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DOE OSTI2025

Clarifying Terminology in Microbial Ecology: A Call for Precision in Scientific Communication

The rapid evolution of microbiology as a field of research has led to the introduction of new terminology and the adaptation of existing terms. However, inconsistencies in the use of these terms, including variations across different scientific disciplines, can lead to confusion and miscommunication within the scientific community. This article discusses the importance of precise terminology in microbiome research, highlighting examples where terms have been misused or redefined without clear justification. We also present a list of frequently used terms in microbial ecology along with their specific definitions. We argue that the misuse of terminology can hinder scientific progress by creating ambiguity and misunderstanding. To address this, we propose a set of guidelines for the consistent use of key terms and provide clear definitions for some of the most commonly misused or newly introduced terms in the field. The definitions provided herein will also function as a guide for young researchers new to the field of microbial ecology. Accurate and consistent use of terminology is crucial for effective communication and collaboration in microbiology research. By adhering to standardised definitions, researchers can ensure that their work is clearly communicated and contributes meaningfully to the progress of science.

definitions↗
DOE OSTI2019

Comparative Genomics Guides Elucidation of Vitamin B 12 Biosynthesis in Novel Human-Associated Akkermansia Strains

Akkermansia muciniphila is a mucin-degrading bacterium found in the gut of most humans and is considered a “next-generation probiotic.” However, knowledge of the genomic and physiological diversity of human-associated Akkermansia sp. strains is limited. Here, we reconstructed 35 metagenome-assembled genomes and combined them with 40 publicly available genomes for comparative genomic analysis. We identified at least four species-level phylogroups (AmI to AmIV), with distinct functional potentials. Most notably, we identified genes for cobalamin (vitamin B 12 ) biosynthesis within the AmII and AmIII phylogroups. To verify these predictions, 10 Akkermansia strains were isolated from adults and screened for vitamin B 12 biosynthesis genes via PCR. Two AmII strains were positive for the presence of cobalamin biosynthesis genes, while all 9 AmI strains tested were negative. To demonstrate vitamin B 12 biosynthesis, we measured the production of acetate, succinate, and propionate in the presence and absence of vitamin supplementation in representative strains of the AmI and AmII phylogroups, since cobalamin is an essential cofactor in propionate metabolism. Results showed that the AmII strain produced acetate and propionate in the absence of supplementation, which is indicative of vitamin B 12 biosynthesis. In contrast, acetate and succinate were the main fermentation products for the AmI strains when vitamin B 12 was not supplied in the culture medium. Lastly, two bioassays were used to confirm vitamin B 12 production by the AmII phylogroup. This novel physiological trait of human-associated Akkermansia strains may affect how these bacteria interact with the human host and other members of the human gut microbiome.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2025

Multi-omics of a model bacterial consortium deciphers details of chitin decomposition in soil

Soil microorganisms interact to carry out decomposition of complex organic carbon and nitrogen compounds, such as chitin, but the high diversity and complexity of the soil microbiome and habitat have posed a challenge to elucidating such interactions. Here, we sought to address this challenge by analysis of a model soil consortium (MSC-2) consisting of eight soil bacterial species. Our aim was to elucidate the specific roles of the member species during chitin metabolism. Samples were collected from MSC-2 incubated in chitin-enriched soil over 3 months. Multi-omics was used to understand how the community composition, transcripts, proteins, and chitin decomposition shifted over time. The data clearly and consistently revealed a temporal shift during chitin decomposition with defined contributions by individual species. A Streptomyces genus member (sp001905665) was a key player in early steps of chitin decomposition, with other MSC-2 members being central in carrying out later steps. These results illustrate how multi-omics applied to a defined consortium untangles the interactions between soil microorganisms.

chitin↗
DOE OSTI2023

LaeA-Regulated Fungal Traits Mediate Bacterial Community Assembly

Cheese rinds are economically important microbial communities where fungi can impact food quality and aesthetics. The specific mechanisms by which fungi can regulate bacterial community assembly in cheeses, other fermented foods, and microbiomes in general are largely unknown.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2018

Need for Laboratory Ecosystems To Unravel the Structures and Functions of Soil Microbial Communities Mediated by Chemistry

The chemistry underpinning microbial interactions provides an integrative framework for linking the activities of individual microbes, microbial communities, plants, and their environments. Currently, we know very little about the functions of genes and metabolites within these communities because genome annotations and functions are derived from the minority of microbes that have been propagated in the laboratory. Yet the diversity, complexity, inaccessibility, and irreproducibility of native microbial consortia limit our ability to interpret chemical signaling and map metabolic networks. In this perspective, we contend that standardized laboratory ecosystems are needed to dissect the chemistry of soil microbiomes. We argue that dissemination and application of standardized laboratory ecosystems will be transformative for the field, much like how model organisms have played critical roles in advancing biochemistry and molecular and cellular biology. Community consensus on fabricated ecosystems (“EcoFABs”) along with protocols and data standards will integrate efforts and enable rapid improvements in our understanding of the biochemical ecology of microbial communities.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
DOE OSTI2025

Aerosol biome of a cafeteria and medical facility in Los Alamos, New Mexico, USA

Aerosol sampling with next-generation sequencing was used to characterize microbial communities in a cafeteria and medical facility waiting room in Los Alamos, New Mexico, USA. We detected sequences from human, bacteria, archaea, fungi, other eukaryotes, and viruses, providing insights into the diversity of the aerosol microbiome.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2025

Characterization of intestinal fungal communities through ITS amplicon from metagenomic libraries of sea cucumber ( Holothuria glaberrima )

The brown rock sea cucumber (Holothuria glaberrima) microbiome is vital for understanding its ecological dynamics. This study focuses on the microbial composition and abundance of fungi across different intestinal regions of H. glaberrima, giving insights into host-microbe interactions and supporting future ecological and comparative studies on their regeneration capabilities.

16S↗
DOE OSTI2021

Discovery of an Antarctic Ascidian-Associated Uncultivated Verrucomicrobia with Antimelanoma Palmerolide Biosynthetic Potential

The Antarctic marine ecosystem harbors a wealth of biological and chemical innovation that has risen in concert over millennia since the isolation of the continent and formation of the Antarctic circumpolar current. Scientific inquiry into the novelty of marine natural products produced by Antarctic benthic invertebrates led to the discovery of a bioactive macrolide, palmerolide A, that has specific activity against melanoma and holds considerable promise as an anticancer therapeutic. While this compound was isolated from the Antarctic ascidian Synoicum adareanum, its biosynthesis has since been hypothesized to be microbially mediated, given structural similarities to microbially produced hybrid nonribosomal peptide-polyketide macrolides. Here, we describe a metagenome-enabled investigation aimed at identifying the biosynthetic gene cluster (BGC) and palmerolide A-producing organism. A 74-kbp candidate BGC encoding the multimodular enzymatic machinery (hybrid type I-trans-AT polyketide synthase-nonribosomal peptide synthetase and tailoring functional domains) was identified and found to harbor key features predicted as necessary for palmerolide A biosynthesis. Surveys of ascidian microbiome samples targeting the candidate BGC revealed a high correlation between palmerolide gene targets and a single 16S rRNA gene variant (R = 0.83 to 0.99). Through repeated rounds of metagenome sequencing followed by binning contigs into metagenome-assembled genomes, we were able to retrieve a nearly complete genome (10 contigs) of the BGC-producing organism, a novel verrucomicrobium within the Opitutaceae family that we propose here as “Candidatus Synoicihabitans palmerolidicus.” The refined genome assembly harbors five highly similar BGC copies, along with structural and functional features that shed light on the host-associated nature of this unique bacterium.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2020

Amylases in the Human Vagina

ABSTRACT Dominance of Lactobacillus species in vaginal communities is a hallmark of healthy conditions in the female genital tract. Key nutrients for lactobacilli include sugars produced when glycogen is degraded by α-amylase in the vagina. While α-amylase activity has been demonstrated in vaginal fluids, it is unclear whether α-amylases are produced solely by the host, bacteria in the vagina, or both. We screened cervicovaginal mucus from 23 reproductive-age women, characterized the species composition of vaginal communities, measured vaginal pH, and determined levels of amylase activity, glycogen, and lactic acid. Based on differences in these measured variables, one sample from each of four individual donors was selected for metagenomic and proteomic analyses. Of eight putative bacterial amylases identified in the assembled bacterial metagenomes, we detected four in vaginal fluids. These amylases were produced by various bacteria in different vaginal communities. Moreover, no two communities were the same in terms of which bacteria were producing amylases. Although we detected bacterial amylases in vaginal fluids, there was no clear association between the bacterial species that was dominant in a community and the level of amylase activity. This association was likely masked by the presence of human α-amylase, which was also detected in vaginal fluids. Finally, the levels of amylase activity and glycogen were only weakly associated. Our findings show, for the first time, that multiple amylases from both bacterial and human origins can be present simultaneously in the vagina. This work also suggests that the link between glycogen, amylase, and Lactobacillus in the vagina is complex. IMPORTANCE In this study, we show that multiple bacteria in the vaginal community produce amylases that hydrolyze glycogen into simpler sugars (i.e., maltose and maltotriose). These sugars serve as “common goods” that sustain bacterial populations in vaginal communities. Given the temporal changes that are observed in the human vaginal microbiome, we expect the kinds of bacterial amylases produced will also vary over time. These differences influence the pool of resources that are broadly shared and shape the species composition of the vaginal bacterial community.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2019

16S rRNA/rRNA Gene Ratios and Cell Activity Staining Reveal Consistent Patterns of Microbial Activity in Plant-Associated Soil

Although the majority of microorganisms in natural ecosystems are dormant, relatively little is known about the dynamics of the active and dormant microbial pools through both space and time. The limited knowledge of microbial activity-dormancy dynamics is in part due to uncertainty in the methods currently used to quantify active taxa. Here, we directly compared two of the most common methods (16S ratios and active cell staining) for estimating microbial activity in plant-associated soil and found that they were largely in agreement in the overarching patterns. Our results suggest that 16S ratios and active cell staining provide complementary information for measuring and interpreting microbial activity-dormancy dynamics in soils. They also support the idea that 16S rRNA/rRNA gene ratios have comparative value and offer a high-throughput, sequencing-based option for understanding relative changes in microbiome activity, as long as this method is coupled with quantification of community size.

16S rRNA↗
DOE OSTI2023

Construction and Modeling of a Coculture Microplate for Real-Time Measurement of Microbial Interactions

The dynamic structures of microbial communities emerge from the complex network of interactions between their constituent microorganisms. Quantitative measurements of these interactions are important for understanding and engineering ecosystem structure. Here, we present the development and application of the BioMe plate, a redesigned microplate device in which pairs of wells are separated by porous membranes. BioMe facilitates the measurement of dynamic microbial interactions and integrates easily with standard laboratory equipment. We first applied BioMe to recapitulate recently characterized, natural symbiotic interactions between bacteria isolated from the Drosophila melanogaster gut microbiome. Specifically, the BioMe plate allowed us to observe the benefit provided by two Lactobacillus strains to an Acetobacter strain. We next explored the use of BioMe to gain quantitative insight into the engineered obligate syntrophic interaction between a pair of Escherichia coli amino acid auxotrophs. We integrated experimental observations with a mechanistic computational model to quantify key parameters associated with this syntrophic interaction, including metabolite secretion and diffusion rates. This model also allowed us to explain the slow growth observed for auxotrophs growing in adjacent wells by demonstrating that, under the relevant range of parameters, local exchange between auxotrophs is essential for efficient growth. The BioMe plate provides a scalable and flexible approach for the study of dynamic microbial interactions.

3D printed device↗
DOE OSTI2019

Toward a Better Understanding of Species Interactions through Network Biology

Within the last decade, there has been an explosion of multi-omics data generated for several microbial systems. At the same time, new methods of analysis have emerged that are based on inferring networks that link features both within and between species based on correlation in abundance. These developments prompt two important questions. What can be done with network approaches to better understand microbial species interactions? What challenges remain in applying network approaches to query the more complex systems of natural settings? Here, I briefly describe what has been done and what questions still need to be answered. Over the next 5 to 10 years, we will be in a strong position to infer networks that contain multiple kinds of omic data and describe systems with multiple species. These applications will open the door for a better understanding and use of microbiomes across a variety of fields.

Microbiology↗
DOE OSTI2019

Advancing Genome-Resolved Metagenomics beyond the Shotgun

Exploration of environmental microbiomes has shed light on the ecological and evolutionary principles at play in natural ecosystems and has been further accelerated through the reconstruction of population genomes to provide genome-centric context. Yet technical challenges with traditional shotgun metagenomics remain for computationally intense short-read assembly, strain heterogeneity within communities, and depth of coverage required for low-abundance microbes. In this Perspective, we highlight three main avenues for promising future developments, including coupling stable isotope probing and genome-resolved metagenomics, applying fluorescence-activated cell sorting approaches to target mini-metagenomes within a larger community, and utilizing single-molecule long-read and synthetic long-read technology to link mobile elements to host microbial cells. These developments on the horizon will undoubtedly advance genome-resolved metagenomic approaches and enable a better understanding of uncultivated microbes in their natural environments.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2019

RefSoil+: a Reference Database for Genes and Traits of Soil Plasmids

Plasmids harbor transferable genes that contribute to the functional repertoire of microbial communities, yet their contributions to metagenomes are often overlooked. Environmental plasmids have the potential to spread antibiotic resistance to clinical microbial strains. In soils, high microbiome diversity and high variability in plasmid characteristics present a challenge for studying plasmids. To improve the understanding of soil plasmids, we present RefSoil+, a database containing plasmid sequences from 922 soil microorganisms. Soil plasmids were larger than other described plasmids, which is a trait associated with plasmid mobility. There was a weak relationship between chromosome size and plasmid size and no relationship between chromosome size and plasmid number, suggesting that these genomic traits are independent in soil. We used RefSoil+ to inform the distributions of antibiotic resistance genes among soil microorganisms compared to those among nonsoil microorganisms. Soil-associated plasmids, but not chromosomes, had fewer antibiotic resistance genes than other microorganisms. These data suggest that soils may offer limited opportunity for plasmid-mediated transfer of described antibiotic resistance genes. RefSoil+ can serve as a reference for the diversity, composition, and host associations of plasmid-borne functional genes in soil, a utility that will be enhanced as the database expands. Our study improves the understanding of soil plasmids and provides a resource for assessing the dynamics of the genes that they carry, especially genes conferring antibiotic resistances.Soil-associated plasmids have the potential to transfer antibiotic resistance genes from environmental to clinical microbial strains, which is a public health concern. A specific resource is needed to aggregate the knowledge of soil plasmid characteristics so that the content, host associations, and dynamics of antibiotic resistance genes can be assessed and then tracked between the environment and the clinic. Here, we present RefSoil+, a database of soil-associated plasmids. RefSoil+ presents a contemporary snapshot of antibiotic resistance genes in soil that can serve as a reference as novel plasmids and transferred antibiotic resistances are discovered. Our study broadens our understanding of plasmids in soil and provides a community resource of important plasmid-associated genes, including antibiotic resistance genes.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Toward FAIR Representations of Microbial Interactions

Despite an ever-growing number of data sets that catalog and characterize interactions between microbes in different environments and conditions, many of these data are neither easily accessible nor intercompatible. These limitations present a major challenge to microbiome research by hindering the streamlined drawing of inferences across studies.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Metabolic Synergy between Human Symbionts Bacteroides and Methanobrevibacter

Trophic interactions between microbes are postulated to determine whether a host microbiome is healthy or causes predisposition to disease. Two abundant taxa, the Gram-negative heterotrophic bacterium Bacteroides thetaiotaomicron and the methanogenic archaeon Methanobrevibacter smithii, are proposed to have a synergistic metabolic relationship. Both organisms play vital roles in human gut health; B. thetaiotaomicron assists the host by fermenting dietary polysaccharides, whereas M. smithii consumes end-stage fermentation products and is hypothesized to relieve feedback inhibition of upstream microbes such as B. thetaiotaomicron. To study their metabolic interactions, we defined and optimized a coculture system and used software testing techniques to analyze growth under a range of conditions representing the nutrient environment of the host. Here we verify that B. thetaiotaomicron fermentation products are sufficient for M. smithii growth and that accumulation of fermentation products alters secretion of metabolites by B. thetaiotaomicron to benefit M. smithii. Studies suggest that B. thetaiotaomicron metabolic efficiency is greater in the absence of fermentation products or in the presence of M. smithii. Under certain conditions, B. thetaiotaomicron and M. smithii form interspecies granules consistent with behavior observed for syntrophic partnerships between microbes in soil or sediment enrichments and anaerobic digesters. Furthermore, when vitamin B 12 , hematin, and hydrogen gas are abundant, coculture growth is greater than the sum of growth observed for monocultures, suggesting that both organisms benefit from a synergistic mutual metabolic relationship.

59 BASIC BIOLOGICAL SCIENCES↗