Prospective association of the infant gut microbiome with social behaviors in the ECHO consortium.

BACKGROUND: Identifying modifiable risk factors of autism spectrum disorders (ASDs) may inform interventions to reduce financial burden. The infant/toddler gut microbiome is one such feature that has been associated with social behaviors, but results vary between cohorts. We aimed to identify consistent overall and sex-specific associations between the early-life gut microbiome and autism-related behaviors. METHODS: Utilizing the Environmental influences on Children Health Outcomes (ECHO) consortium of United States (U.S.) pediatric cohorts, we gathered data on 304 participants with fecal metagenomic sequencing between 6-weeks to 2-years postpartum (481 samples). ASD-related social development was assessed with the Social Responsiveness Scale (SRS-2). Linear regression, PERMANOVA, and Microbiome Multivariable Association with Linear Models (MaAsLin2) were adjusted for sociodemographic factors. Stratified models estimated sex-specific effects. RESULTS: Genes encoding pathways for synthesis of short-chain fatty acids were associated with higher SRS-2 scores, indicative of ASDs. Fecal concentrations of butyrate were also positively associated with ASD-related SRS-2 scores, some of which may be explained by formula use. LIMITATIONS: The distribution of age at outcome assessment differed in the cohorts included, potentially limiting comparability between cohorts. Stool sample collection methods also differed between cohorts. Our study population reflects the general U.S. population, and thus includes few participants who met the criteria for being at high risk of developing ASD. CONCLUSIONS: Our study is among the first multicenter studies in the U.S. to describe prospective microbiome development from infancy in relation to neurodevelopment associated with ASDs. Our work contributes to clarifying which microbial features associate with subsequent diagnosis of neuropsychiatric outcomes. This will allow for future interventional research targeting the microbiome to change neurodevelopmental trajectories.

Longitudinal effects of prenatal alcohol exposure on visual neurodevelopment over infancy.

Prenatal alcohol exposure (PAE) affects neurodevelopment in over 59 million individuals globally. Prior studies using dichotomous categorization of alcohol use and comorbid substance exposures provide limited knowledge of how prenatal alcohol specifically impacts early human neurodevelopment. In this longitudinal cohort study from Cape Town, South Africa, PAE is measured continuously-characterizing timing, dose, and drinking patterns (i.e., binge drinking). High-density electroencephalography (EEG) during a visual-evoked potential (VEP) task was collected from infants aged 8 to 52 weeks with prenatal exposure exclusively to alcohol and matched on sociodemographic factors to infants with no substance exposure in utero. First trimester alcohol exposure related to altered timing of the P1 VEP component over the first 6 months postnatally, and first trimester binge drinking exposure altered timing of the P1 VEP components such that increased exposure was associated with longer VEP latencies while increasing age was related to shorter VEP latencies (n = 108). These results suggest alcohol exposure in the first trimester may alter visual neurodevelopmental timing in early infancy. Exploratory individual-difference analysis across infants with and without PAE tested the relation between VEP latencies and myelination for a subsample of infants with usable magnetic resonance imaging (MRI) T1w and T2w scans collected at the same time point as EEG (n = 47). Decreased MRI T1w/T2w ratios (an indicator of myelin) in the primary visual cortex (n = 47) were linked to longer P1 VEP latencies. Results from these two sets of analyses suggest that prenatal alcohol and postnatal myelination may both separately impact VEP latency over infancy. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Gut-resident microorganisms and their genes are associated with cognition and neuroanatomy in children.

Emerging evidence implicates gut microbial metabolism in neurodevelopmental disorders, but its influence on typical neurodevelopment has not been explored in detail. We investigated the relationship between the microbiome and neuroanatomy and cognition of 381 healthy children, demonstrating that differences in microbial taxa and genes are associated with overall cognitive function and the size of brain regions. Using a combination of statistical and machine learning models, we showed that species including Alistipes obesi, Blautia wexlerae, and Ruminococcus gnavus were enriched or depleted in children with higher cognitive function scores. Microbial metabolism of short-chain fatty acids was also associated with cognitive function. In addition, machine models were able to predict the volume of brain regions from microbial profiles, and taxa that were important in predicting cognitive function were also important for predicting individual brain regions and specific subscales of cognitive function. These findings provide potential biomarkers of neurocognitive development and may enable development of targets for early detection and intervention.

Role of human milk oligosaccharide metabolizing bacteria in the development of atopic dermatitis/eczema.

Despite affecting up to 20% of infants in the United States, there is no cure for atopic dermatitis (AD), also known as eczema. Atopy usually manifests during the first six months of an infant's life and is one predictor of later allergic health problems. A diet of human milk may offer protection against developing atopic dermatitis. One milk component, human milk oligosaccharides (HMOs), plays an important role as a prebiotic in establishing the infant gut microbiome and has immunomodulatory effects on the infant immune system. The purpose of this review is to summarize the available information about bacterial members of the intestinal microbiota capable of metabolizing HMOs, the bacterial genes or metabolic products present in the intestinal tract during early life, and the relationship of these genes and metabolic products to the development of AD/eczema in infants. We find that specific HMO metabolism gene sets and the metabolites produced by HMO metabolizing bacteria may enable the protective role of human milk against the development of atopy because of interactions with the immune system. We also identify areas for additional research to further elucidate the relationship between the human milk metabolizing bacteria and atopy. Detailed metagenomic studies of the infant gut microbiota and its associated metabolomes are essential for characterizing the potential impact of human milk-feeding on the development of atopic dermatitis.

Microclimate is a strong predictor of the native and invasive plant-associated soil microbiome on San Cristóbal Island, Galápagos archipelago.

Understanding the drivers that affect soil bacterial and fungal communities is essential to understanding and mitigating the impacts of human activity on vulnerable ecosystems like those on the Galápagos Islands. The volcanic slopes of these Islands lead to steep elevation gradients that generate distinct microclimates across small spatial scales. Although much is known about the impacts of invasive plant species on the above-ground biodiversity of the Galápagos Islands, little is known about their resident soil microbial communities and the factors shaping them. Here, we investigate the bacterial and fungal soil communities associated with invasive and native plant species across three distinct microclimates on San Cristóbal Island (arid, transition zone and humid). At each site, we collected soil at three depths (rhizosphere, 5 cm and 15 cm) from multiple plants. Sampling location was the strongest driver of both bacterial and fungal communities, explaining 73% and 43% of variation in the bacterial and fungal community structure, respectively, with additional minor but significant impacts from soil depth and plant type (invasive vs. native). This study highlights the continued need to explore microbial communities across diverse environments and demonstrates how both abiotic and biotic factors impact soil microbial communities in the Galápagos archipelago.

Comparative Analysis of 16S rRNA Gene and Metagenome Sequencing in Pediatric Gut Microbiomes.

The colonization of the human gut microbiome begins at birth, and over time, these microbial communities become increasingly complex. Most of what we currently know about the human microbiome, especially in early stages of development, was described using culture-independent sequencing methods that allow us to identify the taxonomic composition of microbial communities using genomic techniques, such as amplicon or shotgun metagenomic sequencing. Each method has distinct tradeoffs, but there has not been a direct comparison of the utility of these methods in stool samples from very young children, which have different features than those of adults. We compared the effects of profiling the human infant gut microbiome with 16S rRNA amplicon vs. shotgun metagenomic sequencing techniques in 338 fecal samples; younger than 15, 15-30, and older than 30 months of age. We demonstrate that observed changes in alpha-diversity and beta-diversity with age occur to similar extents using both profiling methods. We also show that 16S rRNA profiling identified a larger number of genera and we find several genera that are missed or underrepresented by each profiling method. We present the link between alpha diversity and shotgun metagenomic sequencing depth for children of different ages. These findings provide a guide for selecting an appropriate method and sequencing depth for the three studied age groups.

Targeted High-Resolution Taxonomic Identification of Bifidobacterium longum subsp. infantis Using Human Milk Oligosaccharide Metabolizing Genes.

Bifidobacterium longum subsp. infantis (B. infantis) is one of a few microorganisms capable of metabolizing human breast milk and is a pioneer colonizer in the guts of breastfed infants. One current challenge is differentiating B. infantis from its close relatives, B. longum and B. suis. All three organisms are classified in the same species group but only B. infantis can metabolize human milk oligosaccharides (HMOs). We compared HMO-metabolizing genes across different Bifidobacterium genomes and developed B. infantis-specific primers to determine if the genes alone or the primers can be used to quickly characterize B. infantis. We showed that B. infantis is uniquely identified by the presence of five HMO-metabolizing gene clusters, tested for its prevalence in infant gut metagenomes, and validated the results using the B. infantis-specific primers. We observed that only 15 of 203 (7.4%) children under 2 years old from a cohort of US children harbored B. infantis. These results highlight the importance of developing and improving approaches to identify B. infantis. A more accurate characterization may provide insights into regional differences of B. infantis prevalence in infant gut microbiota.

Family SES Is Associated with the Gut Microbiome in Infants and Children.

BACKGROUND: While early life exposures such as mode of birth, breastfeeding, and antibiotic use are established regulators of microbiome composition in early childhood, recent research suggests that the social environment may also exert influence. Two recent studies in adults demonstrated associations between socioeconomic factors and microbiome composition. This study expands on this prior work by examining the association between family socioeconomic status (SES) and host genetics with microbiome composition in infants and children. METHODS: Family SES was used to predict a latent variable representing six genera abundances generated from whole-genome shotgun sequencing. A polygenic score derived from a microbiome genome-wide association study was included to control for potential genetic associations. Associations between family SES and microbiome diversity were assessed. RESULTS: Anaerostipes, Bacteroides, Eubacterium, Faecalibacterium, and Lachnospiraceae spp. significantly loaded onto a latent factor, which was significantly predicted by SES (p < 0.05) but not the polygenic score (p > 0.05). Our results indicate that SES did not predict alpha diversity but did predict beta diversity (p < 0.001). CONCLUSIONS: Our results demonstrate that modifiable environmental factors influence gut microbiome composition at an early age. These results are important as our understanding of gut microbiome influences on health continue to expand.

The Abundance of Human Milk Oligosaccharide (HMO)-Metabolizing Genes in Fecal Samples from Six-Month-Old Human Infants.

Herein, we report the abundance and prevalence of HMO-metabolizing genes, specifically those of Bifidobacterium infantis, in fecal samples from human infants. Forty dyads were enrolled, and each mother collected a fecal sample from her infant at six months of age. Genomic DNA was extracted, and quantitative real-time PCR was used to determine gene abundance. The mode of delivery was not associated with gene abundance. Several gene regions, Sia (a sialidase), B. inf (16S), and GH750 (a glycoside hydrolase), were more abundant in the feces of human milk-fed infants (p < 0.05). Others, Sia and HC bin (16S), tended to be less abundant when a larger percentage of an infant's diet consisted of solids (p < 0.10). When accounting for solid food intake, human milk exposure was positively associated with Sia and B. inf (p < 0.05) and tended to be related to the abundance of the GH750 and HC bin (p < 0.10) gene regions. With further development and validation in additional populations of infants, these assays could be used to group samples by dietary exposure even where no record of dietary intake exists. Thus, these assays would provide a method by which infant human milk intake can be assessed quickly in any well-equipped molecular biology laboratory.

Organic Electron Donors and Terminal Electron Acceptors Structure Anaerobic Microbial Communities and Interactions in a Permanently Stratified Sulfidic Lake.

The extent to which nutrients structure microbial communities in permanently stratified lakes is not well understood. This study characterized microbial communities from the anoxic layers of the meromictic and sulfidic Fayetteville Green Lake (FGL), NY, United States, and investigated the roles of organic electron donors and terminal electron acceptors in shaping microbial community structure and interactions. Bacterial communities from the permanently stratified layer below the chemocline (monimolimnion) and from enrichment cultures inoculated by lake sediments were analyzed using 16S rRNA gene sequencing. Results showed that anoxygenic phototrophs dominated microbial communities in the upper monimolimnion (21 m), which harbored little diversity, whereas the most diverse communities resided at the bottom of the lake (∼52 m). Organic electron donors explained 54% of the variation in the microbial community structure in aphotic cultures enriched on an array of organic electron donors and different inorganic electron acceptors. Electron acceptors only explained 10% of the variation, but were stronger drivers of community assembly in enrichment cultures supplemented with acetate or butyrate compared to the cultures amended by chitin, lignin or cellulose. We identified a range of habitat generalists and habitat specialists in both the water column and enrichment samples using Levin's index. Network analyses of interactions among microbial groups revealed Chlorobi and sulfate reducers as central to microbial interactions in the upper monimolimnion, while Syntrophaceae and other fermenting organisms were more important in the lower monimolimnion. The presence of photosynthetic microbes and communities that degrade chitin and cellulose far below the chemocline supported the downward transport of microbes, organic matter and oxidants from the surface and the chemocline. Collectively, our data suggest niche partitioning of bacterial communities via interactions that depend on the availability of different organic electron donors and terminal electron acceptors. Thus, light, as well as the diversity and availability of chemical resources drive community structure and function in FGL, and likely in other stratified, meromictic lakes.

Biotic and Environmental Drivers of Plant Microbiomes Across a Permafrost Thaw Gradient.

Plant-associated microbiomes are structured by environmental conditions and plant associates, both of which are being altered by climate change. The future structure of plant microbiomes will depend on the, largely unknown, relative importance of each. This uncertainty is particularly relevant for arctic peatlands, which are undergoing large shifts in plant communities and soil microbiomes as permafrost thaws, and are potentially appreciable sources of climate change feedbacks due to their soil carbon (C) storage. We characterized phyllosphere and rhizosphere microbiomes of six plant species, and bulk peat, across a permafrost thaw progression (from intact permafrost, to partially- and fully-thawed stages) via 16S rRNA gene amplicon sequencing. We tested the hypothesis that the relative influence of biotic versus environmental filtering (the role of plant species versus thaw-defined habitat) in structuring microbial communities would differ among phyllosphere, rhizosphere, and bulk peat. Using both abundance- and phylogenetic-based approaches, we found that phyllosphere microbial composition was more strongly explained by plant associate, with little influence of habitat, whereas in the rhizosphere, plant and habitat had similar influence. Network-based community analyses showed that keystone taxa exhibited similar patterns with stronger responses to drivers. However, plant associates appeared to have a larger influence on organisms belonging to families associated with methane-cycling than the bulk community. Putative methanogens were more strongly influenced by plant than habitat in the rhizosphere, and in the phyllosphere putative methanotrophs were more strongly influenced by plant than was the community at large. We conclude that biotic effects can be stronger than environmental filtering, but their relative importance varies among microbial groups. For most microbes in this system, biotic filtering was stronger aboveground than belowground. However, for putative methane-cyclers, plant associations have a stronger influence on community composition than environment despite major hydrological changes with thaw. This suggests that plant successional dynamics may be as important as hydrological changes in determining microbial relevance to C-cycling climate feedbacks. By partitioning the degree that plant versus environmental filtering drives microbiome composition and function we can improve our ability to predict the consequences of warming for C-cycling in other arctic areas undergoing similar permafrost thaw transitions.

Light-driven anaerobic microbial oxidation of manganese.

Oxygenic photosynthesis supplies organic carbon to the modern biosphere, but it is uncertain when this metabolism originated. It has previously been proposed1,2 that photosynthetic reaction centres capable of splitting water arose by about 3 billion years ago on the basis of the inferred presence of manganese oxides in Archaean sedimentary rocks. However, this assumes that manganese oxides can be produced only in the presence of molecular oxygen3, reactive oxygen species4,5 or by high-potential photosynthetic reaction centres6,7. Here we show that communities of anoxygenic photosynthetic microorganisms biomineralize manganese oxides in the absence of molecular oxygen and high-potential photosynthetic reaction centres. Microbial oxidation of Mn(II) under strictly anaerobic conditions during the Archaean eon would have produced geochemical signals identical to those used to date the evolution of oxygenic photosynthesis before the Great Oxidation Event1,2. This light-dependent process may also produce manganese oxides in the photic zones of modern anoxic water bodies and sediments.

An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen Erwinia tracheiphila.

Erwinia tracheiphila is the causal agent of bacterial wilt of cucurbits, an economically important phytopathogen affecting an economically important phytopathogen affecting few cultivated Cucurbitaceae few cultivated Cucurbitaceae host plant species in temperate eastern North America. However, essentially nothing is known about E. tracheiphila population structure or genetic diversity. To address this shortcoming, a representative collection of 88 E. tracheiphila isolates was gathered from throughout its geographic range, and their genomes were sequenced. Phylogenomic analysis revealed three genetic clusters with distinct hrpT3SS virulence gene repertoires, host plant association patterns, and geographic distributions. Low genetic heterogeneity within each cluster suggests a recent population bottleneck followed by population expansion. We showed that in the field and greenhouse, cucumber (Cucumis sativus), which was introduced to North America by early Spanish conquistadors, is the most susceptible host plant species and the only species susceptible to isolates from all three lineages. The establishment of large agricultural populations of highly susceptible C. sativus in temperate eastern North America may have facilitated the original emergence of E. tracheiphila into cucurbit agroecosystems, and this introduced plant species may now be acting as a highly susceptible reservoir host. Our findings have broad implications for agricultural sustainability by drawing attention to how worldwide crop plant movement, agricultural intensification, and locally unique environments may affect the emergence, evolution, and epidemic persistence of virulent microbial pathogens.IMPORTANCEErwinia tracheiphila is a virulent phytopathogen that infects two genera of cucurbit crop plants, Cucurbita spp. (pumpkin and squash) and Cucumis spp. (muskmelon and cucumber). One of the unusual ecological traits of this pathogen is that it is limited to temperate eastern North America. Here, we complete the first large-scale sequencing of an E. tracheiphila isolate collection. From phylogenomic, comparative genomic, and empirical analyses, we find that introduced Cucumis spp. crop plants are driving the diversification of E. tracheiphila into multiple lineages. Together, the results from this study show that locally unique biotic (plant population) and abiotic (climate) conditions can drive the evolutionary trajectories of locally endemic pathogens in unexpected ways.

Stressing Escherichia coli to educate students about research: A CURE to investigate multiple levels of gene regulation.

Course-based undergraduate research experiences (CUREs) have been shown to increase student retention and learning in the biological sciences. Most CURES cover only one aspect of gene regulation, such as transcriptional control. Here we present a new inquiry-based lab that engages understanding of gene expression from multiple perspectives. Students carry out a forward genetic screen to identify regulators of the stationary phase master regulator RpoS in the model organism Escherichia coli and then use a series of reporter fusions to determine if the regulation is at the level of transcription or the post-transcription level. This easy-to-implement course has been run both as a 9-week long project and a condensed 5-6 week version in three different schools and types of courses. A majority of the genes found in the screen are novel, thus giving students the opportunity to contribute to original findings to the field. Assessments of this CURE show student gains in learning in many knowledge areas. In addition, attitudinal surveys suggest the students are enthusiastic about the screen and their learning about gene regulation. In summary, this lab would be an appropriate addition to an intermediate or advanced level Molecular Biology, Genetics, or Microbiology curriculum. © 2017 by The International Union of Biochemistry and Molecular Biology, 45(5):449-458, 2017.

Microbiology and ecology are vitally important to premedical curricula.

Despite the impact of the human microbiome on health, an appreciation of microbial ecology is yet to be translated into mainstream medical training and practice. The human microbiota plays a role in the development of the immune system, in the development and function of the brain, in digestion, and in host defense, and we anticipate that many more functions are yet to be discovered. We argue here that without formal exposure to microbiology and ecology-fields that explore the networks, interactions and dynamics between members of populations of microbes-vitally important links between the human microbiome and health will be overlooked. This educational shortfall has significant downstream effects on patient care and biomedical research, and we provide examples from current research highlighting the influence of the microbiome on human health. We conclude that formally incorporating microbiology and ecology into the premedical curricula is invaluable to the training of future health professionals and critical to the development of novel therapeutics and treatment practices.

Differentiation of salivary bacterial profiles of subjects with periodontitis and dental caries.

Bacterial profiles of saliva in subjects with periodontitis and dental caries have been demonstrated to differ from that of oral health. The aim of this comparative analysis of existing data generated by the Human Oral Microbe Identification Microarray (HOMIM) from 293 stimulated saliva samples was to compare bacterial profiles of saliva in subjects with periodontitis and dental caries.

Beta-diversity metrics of the upper digestive tract microbiome are associated with body mass index.

OBJECTIVE: Studies of the fecal microbiome have implicated the gut microbiota in obesity, but few studies have examined the microbial diversity at other sites. The association between obesity and the upper gastrointestinal (UGI) microbial diversity was explored. METHODS: The UGI microbiome of 659 healthy Chinese adults with a measured body mass index (BMI) range of 15.0 to 35.7 was characterized using the 16S rRNA gene DNA microarray (HOMIM). RESULTS: In multivariate-adjusted models, alpha diversity was not associated with BMI. However, beta diversity, assessed by principal coordinate vectors generated from an unweighted UniFrac distance matrix of pairwise comparisons, was associated with BMI (third and fourth vectors, P = 0.01 and P = 0.03, respectively). Moreover, beta diversity, assessed by cluster membership (three clusters), was also associated with BMI; individuals in the first cluster [median BMI 22.35, odds ratio (OR) = 0.48, 95% confidence interval (CI) = 0.05-4.34] and second cluster [median BMI 22.55, OR = 0.26, 95% CI = 0.09-0.75] were significantly less likely to be obese (BMI ≥ 27.5) than those in the third cluster (median BMI 23.59). CONCLUSIONS: A beta-diversity metric of the UGI microbiome is associated with a four fold difference in obesity risk in this Asian population. Future studies should address whether the UGI microbiome plays a causal role in obesity.

Association between tobacco use and the upper gastrointestinal microbiome among Chinese men.

PURPOSE: Tobacco causes many adverse health conditions and may alter the upper gastrointestinal (UGI) microbiome. However, the few studies that studied the association between tobacco use and the microbiome were small and underpowered. Therefore, we investigated the association between tobacco use and the UGI microbiome in Chinese men. METHODS: We included 278 men who underwent esophageal cancer screening in Henan Province, China. Men were categorized as current, former, or never smokers from questionnaire data. UGI tract bacterial cells were characterized using the Human Oral Microbial Identification Microarray. Counts of unique bacterial species and genera estimated alpha diversity. For beta diversity, principal coordinate (PCoA) vectors were generated from an unweighted UniFrac distance matrix. Polytomous logistic regression models were used for most analyses. RESULTS: Of the 278 men in this study, 46.8% were current smokers and 12.6% were former smokers. Current smokers tended to have increased alpha diversity (mean 42.3 species) compared to never smokers (mean 38.9 species). For a 10 species increase, the odds ratio (OR) for current smoking was 1.29 (95% CI 1.04-1.62). Beta diversity was also associated with current smoking. The first two PCoA vectors were strongly associated with current smoking (PCoA1 OR 0.66; 95% CI 0.51-0.87; PCoA2 OR 0.73; 95% CI 0.56-0.95). Furthermore, Dialister invisus and Megasphaera micronuciformis were more commonly detected in current smokers than in never smokers. CONCLUSIONS: Current smoking was associated with both alpha and beta diversity in the UGI tract. Future work should consider how the UGI microbiome is associated with smoking-related diseases.

The association between the upper digestive tract microbiota by HOMIM and oral health in a population-based study in Linxian, China.

BACKGROUND: Bacteria affect oral health, but few studies have systematically examined the role of bacterial communities in oral diseases. We examined this relationship in a large population-based Chinese cancer screening cohort. METHODS: Human Oral Microbe Identification Microarrays were used to test for the presence of 272 human oral bacterial species (97 genera) in upper digestive tract (UDT) samples collected from 659 participants. Oral health was assessed using US NHANES (National Health and Nutrition Examination Survey) protocols. We assessed both dental health (total teeth missing; tooth decay; and the decayed, missing, and filled teeth (DMFT) score) and periodontal health (bleeding on probing (BoP) extent score, loss of attachment extent score, and a periodontitis summary estimate). RESULTS: Microbial richness, estimated by number of genera per sample, was positively correlated with BoP score (P = 0.015), but negatively correlated with tooth decay and DMFT score (P = 0.008 and 0.022 respectively). Regarding ß-diversity, as estimated by the UniFrac distance matrix for pairwise differences among samples, at least one of the first three principal components of the UniFrac distance matrix was correlated with the number of missing teeth, tooth decay, DMFT, BoP, or periodontitis. Of the examined genera, Parvimonas was positively associated with BoP and periodontitis. Veillonellacease [G-1] was associated with a high DMFT score, and Filifactor and Peptostreptococcus were associated with a low DMFT score. CONCLUSIONS: Our results suggest distinct relationships between UDT microbiota and dental and periodontal health. Poor dental health was associated with a less microbial diversity, whereas poor periodontal health was associated with more diversity and the presence of potentially pathogenic species.

Consumption of atmospheric hydrogen during the life cycle of soil-dwelling actinobacteria.

Microbe-mediated soil uptake is the largest and most uncertain variable in the budget of atmospheric hydrogen (H2 ). The diversity and ecophysiological role of soil microorganisms that can consume low atmospheric abundances of H2 with high-affinity [NiFe]-hydrogenases is unknown. We expanded the library of atmospheric H2 -consuming strains to include four soil Harvard Forest Isolate (HFI) Streptomyces spp., Streptomyces cattleya and Rhodococcus equi by assaying for high-affinity hydrogenase (hhyL) genes and quantifying H2 uptake rates. We find that aerial structures (hyphae and spores) are important for Streptomyces H2 consumption; uptake was not observed in S. griseoflavus Tu4000 (deficient in aerial structures) and was reduced by physical disruption of Streptomyces sp. HFI8 aerial structures. H2 consumption depended on the life cycle stage in developmentally distinct actinobacteria: Streptomyces sp. HFI8 (sporulating) and R. equi (non-sporulating, non-filamentous). Strain HFI8 took up H2 only after forming aerial hyphae and sporulating, while R. equi only consumed H2 in the late exponential and stationary phase. These observations suggest that conditions favouring H2 uptake by actinobacteria are associated with energy and nutrient limitation. Thus, H2 may be an important energy source for soil microorganisms inhabiting systems in which nutrients are frequently limited.