbiome interactions can provide important opportunities for broadening system-level understandings and significantly inform microbial approaches to improving host health and fitness.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Comparing western (Megascops kennicottii) and whiskered (M. trichopsis) screech-owl microbiomes in southern Arizona using a novel 16S rRNA sequencing method

Microbiomes are essential to a host’s physiology and health. Despite the overall importance of microbiomes to animal health, they remain understudied in wildlife. Microbiomes function as physical barriers to invading pathogens, and changes in the diversity or composition of microbes within a host may disrupt this barrier. In order to use microbiomes in wildlife ecology, knowledge of the natural variation within and among species is essential. We compare the diversity and composition of two avian species that share the same habitat and niche in our study area, the western screech-owl (Megascops kennicottii) and the whiskered screech-owl (M. trichopsis). We used a targeted 16S sequencing method to improve the taxonomic resolution of microbiomes. We found similar measures of alpha diversity between species and sample types (cloacal samples vs. fecal samples). However, there were significant differences in bacterial species richness among nestlings from different nest boxes, and the composition differed between the two bird species and among nestlings from different nest boxes. Western screech-owls had more variation in alpha diversity and composition and had fewer bacterial species in their core microbiome than whiskered screech-owls. Siblings are likely to yield similar findings for microbiomes; thus, sampling nestlings from different nests may be most informative for monitoring population-level changes.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2026

2024 International Conference on Microbiome Engineering (ICME)

The 2024 International Conference on Microbiome Engineering (ICME) took place November 12-14 at Tufts University in Medford, MA. ICME connects experts from academia and industry to share the most recent developments in the field of microbiome engineering. This includes genetically engineered organisms that function within microbiomes, control of microbiomes through environmental/nutrient modifications, and inference of engineering principles from analysis of synthetic and natural microbiomes. The conference is unique and distinct from other microbiome conferences in that it specifically highlights the integration of engineering design principles with microbiome research (others are more focused on basic biological principles). The conference thus integrates synthetic biology, systems biology, microbial ecology, and bioinformatics across a range of application spaces from the environment to manufacturing, food, and human health. This project utilized support from the Department of Energy’s (DOE) Office of Biological and Environmental Research (BER) to help trainees and early career faculty attend ICME.

60 APPLIED LIFE SCIENCES↗

DOE OSTI2020

Microbe to Microbiome: A Paradigm Shift in the Application of Microorganisms for Sustainable Agriculture

Light, water and healthy soil are three essential natural resources required for agricultural productivity. Industrialization of agriculture has resulted in intensification of cropping practices using enormous amounts of chemical pesticides and fertilizers that damage these natural resources. Therefore, there is a need to embrace agriculture practices that do not depend on greater use of fertilizers and water to meet the growing demand of global food requirements. Plants and soil harbor millions of microorganisms, which collectively form a microbial community known as the microbiome. An effective microbiome can offer benefits to its host, including plant growth promotion, nutrient use efficiency, and control of pests and phytopathogens. Therefore, there is an immediate need to bring functional potential of plant-associated microbiome and its innovation into crop production. In addition to that, new scientific methodologies that can track the nutrient flux through the plant, its resident microbiome and surrounding soil, will offer new opportunities for the design of more efficient microbial consortia design. It is now increasingly acknowledged that the diversity of a microbial inoculum is as important as its plant growth promoting ability. Not surprisingly, outcomes from such plant and soil microbiome studies have resulted in a paradigm shift away from single, specific soil microbes to a more holistic microbiome approach for enhancing crop productivity and the restoration of soil health. Herein, we have reviewed this paradigm shift and discussed various aspects of benign microbiome-based approaches for sustainable agriculture.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Drought legacies mediated by trait trade‐offs in soil microbiomes

Abstract Soil microbiomes play a key role in driving biogeochemical cycles of the Earth system. As drought frequency and intensity increase due to climate change, soil microbes and the processes they control will be impacted. Even after a drought ends, microbiomes and other systems take time to recover and may display a memory of previous climate conditions. Still, the mechanisms involved in these legacy effects remain unclear, making it difficult to predict climate and biogeochemical rates in the future. Here, we used a trait‐based microbiome model (DEMENTpy) to implement trade‐off‐mediated mechanisms that may lead to drought legacy effects on litter decomposition. Trade‐offs were assumed to follow the Y‐A‐S framework that defines three primary life‐history strategies of microorganisms: high growth Yield, resource Acquisition, and Stress tolerance. We represented cellular trade‐offs between osmolytes required for drought tolerance and investment in enzymes involved in litter decomposition. Simulations were run under varying levels of drought severity and dispersal. With high levels of dispersal, no legacy effects were predicted by DEMENTpy following drought. With limited dispersal, severe drought resulted in a persistent legacy of altered community‐level traits and reduced litter decomposition. Moderate drought resulted in a transient legacy that disappeared after two years, consistent with recent empirical observations in Southern California ecosystems. These results imply that greater movement along the trade‐off between enzyme investment and osmolyte production resulted in stronger legacy effects. More generally, factors that shift the position of a microbiome in YAS space may alter the legacy outcome following drought. Our trait‐based modeling study motivates additional empirical measurements to quantify YAS traits and trade‐offs that are needed to make accurate predictions of soil microbiome resilience and functioning. Also, our study illustrates an emerging approach for representing trait trade‐offs in microbiomes and vegetation that dictate ecosystem responses to drought and other environmental perturbations.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2021

Thirdhand cigarette smoke leads to age-dependent and persistent alterations in the cecal microbiome of mice

The gut microbiome composition is influenced by many factors including environmental exposures. Here, we investigated the effect of thirdhand cigarette smoke (THS) and exposure age on gut microbiome diversity. C57BL/6 mice were exposed to THS at human exposure relevant levels for three weeks during three different life stages: postnatal (0–3 weeks of age), pubescent (4–7 weeks of age), and adult (9–12 weeks of age), respectively. Cecal microbiome profiles were assessed at 17 weeks of age by 16S rRNA gene sequencing. We found that age at THS exposure strongly influenced the cecal microbiome composition. Although postnatal THS exposure significantly influenced the microbial composition, pubescent and adulthood exposures only had minor effects. The microbiome of postnatally THS-exposed mice significantly increased several degradation pathways that regulate glycolysis and pyruvate decarboxylation, and significantly decreased coenzyme A biosynthesis and pyrimidine deoxyribonucleoside salvage. Our results indicate that mouse postnatal development is particularly susceptible to persistent THS exposure effects on the gut microbiome.

16S rRNA gene sequencing↗

DOE OSTI2021

Gut microbiome associations with outcome following co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2) in pigs immunized with a PRRS modified live virus vaccine

Porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2) are two of the most significant pathogens affecting swine. Co-infections are common and result in respiratory disease and reduced weight gain in growing pigs. Although PRRS modified live virus (MLV) vaccines are widely used to decrease PRRS-associated losses, they are generally considered inadequate for disease control. The gut microbiome provides an alternative strategy to enhance vaccine efficacy and improve PRRS control. The objective of this work was to identify gut microbiome characteristics associated with improved outcome in pigs immunized with a PRRS MLV and co-challenged with PRRSV and PCV2b. Twenty-eight days after vaccination and prior to co-challenge, fecal samples were collected from an experimental population of 50 nursery pigs. At 42 days post-challenge, 20 pigs were retrospectively identified as having high or low growth outcomes during the post-challenge period. Gut microbiomes of the two outcome groups were compared using the Lawrence Livermore Microbial Detection Array (LLMDA) and 16S rDNA sequencing. High growth outcomes were associated with several gut microbiome characteristics, such as increased bacterial diversity, increased Bacteroides pectinophilus, decreased Mycoplasmataceae species diversity, higher Firmicutes:Bacteroidetes ratios, increased relative abundance of the phylum Spirochaetes, reduced relative abundance of the family Lachnospiraceae, and increased Lachnospiraceae species C6A11 and P6B14. Overall, this study identifies gut microbiomes associated with improved outcomes in PRRS vaccinated pigs following a polymicrobial respiratory challenge and provides evidence towards the gut microbiome playing a role in PRRS vaccine efficacy.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Regional biogeography versus intra-annual dynamics of the root and soil microbiome

Abstract Background Root and soil microbial communities constitute the below-ground plant microbiome, are drivers of nutrient cycling, and affect plant productivity. However, our understanding of their spatiotemporal patterns is confounded by exogenous factors that covary spatially, such as changes in host plant species, climate, and edaphic factors. These spatiotemporal patterns likely differ across microbiome domains (bacteria and fungi) and niches (root vs. soil). Results To capture spatial patterns at a regional scale, we sampled the below-ground microbiome of switchgrass monocultures of five sites spanning > 3 degrees of latitude within the Great Lakes region. To capture temporal patterns, we sampled the below-ground microbiome across the growing season within a single site. We compared the strength of spatiotemporal factors to nitrogen addition determining the major drivers in our perennial cropping system. All microbial communities were most strongly structured by sampling site, though collection date also had strong effects; in contrast, nitrogen addition had little to no effect on communities. Though all microbial communities were found to have significant spatiotemporal patterns, sampling site and collection date better explained bacterial than fungal community structure, which appeared more defined by stochastic processes. Root communities, especially bacterial, were more temporally structured than soil communities which were more spatially structured, both across and within sampling sites. Finally, we characterized a core set of taxa in the switchgrass microbiome that persists across space and time. These core taxa represented < 6% of total species richness but > 27% of relative abundance, with potential nitrogen fixing bacteria and fungal mutualists dominating the root community and saprotrophs dominating the soil community. Conclusions Our results highlight the dynamic variability of plant microbiome composition and assembly across space and time, even within a single variety of a plant species. Root and soil fungal community compositions appeared spatiotemporally paired, while root and soil bacterial communities showed a temporal lag in compositional similarity suggesting active recruitment of soil bacteria into the root niche throughout the growing season. A better understanding of the drivers of these differential responses to space and time may improve our ability to predict microbial community structure and function under novel conditions.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Microbiomes of commercially-available pine nuts and sesame seeds

Metagenomic analysis of food is becoming more routine and can provide important information pertaining to the shelf life potential and the safety of these products. However, less information is available on the microbiomes associated with low water activity foods. Pine nuts and sesame seeds, and food products which contain these ingredients, have been associated with recalls due to contamination with bacterial foodborne pathogens. The objective of this study was to identify the microbial community of pine nuts and sesame seeds using targeted 16S rRNA sequencing technology. Ten different brands of each seed type were assessed, and core microbiomes were determined. A total of 21 and 16 unique taxa with proportional abundances >1% in at least one brand were identified in the pine nuts and sesame seeds, respectively. Members of the core pine nut microbiome included the genera Alishewanella, Aminivibrio, Mycoplasma, Streptococcus, and unassigned OTUs in the families of Desulfobacteraceae and Xanthomonadaceae. For sesame seeds, the core microbiome included Aminivibrio, Chryseolina, Okibacterium, and unassigned OTUs in the family Flavobacteriaceae. The microbiomes of these seeds revealed that these products are dominated by environmental bacterial genera commonly isolated from soil, water, and plants; bacterial genera containing species known as commensal organisms were also identified. Understanding these microbiomes can aid in the risk assessment of these products by identifying food spoilage potential and community members which may co-enrich with foodborne bacterial pathogens.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Five key aspects of metaproteomics as a tool to understand functional interactions in host-associated microbiomes

Host-associated microbial communities (microbiomes) play critical roles in human, animal, and plant health and development. However, interactions between the host, members of the microbiome, and invading pathogens are in most cases still poorly understood. Such interactions are multidimensional and can alter the taxonomic composition and/or the functional metabolic activities of the microbiome in response to disease or treatment conditions. For example, after 2 days of antibiotic treatment, the mouse gut microbiome is altered and more susceptible to invasion by the pathogen Clostridioides difficile. Studies of these multidimensional interactions have been fueled by the ability to use high-throughput sequencing of phylogenetic marker genes to profile microbial community composition and shotgun metagenomics to profile functional potential. However, many protein-coding genes predicted from metagenomes are not necessarily expressed under a given condition, and thus, it is difficult to assess the activities and functional interactions in microbial communities based on DNA sequencing data alone. The physiological and pathological processes expressed in these communities under specific conditions are better reflected by the abundances of transcripts or proteins. In this Pearl, we provide a brief introduction to metaproteomics, which is a tool for the large-scale analysis of proteins in microbiomes that allows researchers to address a diversity of questions related to functions and interactions in microbiomes. The term “metaproteomics” was first used in 2004 for “the large-scale characterization of the entire protein complement of environmental microbiota at a given point in time”, and since then, a large array of metaproteomics approaches have been developed. Our objective in this Pearl is to highlight what we feel are 5 essential elements to be considered for a metaproteomics research campaign and to introduce nonexpert readers to the topic without going into too much technical detail.

59 BASIC BIOLOGICAL SCIENCES↗