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DOE OSTI2025

Redox Homeostasis as a Key Regulator of Intramolecular Cyclization in Fungal Perylenequinones

Perylenequinones (PQs) such as hypocrellins and hypomycins are fungal-derived redox-active metabolites with known roles as photosensitizers in the oxidative stress response and applications in photodynamic therapy (PDT). Here, we report that Shiraia sp., a filamentous fungus, can survive and grow under strictly anaerobic (argon) conditions─an unexpected finding for a multicellular eukaryote. Modulating redox homeostasis through chemical reduction and oxygen limitation promotes the intramolecular cyclization of hypocrellins, enhancing hypomycin biosynthesis. Moisture content further influences these transformations, with high water levels favoring keto–enol tautomerization and dry, reducing environments promoting hydride substitution at the peripheral positions. These findings highlight redox modulation as a key driver of perylenequinone metabolism and suggest that PQs may contribute to maintaining redox balance under anaerobic stress, hinting at a broader role in oxygen-independent adaptation in filamentous fungi. This work offers new insights at the interface of redox biology, chemical signaling, and fungal metabolism, with potential implications for the stability and function of PQ-based PDT agents in hypoxic, reducing conditions such as tumor microenvironments.

cyclization↗

DOE OSTI2024

Metagenomic clustering links specific metabolic functions to globally relevant ecosystems

ABSTRACT Metagenomic sequencing has advanced our understanding of biogeochemical processes by providing an unprecedented view into the microbial composition of different ecosystems. While the amount of metagenomic data has grown rapidly, simple-to-use methods to analyze and compare across studies have lagged behind. Thus, tools expressing the metabolic traits of a community are needed to broaden the utility of existing data. Gene abundance profiles are a relatively low-dimensional embedding of a metagenome’s functional potential and are, thus, tractable for comparison across many samples. Here, we compare the abundance of KEGG Ortholog Groups (KOs) from 6,539 metagenomes from the Joint Genome Institute’s Integrated Microbial Genomes and Metagenomes (JGI IMG/M) database. We find that samples cluster into terrestrial, aquatic, and anaerobic ecosystems with marker KOs reflecting adaptations to these environments. For instance, functional clusters were differentiated by the metabolism of antibiotics, photosynthesis, methanogenesis, and surprisingly GC content. Using this functional gene approach, we reveal the broad-scale patterns shaping microbial communities and demonstrate the utility of ortholog abundance profiles for representing a rapidly expanding body of metagenomic data. IMPORTANCE Metagenomics, or the sequencing of DNA from complex microbiomes, provides a view into the microbial composition of different environments. Metagenome databases were created to compile sequencing data across studies, but it remains challenging to compare and gain insight from these large data sets. Consequently, there is a need to develop accessible approaches to extract knowledge across metagenomes. The abundance of different orthologs (i.e., genes that perform a similar function across species) provides a simplified representation of a metagenome’s metabolic potential that can easily be compared with others. In this study, we cluster the ortholog abundance profiles of thousands of metagenomes from diverse environments and uncover the traits that distinguish them. This work provides a simple to use framework for functional comparison and advances our understanding of how the environment shapes microbial communities.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2023

Uncovering a miltiradiene biosynthetic gene cluster in the Lamiaceae reveals a dynamic evolutionary trajectory

The spatial organization of genes within plant genomes can drive evolution of specialized metabolic pathways. Terpenoids are important specialized metabolites in plants with diverse adaptive functions that enable environmental interactions. Here, we report the genome assemblies of Prunella vulgaris, Plectranthus barbatus, and Leonotis leonurus. We investigate the origin and subsequent evolution of a diterpenoid biosynthetic gene cluster (BGC) together with other seven species within the Lamiaceae (mint) family. Based on core genes found in the BGCs of all species examined across the Lamiaceae, we predict a simplified version of this cluster evolved in an early Lamiaceae ancestor. The current composition of the extant BGCs highlights the dynamic nature of its evolution. We elucidate the terpene backbones generated by the Callicarpa americana BGC enzymes, including miltiradiene and the terpene (+)-kaurene, and show oxidization activities of BGC cytochrome P450s. Our work reveals the fluid nature of BGC assembly and the importance of genome structure in contributing to the origin of metabolites.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Permafrost microbial communities and functional genes are structured by latitudinal and soil geochemical gradients

Permafrost underlies approximately one quarter of Northern Hemisphere terrestrial surfaces and contains 25–50% of the global soil carbon (C) pool. Permafrost soils and the C stocks within are vulnerable to ongoing and future projected climate warming. The biogeography of microbial communities inhabiting permafrost has not been examined beyond a small number of sites focused on local-scale variation. Permafrost is different from other soils. Perennially frozen conditions in permafrost dictate that microbial communities do not turn over quickly, thus possibly providing strong linkages to past environments. Thus, the factors structuring the composition and function of microbial communities may differ from patterns observed in other terrestrial environments. Here, we analyzed 133 permafrost metagenomes from North America, Europe, and Asia. Permafrost biodiversity and taxonomic distribution varied in relation to pH, latitude and soil depth. The distribution of genes differed by latitude, soil depth, age, and pH. Genes that were the most highly variable across all sites were associated with energy metabolism and C-assimilation. Specifically, methanogenesis, fermentation, nitrate reduction, and replenishment of citric acid cycle intermediates. This suggests that adaptations to energy acquisition and substrate availability are among some of the strongest selective pressures shaping permafrost microbial communities. The spatial variation in metabolic potential has primed communities for specific biogeochemical processes as soils thaw due to climate change, which could cause regional- to global- scale variation in C and nitrogen processing and greenhouse gas emissions.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS1990

Metabolic and morphologic properties of single muscle fibers in the rat after spaceflight, Cosmos 1887

The adaptation of a slow (soleus, Sol) and a fast (medial gastrocnemius, MG) skeletal muscle to spaceflight was studied in five young male rats. The flight period was 12.5 days and the rats were killed approximately 48 h after returning to 1 g. Five other rats that were housed in cages similar to those used by the flight rats were maintained at 1 g for the same period of time to serve as ground-based controls. Fibers were classified as dark or light staining for myosin adenosine triphosphatase (ATPase). On the average, the fibers in the Sol of the flight rats atrophied twice as much as those in the MG. Further, the fibers located in the deep (close to the bone and having the highest percentage of light ATPase and high oxidative fibers in the muscle cross section) region of the MG atrophied more than the fibers located in the superficial (away from the bone and having the lowest percentage of light ATPase and high oxidative fibers in the muscle cross-section) region of the muscle. Based on quantitative histochemical assays of single muscle fibers, succinate dehydrogenase (SDH) activity per unit volume was unchanged in fibers of the Sol and MG. However, in the Sol, but not the MG, the total amount of SDH activity in a 10-microns-thick section of a fiber decreased significantly in response to spaceflight. Based on population distributions, it appears that the alpha-glycerophosphate dehydrogenase (GPD) activities were elevated in the dark ATPase fibers in the Sol, whereas the light fibers in the Sol and both fiber types in the MG did not appear to change. The ratio of GPD to SDH activities increased in the dark (but not light) fibers of the Sol and was unaffected in the MG. Immunohistochemical analyses indicate that approximately 40% of the fibers in the Sol of flight rats expressed a fast myosin heavy chain compared with 22% in control rats. Further, 31% of the fibers in the Sol of flight rats expressed both fast and slow myosin heavy chains compared with 8% in control rats. Immunohistochemical changes in the MG were minimal. These data suggest that the magnitude and direction of enzymatic activity and cell volume changes are dependent on the muscle, the region of the muscle, and the type of myosin expressed in the fibers. Further, the ability of fibers to maintain normal or even elevated activities per unit volume of some metabolic enzymes is remarkable considering the marked and rapid decrease in fiber volume.

NASA Experiment Number COS 1887-26↗

DOE OSTI2022

The Complete Genome Sequence and Structure of the Oleaginous Rhodococcus opacus Strain PD630 Through Nanopore Technology

Rhodococcus bacterial strains are characterized by wide metabolic versatility and extraordinary resistance to environmental stresses. The high versatility and adaptability of Rhodococcus strains is partly related with large and complex genomes (up to 10.1 Mbp) including high genetic redundancy and the presence of several circular and linear (mega)plasmids, which harbour peculiar catabolic and biosynthetic genes. Within Rhodococcus genus, R. opacus strain PD630 is considered a model oleaginous strain for its ability to produce and accumulate lipids (mostly triacyglycerols, TAGs) using different carbon sources, including low-cost and renewable resources such as lignocellulose. Notably, under specific growth conditions, this strain is capable of accumulating up to 80% of its cellular dry weight in TAGs; that is a rare feature in the prokaryotic and eukaryotic kingdoms. Multi-omic approaches have been applied to obtain system-level information about metabolic and regulatory pathways involved in these biosynthetic processes. Novel molecular tools for genome editing (CRISPR/Cas9 and recombineering) have been recently developed highlighting the possible utilization of R. opacus PD630 as synthetic biology platform for lipids production.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

Rewiring Aromatic Compound Consumption: Chromosomal Amplification and Evolution of a Foreign Pathway in Acinetobacter baylyi ADP1

Rational engineering strategies that seek to harness the remarkable diversity of microbial metabolism can be limited by incomplete biological knowledge. As described here, a novel approach to address this challenge involved replacing a native pathway for degrading lignin-derived aromatic compounds via ortho cleavage of protocatechuate in Acinetobacter baylyi ADP1 with a foreign meta-cleavage pathway that uses different enzymes, metabolites, and redox carriers. This alteration may improve lignin valorization and coordinate catabolism with bioproduction strategies. When a 14-kbp region of foreign DNA was inserted in the chromosome, the heterologous genes failed to confer growth on target substrates. Regional gene dosage was increased using a synthetic DNA fragment to promote recombination, and higher copy number enabled growth. During adaptive laboratory evolution, compensatory mutations arose that permit growth with one copy of the foreign genes. This complex metabolic remodeling was accomplished without assumptions about the impediments that initially prevented growth. To understand the changes that emerged, a novel transformation assay identified a combination of mutations sufficient for the new phenotype. Three unexpected changes were revealed: loss of one foreign enzyme, loss of one native enzyme, and loss of a two-component transcriptional regulatory system. This study establishes that large multicopy tandem arrays of poorly adapted pathway genes can confer new functions and improve understanding of metabolism.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗

DOE OSTI2021

Elucidating gene expression adaptation of phylogenetically divergent coral holobionts under heat stress

As coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbiont duo during heat stress. Our results stress the importance of integrative and comparative approaches across a wide range of species to better understand coral survival under the predicted rise in sea surface temperatures.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Mycobacterium tuberculosis CitA activity is modulated by cysteine oxidation and pyruvate binding

As an adaptation for survival during infection, Mycobacterium tuberculosis becomes dormant, reducing its metabolism and growth. Two types of citrate synthases have been identified in Mycobacterium tuberculosis, GltA2 and CitA. Previous work shows that overexpression of CitA, the secondary citrate synthase, stimulates the growth of Mycobacterium tuberculosis under hypoxic conditions without showing accumulation of triacylglycerols and makes mycobacteria more sensitive to antibiotics, suggesting that CitA may play a role as a metabolic switch during infection and may be an interesting TB drug target. To assess the druggability and possible mechanisms of targeting CitA with small-molecule compounds, the CitA crystal structure was solved to 2.1 Å by X-ray crystallography. The solved structure shows that CitA lacks an NADH binding site that would afford allosteric regulation, which is atypical of most citrate synthases. However, a pyruvate molecule is observed within the analogous domain, suggesting pyruvate may instead be the allosteric regulator for CitA. Further, the R149 and R153 residues forming the charged portion of the pyruvate binding pocket were mutated to glutamate and methionine, respectively, to assess the effect of mutations on activity. Protein thermal shift assay shows thermal stabilization of CitA in the presence of pyruvate compared to the two CitA variants designed to decrease pyruvate affinity. Solved crystal structures of both variants show no significant structural changes. However, the catalytic efficiency of the R153M variant increases by 2.6-fold. Additionally, we show that covalent modification of C143 of CitA by Ebselen completely arrests enzyme activity. Similar inhibition is observed using two spirocyclic Michael acceptor containing compounds, which inhibit CitA with IC app 50 values of 6.6 and 10.9 μM. A crystal structure of CitA modified by Ebselen was solved, but significant structural changes were lacking. Considering that covalent modification of C143 inactivates CitA and the proximity of C143 to the pyruvate binding site, this suggests that structural and/or chemical changes in this sub-domain are responsible for regulating CitA enzymatic activity.

60 APPLIED LIFE SCIENCES↗

NASA NTRS1992

Fuel utilization during exercise after 7 days of bed rest

Energy yield from carbohydrate, fat, and protein during physical activity is partially dependent on an individual's fitness level. Prolonged exposure to microgravity causes musculoskeletal and cardiovascular deconditioning; these adaptations may alter fuel utilization during space flight. Carbohydrate and fat metabolism during exercise were analyzed before and after 7 days of horizontal bed rest.

Barrows, Linda H.↗

DOE OSTI2021

Non-structural carbohydrates mediate seasonal water stress across Amazon forests

Non-structural carbohydrates (NSC) are major substrates for plant metabolism and have been implicated in mediating drought-induced tree mortality. Despite their significance, NSC dynamics in tropical forests remain little studied. We present leaf and branch NSC data for 82 Amazon canopy tree species in six sites spanning a broad precipitation gradient. During the wet season, total NSC (NSC T ) concentrations in both organs were remarkably similar across communities. However, NSC T and its soluble sugar (SS) and starch components varied much more across sites during the dry season. Notably, the proportion of leaf NSC T in the form of SS (SS:NSC T ) increased greatly in the dry season in almost all species in the driest sites, implying an important role of SS in mediating water stress in these sites. This adjustment of leaf NSC balance was not observed in tree species less-adapted to water deficit, even under exceptionally dry conditions. Thus, leaf carbon metabolism may help to explain floristic sorting across water availability gradients in Amazonia and enable better prediction of forest responses to future climate change.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2024

Metabolic Costs of Walking with Weighted Vests

ABSTRACT Introduction The US Army Load Carriage Decision Aid (LCDA) metabolic model is used by militaries across the globe and is intended to predict physiological responses, specifically metabolic costs, in a wide range of dismounted warfighter operations. However, the LCDA has yet to be adapted for vest-borne load carriage, which is commonplace in tactical populations, and differs in energetic costs to backpacking and other forms of load carriage. Purpose The purpose of this study is to develop and validate a metabolic model term that accurately estimates the effect of weighted vest loads on standing and walking metabolic rate for military mission-planning and general applications. Methods Twenty healthy, physically active military-age adults (4 women, 16 men; age, 26 ± 8 yr old; height, 1.74 ± 0.09 m; body mass, 81 ± 16 kg) walked for 6 to 21 min with four levels of weighted vest loading (0 to 66% body mass) at up to 11 treadmill speeds (0.45 to 1.97 m·s −1 ). Using indirect calorimetry measurements, we derived a new model term for estimating metabolic rate when carrying vest-borne loads. Model estimates were evaluated internally byk-fold cross-validation and externally against 12 reference datasets (264 total participants). We tested if the 90% confidence interval of the mean paired difference was within equivalence limits equal to 10% of the measured walking metabolic rate. Estimation accuracy, precision, and level of agreement were also evaluated by the bias, standard deviation of paired differences, and concordance correlation coefficient (CCC), respectively. Results Metabolic rate estimates using the new weighted vest term were statistically equivalent (P< 0.01) to measured values in the current study (bias, −0.01 ± 0.54 W·kg −1 ; CCC, 0.973) as well as from the 12 reference datasets (bias, −0.16 ± 0.59 W·kg −1 ; CCC, 0.963). Conclusions The updated LCDA metabolic model calculates accurate predictions of metabolic rate when carrying heavy backpack and vest-borne loads. Tactical populations and recreational athletes that train with weighted vests can confidently use the simplified LCDA metabolic calculator provided as Supplemental Digital Content to estimate metabolic rates for work/rest guidance, training periodization, and nutritional interventions.

Sport Sciences↗

DOE OSTI2022

Genome sequence, phylogenetic analysis, and structure-based annotation reveal metabolic potential of Chlorella sp. SLA-04

Algae are a broad class of photosynthetic eukaryotes that are phylogenetically and physiologically diverse. Most of the phylogenetic diversity has been inferred from 18S rDNA sequencing since there are only a few complete genomes available in public databases. Here we use ultra-long-read Nanopore sequencing to determine a gapless, telomere-to-telomere complete genome sequence of Chlorella sp. SLA-04, previously described as Chlorella sorokiniana SLA-04. Chlorella sp. SLA-04 is a green alga that grows to high cell density in a wide variety of environments - high and neutral pH, high and low alkalinity, and high and low salinity. SLA-04's ability to grow in high pH and high alkalinity media without external CO 2 supply is favorable for large-scale algal biomass production. Phylogenetic analysis performed using ribosomal DNA and conserved protein sequences consistently reveal that Chlorella sp. SLA-04 forms a distinct lineage from other strains of Chlorella sorokiniana. We complement traditional genome annotation methods with high throughput structural predictions and demonstrate that this approach expands functional prediction of the SLA-04 proteome. Genomic analysis of the SLA-04 genome identifies the genes capable of utilizing TCA cycle intermediates to replenish cytosolic acetyl-CoA pools for lipid production. We also identify a complete metabolic pathway for sphingolipid anabolism that may allow SLA-04 to readily adapt to changing environmental conditions and facilitate robust cultivation in mass production systems. Altogether, this work clarifies the phylogeny of Chlorella sp. SLA-04 within Trebouxiophyceae and demonstrates how structural predictions can be used to improve annotation beyond sequencebased methods.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

Knocking out the carboxyltransferase interactor 1 (CTI1) in Chlamydomonas boosted oil content by fivefold without affecting cell growth

Summary The first step in chloroplast de novo fatty acid synthesis is catalysed by acetyl‐CoA carboxylase (ACCase). As the rate‐limiting step for this pathway, ACCase is subject to both positive and negative regulation. In this study, we identify a Chlamydomonas homologue of the plant carboxyltransferase interactor 1 (CrCTI1) and show that this protein interacts with the Chlamydomonas α‐carboxyltransferase (Crα‐CT) subunit of the ACCase by yeast two‐hybrid protein–protein interaction assay. Three independent CRISPR‐Cas9 mediated knockout mutants for CrCTI1 each produced an ‘enhanced oil’ phenotype, accumulating 25% more total fatty acids and storing up to fivefold more triacylglycerols (TAGs) in lipid droplets. The TAG phenotype of the crcti1 mutants was not influenced by light but was affected by trophic growth conditions. By growing cells under heterotrophic conditions, we observed a crucial function of CrCTI1 in balancing lipid accumulation and cell growth. Mutating a previously mapped in vivo phosphorylation site (CrCTI1 Ser108 to either Ala or to Asp), did not affect the interaction with Crα‐CT. However, mutating all six predicted phosphorylation sites within Crα‐CT to create a phosphomimetic mutant reduced this pairwise interaction significantly. Comparative proteomic analyses of the crcti1 mutants and WT suggested a role for CrCTI1 in regulating carbon flux by coordinating carbon metabolism, antioxidant and fatty acid β‐oxidation pathways, to enable cells to adapt to carbon availability. Taken together, this study identifies CrCTI1 as a negative regulator of fatty acid synthesis in algae and provides a new molecular brick for the genetic engineering of microalgae for biotechnology purposes.

Li, Zhongze [Aix‐Marseille Université, CEA, CNRS, ↗

NASA NTRS1973

Weightlessness

Weightlessness effects on physiological systems are summarized, including cardiovascular responses, hematological effects, work capacity (exercise tolerance), respiratory responses, skeletal responses, neuromuscular changes, vestibular responses, metabolism, endocrine and electrolyte responses, and weight loss. The nature of the adaptive response to space flight and microbial changes are also discussed. The effects of zero gravity upon performance are ascertained, and the physiological effects of weightlessness are counteracted.

Charles Berry↗

NASA NTRS2003

Nitric oxide in microgravity-induced orthostatic intolerance: relevance to spinal cord injury

Prolonged exposure to microgravity results in cardiovascular deconditioning which is marked by orthostatic intolerance in the returning astronauts and recovering bed-ridden patients. Recent studies conducted in our laboratories at University of California, Irvine have revealed marked elevation of nitric oxide (NO) production in the kidney, heart, brain, and systemic arteries coupled with significant reduction of NO production in the cerebral arteries of microgravity-adapted animals. We have further demonstrated that the observed alteration of NO metabolism is primarily responsible for the associated cardiovascular deconditioning. Recovery from acute spinal cord injury (SCI) is frequently complicated by orthostatic intolerance that is due to the combined effects of the disruption of efferent sympathetic pathway and cardiovascular deconditioning occasioned by prolonged confinement to bed. In this presentation, I will review the nature of altered NO metabolism and its role in the pathogenesis of microgravity-induced cardiovascular deconditioning. The possible relevance of the new findings to orthostatic intolerance in patients with acute SCI and its potential therapeutic implications will be discussed.

Review↗

NASA NTRS1994

Neuromuscular adaptation to actual and simulated weightlessness

The chronic "unloading" of the neuromuscular system during spaceflight has detrimental functional and morphological effects. Changes in the metabolic and mechanical properties of the musculature can be attributed largely to the loss of muscle protein and the alteration in the relative proportion of the proteins in skeletal muscle, particularly in the muscles that have an antigravity function under normal loading conditions. These adaptations could result in decrements in the performance of routine or specialized motor tasks, both of which may be critical for survival in an altered gravitational field, i.e., during spaceflight and during return to 1 G. For example, the loss in extensor muscle mass requires a higher percentage of recruitment of the motor pools for any specific motor task. Thus, a faster rate of fatigue will occur in the activated muscles. These consequences emphasize the importance of developing techniques for minimizing muscle loss during spaceflight, at least in preparation for the return to 1 G after spaceflight. New insights into the complexity and the interactive elements that contribute to the neuromuscular adaptations to space have been gained from studies of the role of exercise and/or growth factors as countermeasures of atrophy. The present chapter illustrates the inevitable interactive effects of neural and muscular systems in adapting to space. It also describes the considerable progress that has been made toward the goal of minimizing the functional impact of the stimuli that induce the neuromuscular adaptations to space.

Non-NASA Center↗

DOE OSTI2024

From wolves to humans: oral microbiome resistance to transfer across mammalian hosts

The mammalian mouth is colonized by complex microbial communities, adapted to specific niches, and in homeostasis with the host. Individual microbes interact metabolically and rely primarily on nutrients provided by the host, with which they have potentially co-evolved along the mammalian lineages. The oral environment is similar across mammals, but the diversity, specificity, and evolution of community structure in related or interacting mammals are little understood. Here, we compared the oral microbiomes of dogs with those of wild wolves and humans. In dogs, we found an increased microbial diversity relative to wolves, possibly related to the transition to omnivorous nutrition following domestication. This includes a larger diversity of Patescibacteria than previously reported in any other oral microbiota. The oral microbes are most distinct at bacterial species or strain levels, with few if any shared between humans and canids, while the close evolutionary relationship between wolves and dogs is reflected by numerous shared taxa. More taxa are shared at higher taxonomic levels including with humans, supporting their more ancestral common mammalian colonization followed by diversification. Phylogenies of selected oral bacterial lineages do not support stable human-dog microbial transfers but suggest diversification along mammalian lineages (apes and canids). Therefore, despite millennia of cohabitation and close interaction, the host and its native community controls and limits the assimilation of new microbes, even if closely related. Higher resolution metagenomic and microbial physiological studies, covering a larger mammalian diversity, should help understand how oral communities assemble, adapt, and interact with their hosts.

59 BASIC BIOLOGICAL SCIENCES↗